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Neurons in cat primary auditory cortex sensitive to correlates of auditory motion in three-dimensional… Stumpf, Erika 1990

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N E U R O N S I N C A T P R I M A R Y A U D I T O R Y C O R T E X S E N S I T I V E T O C O R R E L A T E S O F A U D I T O R Y M O T I O N I N T H R E E - D I M E N S I O N A L S P A C E by E r i k a Stumpf B . S c , M c G i l l Universi ty, 1988 A T H E S I S S U B M I T T E D I N P A R T I A L F U L F I L L M E N T O F T H E R E Q U I R E M E N T S F O R T H E D E G R E E O F M A S T E R O F A R T S i n T H E F A C U L T Y O F G R A D U A T E S T U D I E S (Department of Psychology) We accept this thesis as conforming to the required standard T H E U N I V E R S I T Y O F B R I T I S H C O L U M B I A August 1990 © E r i k a Stumpf 1990 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department or by his or her representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of P&fCAAO(&$M The University of British Columbia Vancouver, Canada Date AugUSt- B, !W0 DE-6 (2/88) i i ABSTRACT The pr imary auditory cortex (area A l ) plays an important role i n the localization of static sound sources. However, l i t t le is known concerning how i t processes information about sound source motion. This study was undertaken to investigate the responses of single neurons i n the pr imary auditory cortex of the cat to correlates of auditory motion i n space. Diotic and dichotic changes i n sound intensity presented through earphones simulated auditory motion i n four directions: toward and away from the receiver along the midl ine, into the ipsi lateral hemifield and into the contralateral hemifield. Different rates of intensity change simulated sound source velocity. Results indicate that A l neurons can be highly selective to intensity correlates of auditory motion. Three major classes of neurons were encountered: neurons sensitive to motion toward or away from the receiver, neurons sensitive to ipsi lateral- or contralateral-directed motion, and monaural-l ike neurons. The different classes of direction-selective neurons were spatially segregated from each other and appeared to occur i n clusters or columns i n the cortex. In addition to their selectivity for different directions of simulated sound source motion, A l neurons also responded selectively to the rate and excursion of intensity changes, a correlate of sound source velocity. The major determinants of direction and velocity selectivity were interactions between the following response properties of A l neurons: b inaura l interaction type, ear dominance, on/off responses, and monotonicity of rate/intensity function. These findings suggest that neural processing of auditory motion may involve neural mechanisms distinct from those involved i n static sound localization, and indicate that some neurons i n the pr imary auditory cortex may be part of a specialized motion-detecting mechanism i n the auditory system. i i i TABLE OF CONTENTS A B S T R A C T i i L I S T O F F I G U R E S iv I N T R O D U C T I O N 1 Sound l o c a l i z a t i o n 1 A u d i t o r y sys tem 4 P r i m a r y audi tory cortex 8 The role of the pr imary auditory cortex i n the encoding of sound source loca t i on 9 R e a l and s imula ted movement 12 Implementa t ion and predict ions 15 M E T H O D S 18 A n i m a l p repa ra t ion 18 S t i m u l i 19 C a l i b r a t i o n 22 D a t a co l lec t ion 22 D a t a ana lys i s 23 R E S U L T S 25 D i r e c t i o n a l se lec t iv i ty 25 A . M o t i o n i n depth 27 B . M o t i o n i n a z i m u t h 38 C . M o n a u r a l - l i k e un i t s 44 D . D i s t r i bu t ion of un i t types 48 V e l o c i t y se lec t iv i ty 48 Effect of changing frequency GO D I S C U S S I O N 61 Mechanisms of direction and velocity selectivity 61 A . M o t i o n i n depth 61 B . M o t i o n i n a z i m u t h 62 C . M o n a u r a l - l i k e un i t s 63 D . Ve loc i ty select ivi ty 63 E . A model for direction and velocity selectivity 64 T e c h n i c a l considerat ions 66 Ana log ies to v i s i o n 68 Specialized motion-detecting mechanisms i n the auditory system? 69 R E F E R E N C E S 74 i v LIST OF FIGURES Figure 1 Ascend ing audi tory pathways 6 Figure 2 B i n a u r a l in te rac t ion classes 10 Figure 3 S t i m u l u s condi t ions 20 Figure 4 Summary of directional preferences for population of neurons encountered 26 Figure 5 Post-st imulus t ime histograms: toward-preferring neuron 28 Figure 6 Po la r plots: toward-preferring neurons 30 Figure 7 Post-s t imulus time histograms: away-preferring neuron 33 Figure 8 Po la r plots: away-preferr ing neurons 34 Figure 9 Plot of preferred direction of motion i n depth versus response to b i n a u r a l onset and offset 35 Figure 10 Plot of breadth of tuning for motion i n depth versus binaural i n t e r a c t i o n 37 Figure 11 Post-st imulus time histograms: ipsi lateral-preferring neuron... 39 Figure 12 Po la r plots: azimuth-preferr ing neurons 40 Figure 13 Plot of preferred direction of motion i n az imuth versus ear dominance 43 Figure 14 Post-s t imulus time histograms: monaural - l ike neuron 45 Figure 15 Po la r plots: monaura l - l ike neurons 47 Figure 16 Schematic electrode penetrations 49 Figure 17 Polar plots and rate/intensity functions: monotonic, velocity-dependent u n i t 51 Figure 18 Polar plots and rate/intensity functions: non-monotonic, velocity-dependent un i t 54 Figure 19 Polar plots and rate/intensity functions: idiosyncratic uni t 56 V Figure 20 Polar plots: and rate/intensity functions: velocity-independent u n i t 58 Figure 21 Mode l of direction and velocity selectivity 65 1 EmtODUCTION One role of sensory systems is to convey information to l i v ing organisms about s t imul i i n the environment. L i v i n g organisms are equipped wi th receptor end-organs specialized to transduce physical s t imul i of a specific sensory modali ty into electrical impulses; these signals from the receptor organs are then relayed to the central nervous system, where they undergo extensive processing. The result of this signal processing provides organisms wi th information concerning the nature of s t imul i i n the environment (what), and the location of these s t imul i wi th respect to the organism (where). The focus of this research is the latter aspects of sensory processing, and more precisely on the role of the auditory cortex i n the localization of sound sources moving i n space. Sound localization The receptor organs of the v isual , auditory and somatosensory systems i n mammals follow a specific arrangement: re t inal ganglion cells, cochlear hai r cells and cutaneous receptors are organized i n an orderly array or sensory epithelium. The spatial organization of the sensory epithelium i n these three systems is preserved i n the projections to the central nervous system, i n a so-called point-to-point projection: receptors from neighboring regions of sensory epi thel ium project to neighboring regions of sensory cortex. In the visual and somatosensory systems, this arrangement preserves information about the location of s t imul i i n space. In the visual system, portions of the ret ina receive input from specific parts of the visual field, and i n tu rn project to distinct areas of v i sua l cortex; a s imi lar arrangement exists i n the somatosensory system. Therefore, spatial information is preserved i n the ascending v isua l and somatosensory pathways and is directly available i n the cortex by virtue of 2 retinotopic and somatotopic projections. This does not hold for the auditory system. The sensory epithelium of the auditory system is the basilar membrane located i n the cochlea of the inner ear. The basilar membrane codes for sound source frequency (pitch) along its length, and the receptor organs (the hair cells of the organ of Corti) also have an orderly spatial arrangement: ha i r cells located at the base of the basilar membrane respond to h igh frequency sound, and those located at the apex respond to low frequency sound. This arrangement is due to the mechanical properties of the membrane itself. This tonotopic organization is preserved i n the projections of the auditory pathway to various brainstem nuclei and most areas of the auditory cortex. Al though frequency coding provides crucial information about the nature of auditory s t imul i , i t gives no information about the spatial location of such s t imul i because sound sources from a l l directions impinge on a common sensory epi thel ium extended i n frequency rather than space. Information about sound source location must then be computed and extracted by the central nervous system. Organisms equipped w i t h two auditory end-organs can solve the problem of sound localization: the pr incipal cues for sound localization are differences i n the signals reaching the two ears. These binaural cues depend on the spatial location and frequency spectrum of the sound source, and on the size and shape of the receiver's head. The distance between the two ears imposes an interaural t ime difference (ITD) on ar r iv ing s t imul i , result ing i n in teraural disparities i n transient a r r iva l time and i n on-going phase. ITDs are important i n localizing low frequency sound sources (below about 1500 H z i n humans). The acoustic shadow of the head and pinnae generate interaural intensity differences (IID) which are useful i n localizing h igh frequency sound sources (above 1500 Hz) . This so-called duplex theory of sound localization describes accurately how 3 mammals localize pure tones, us ing temporal cues for the lower portion of the audible spectrum and intensive cues for the higher portion (Stevens & Newman, 1936). Another consequence of the shadowing effect of the head and pinnae is the creation of in teraural frequency disparities (IFD), which may be helpful for local izing complex broadband sound sources (Mendelson & Cynader, 1983). The external ear (pinna) also plays an important role i n sound localization. In addition to generating interaural intensity differences, the convolutions of the pinnae and the resonances i n the ear canal differentially amplify or dampen certain frequencies, result ing i n a transformation of the frequency spectrum from the free sound field to the eardrum (Calford & Pettigrew, 1984; Phi l l ips , Calford, Pettigrew, A i t k i n , & Semple, 1982; Shaw, 1974). This cue is especially important i n localizing broadband sound wi th h igh frequency components and is thought to underlie vert ical sound localization (Brown, Schessler, Moody & Stebbins, 1982; But ler , 1969; Middlebrooks, Makous, & Green, 1989) and the resolution of front-to-back ambiguities (Musicant & Butler , 1984). A l l the b inaura l sound localization cues l is ted above (ITD, IID and IFD) can be generated wi th the head i n a fixed position. However, head movements are widely used by animals attempting to locate a sound source. Head movements produce a series of changing binaural cues which l i m i t the possible positions of a sound source relative to the receiver (Mi l l s , 1972) and significantly improve localizat ion accuracy i n humans (Thurlow, Mangels , & Runge, 1967; Thur low & Runge, 1967). In addition to moving the head, animals wi th moveable pinnae frequently use p inna movements when local iz ing sound sources. Because most electrophysiological and psychophysical studies focus on static localization cues, the importance of head movements i n sound localization is usual ly overlooked. 4 Interaural intensity differences show marked dependence on the frequency and azimuthal location of the sound source (Irvine, 1987; M a r t i n & Webster, 1989). The IID/azimuth function is monotonic for the frontal region of space (within about 45 degrees of the midline on either side) and is frequency dependent, being steepest at high frequencies (8 k H z i n the cat). This agrees well w i th psychophysical data which shows that localization acuity i n cats and monkeys is greatest for high frequency sounds (Mar t in & Webster, 1987; Casseday & Neff, 1973) and for s t imul i located close to the midline (Brown et al . , 1982; Heffner & Heffner, 1988). Interaural time differences are also frequency dependent although this effect is relatively independent of the pinnae. As i n the case of IIDs, ITDs generated by sound sources close to the midl ine provide useful localization cues (Roth, Kochhar, & H i n d , 1980). Local izat ion of sound sources implies extracting information about the spatial location of s t imul i largely from the binaural cues generated by that source. However this process can be reversed: presenting b inaura l sound localization cues through earphones produces a fused auditory image located wi th in the head instead of i n the free acoustic field, and listeners can locate the sound source accordingly. This task is called lateral izat ion (in contrast wi th the usual task of localization). The binaural temporal and intensive disparities that are thought to underlie sound localization of pure tones can be used to lateralize tonal s t imul i ; localization and lateral izat ion acuity are s imilar , suggesting that s imi la r mechanisms underlie local iz ing in ternal and external sound sources (Jeffress & Taylor, 1961). Moreover, the lateralization acuities of cats and humans are comparable (Wakeford & Robinson, 1974; Yost, 1974). Auditory system The organization of the central auditory system is more complex than that 5 of other sensory systems: i n contrast w i th the somatosensory system where information can reach the cortex wi th as few as two synapses, or the visual system where there is only one major relay nucleus, information from the hai r cells i n the inner ear passes through several nuclei before reaching the auditory cortex, and the interconnections between the various nuclei are intricate. Several distinct auditory areas exist at the level of the cortex. In addition, paral lel descending pathways add to the complexity of this system. A simplified scheme of the ascending auditory pathway is shown on figure 1. Neurons wi th cell bodies i n the spiral ganglion synapse wi th the hai r cells of the organ of Cort i ; the axons form the auditory nerve (the auditory part of the eighth cranial nerve) and terminate i n the dorsal and ventral divisions of the cochlear nucleus. F r o m the cochlear nucleus, fibers ascend i n the dorsal acoustic str ia (stria of Monakow) and the intermediate str ia of H e l d to the contralateral la tera l lemniscus and inferior colliculus, sending collaterals along the way to brainstem nuclei. Fibers from the cochlear nucleus also ascend i n the trapezoid body, sending collaterals to the superior olivary complex of the brainstem before synapsing cont ra la te ra l^ i n the lateral lemniscus and/or the inferior colliculus. The medial superior olive is part icular ly noteworthy: i t is the first nucleus i n the ascending auditory pathway which receives input from both ears. Fibers from the superior olivary complex project bi lateral ly to the lateral lemniscus and the inferior colliculus. The latter is the midbra in auditory area; i t sends fibers to the thalamic auditory nucleus (the medial geniculate body), which i n tu rn projects to the auditory cortex. Al though ascending projections from the cochlear nucleus are largely contralateral, there are significant crossed connections from the level of the lateral lemniscus upward, that the inferior colliculus, the medial geniculate body and the auditory cortex a l l receive binaural information. Ascending projections preserve the tonotopic organization of the 6 Figure 1. Schematic representation of the mammal ian ascending auditory pathways. D C N : dorsal cochlear nucleus; V C N : ventral cochlear nucleus; L S O : lateral superior olive; M S O : medial superior olive; N T B : nucleus of the trapezoid body; L L : la teral lemniscus; IC: inferior colliculus; M G : medial geniculate nucleus of the thalamus; S H : stria of He ld ; S M : s tr ia of Monakow (from Mol ler , 1983). 7 cochlea so that frequency coding is present at a l l levels of the auditory pathway. The auditory cortex is made up of several distinct auditory areas. In the cat, as many as eight distinct fields have been identified, and about a th i rd of the auditory cortex is non-tonotopically organized (Reale & Imig, 1980). The most prominent are the pr imary and secondary auditory fields ( A l and A l l ) , the anterior auditory field (AAF) , and the posterior and ventroposterior auditory fields ( P A F and V P A F ) . Contrary to what its name may imply, the pr imary auditory cortex is not the only site receiving direct thalamic input; rather, several paral lel projections run from the medial geniculate body to the different auditory fields so the a l l fields receive equally direct thalamic input. There are two largely segregated thalamocortical auditory projection systems i n the cat: a tonotopic projection to A l , A A F , P A F and V P A F , and a non-tonotopic projection to A l l and other secondary regions (Andersen, Knigh t , & Merzenich, 1980). In addition, various intracort ical and interhemispheric connections also exist (Brugge & Imig, 1978; Matsubara & Phi l l ips , 1988). A l l nuclei of the ascending pathway receive input from higher levels. The descending auditory pathway of made up of two systems: the corticothalamic system which terminates i n the medial geniculate body, and the corticocochlear system which is a widely distributed network of connections to a l l nuclei of the ascending pathway, extending to the cochlear ha i r cells (Harr ison & Howe, 1975). The descending pathways are thought to exert an inhibi tory influence of the activity of the ascending pathway. A salient feature of signal processing i n the auditory system (which is probably true of other sensory systems as well) is its increasing complexity as one ascends the auditory pathway. The many nuclei of the ascending auditory pathway are not mere relays; signals from the cochlear hai r cells are extensively processed. In the inner ear and auditory nerve, one can record the cochlear 8 microphonic, an electrical potential which faithfully reproduces the waveform of a sound wi th l i t t le distortion. Neurons at lower levels of the pathway respond throughout the length of the stimulus; these sustained responses are gradually replaced by transient responses at higher levels, and are v i r tua l ly absent from the cortex. Bra ins tem auditory neurons show phase-locking; again, these responses gradually disappear at the level of the midbrain and are absent i n the thalamus and cortex. In the auditory cortex, rapidly adapting neurons predominate; transient excitatory responses are common and responses to sound offset also appear. Cort ical neurons also respond wel l to frequency and amplitude modulated sound (Mendelson & Cynader, 1985; Ph i l l i p s , Mendelson, Cynader, & Douglas, 1985; Schreiner & Urbas, 1988). Overal l , neurons i n lower auditory centers show l i t t le adaptation; i n higher centers and especially i n the cortex, neurons show more adaptation, g iving more transient responses, a greater variety of response patterns and strong excitatory and inhibi tory responses. Cor t ica l neurons respond best to change and show rapid adaptation; the increasing complexity i n signal processing i n the ascending auditory pathway allows these neurons to enhance change, and i n turn , neuronal adaptation saves channel capacity i n the cortex (Moller, 1983). Primary auditory cortex Information about sound source frequency is preserved i n the pr imary auditory cortex. Area A l is tonotopically arranged: isofrequency bands run dorsoventrally, w i t h h igh frequencies located rostral ly and low frequencies more caudally (Merzenich, Knight , & Roth, 1975; Ph i l l ips & Irvine, 1981a). Neurons i n area A l are sharply tuned to sound frequency; i n addition, neurons found wi th in the same perpendicular penetration show s imi la r frequency tuning, which is evidence for some form of columnar organization i n the auditory cortex wi th 9 respect to frequency (Merzenich et a l . , 1975). There is also a gradient for breadth of frequency tuning i n A l : neurons i n the dorsal part show narrower frequency tuning and those i n more ventral locations are more broadly tuned (Schreiner & Cynader, 1984). The rate/intensity functions of the responses of pr imary auditory neurons can be monotonic or non-monotonic, although the latter are less frequent (Phil l ips & Irvine, 1981a). Most neurons i n A l respond wel l to st imulation of the contralateral ear, and respond differently to monaural and binaural s t imulat ion. The responses of A l neurons to b inaura l st imulation can be classified i n one of three functional categories: 1- E E units (excitatory/excitatory) i n which the response evoked by st imulat ion of the dominant ear is facilitated by simultaneous st imulat ion of the other ear; 2- E I and I E units (excitatory/inhibitory and vice versa) i n which the response evoked by st imulation of the dominant ear is inhibi ted by simultaneous st imulat ion of the other ear; 3- E O units (monaural) i n which the response evoked by st imulat ion of one ear is unaffected by binaural s t imulat ion (Imig & A d r i a n , 1977; figure 2). Neurons found along the same electrode penetration tend to display s imi lar b inaura l interactions, suggesting that area A l is organized i n vert ical b inaura l interaction columns. These columns are grouped together i n bands which are oriented orthogonal to the isofrequency bands (Middlebrooks, Dykes, & Merzenich, 1980). The role of the primary auditory cortex in the encoding of sound source location Three kinds of experiments have attempted to delineate the role of the pr imary auditory cortex i n sound localization: electrophysiological experiments us ing sealed systems to present binaural sound localization cues, electrophysiological experiments using free-field s t imul i , and studies of sound localization behavior following selective cortical lesions. The first type of 10 Binaural interaction types 100 80 60 40 20 0 EE EI IE EO contralateral ear stimulation ipsilateral ear stimulation binaural stimulation Figure 2. B inau ra l interaction classes of pr imary auditory cortex neurons. E E : excitatory/excitatory (binaural facilitation); E I : excitatory/inhibitory (contralateral-ear-dominated w i t h b inaural inhibit ion); I E : inhibitory/excitatory (ipsilateral-ear-dominated w i t h b inaura l inhibition); E O : monaural (no binaural interaction). 11 experiments has demonstrated that neurons i n the pr imary auditory cortex of the cat are sensitive to binaural sound localization cues (IIDs, ITDs, and IFDs) corresponding to the frontal and contralateral regions of auditory space (Brugge, Dubrovsky, A i t k i n , & Anderson, 1969; Kitzes , Wrege, & Cassady, 1980; Mendelson & Cynader, 1983; Phi l l ips & Irvine, 1981b; Reale & Kettner, 1986). The selectivity of A l neurons to interaural time, intensity and frequency differences is related to b inaura l response category. Preferences for IIDs and ITDs seem to result from the interaction of excitatory and/or inhibitory events evoked by s t imulat ion of each ear; the binaural response i n such cells is dependent on the t iming of the sequence of excitatory and inhibitory events at the site of interaction, which i n tu rn depends on stimulus intensity (Brugge et a l . , 1969; Ki tzes et a l . , 1980). Free-field studies have demonstrated that A l neurons are sensitive to the spatial location of pure tone and noise s t imul i . Aga in , A l neurons seem to respond best to sound sources located i n the frontal and contralateral sound fields (Eisenman, 1974; Benson, Hienz, & Goldstein, 1981). Middlebrooks and Pettigrew (1981) have proposed that pr imary auditory neurons can be classified i n one of three classes of spatial receptive fields based on their sensitivity to st imulus location: hemifield units, which respond to sound i n the contralateral sound hemifield; ax ia l units, which respond to sound i n the acoustic axis of the contralateral pinna; and omnidirectional units , which respond to sound from any direction i n front of the animal . These auditory spatial receptive fields are computational: they are not derived from a point-to-point map from the inner ear to the cortex but are computed from comparisons of the signals at the two ears. However, despite the existence of location-sensitive units i n the pr imary auditory cortex of the cat, there is no indication of a systematic map of auditory space i n area A l (Middlebrooks & Pettigrew, 1981). 1 2 Lesion to the pr imary auditory cortex spare intensity and frequency discr iminat ion abilities but produce permanent sound localization deficits i n the sound field contralateral to the lesion. This conclusion has been reached i n studies wi th cats (Jenkins & Masterton, 1982), dogs (Heffher, 1978) and monkeys (Heffner & Masterton, 1975). Comparisons between lesions to area A l and to other auditory cortical fields indicate that among other auditory cortical fields, integri ty of area A l is necessary and sufficient for normal b inaura l sound localization behavior. Area A l i n each hemisphere contributes p r imar i ly to location representation i n the contralateral sound field (Phil l ips & Gates, 1982; Jenkins & Merzenich, 1984). The sensitivity of auditory neurons to binaural sound localization cues and to the spatial location of sound sources, and the importance of the pr imary auditory cortex for accurate sound localization indicate that area A l of the auditory cortex plays an essential role i n directional hearing. Real and simulated auditory movement A l l of the research cited above has been carried out using stationary sound sources, or correlates of such sounds. Yet , a conspicuous feature of auditory s t imul i i n the environment is their motion wi th respect to the receiver. Despite this prominence, auditory movement as a st imulus feature has largely been overlooked by most investigators of the psychophysics and neurophysiology of sound localizat ion. Al though much progress has been made i n understanding static sound localization, l i t t le is known about how the auditory system extracts information about st imulus motion. As sound sources move across the auditory field, they provide the auditory system w i t h a series of changing binaural disparities. In part icular, movement of a sound source i n az imuth produces modulations of in teraural differences i n 1 3 intensity, on-going phase and frequency spectrum; the rate of change i n these binaural cues is a correlate of sound source velocity. Therefore i t is possible to simulate sound source movement without actually providing real motion, by presenting correlates of motion (modulated IIDs, ITDs and IFDs) to a listener v ia earphones or speakers; dichotic modulations of both ITDs and IIDs can produce simulated auditory motion, and subjects can lateralize such s t imul i . Briggs and Perrott (1972), and Perrott (1974) demonstrated auditory apparent movement by presenting human subjects w i t h dichotic noise s t imul i of vary ing interst imulus onset. A t optimal interst imulus onset, subjects perceived two sounds as one continuous moving sound; these findings concerning auditory motion perception coincided wi th those obtained from free-field studies. However, the temporal disparities used i n this study to simulate auditory motion (tens or hundreds of milliseconds) were not faithful representations of the actual temporal cues used by the auditory system for sound localization, which are i n the order of tenths of milliseconds. A l t a i a n and Viskov (1977) used continuous modulations of in teraural phase differences i n a dichotic paradigm (click trains of vary ing interaural t ime delays) to simulate auditory motion; these s t imul i were derived from actual ITDs generated by sound sources moving i n azimuth. Such s t imul i produced a fused auditory image (FAI) which moved wi th in the head, and evoked a distinct sensation of auditory motion i n human subjects. In addition, subjects could make velocity discriminations based on perceived F A I movement. Gran tham (1984, 1986) came to s imilar conclusions by presenting subjects wi th amplitude modulated narrow-band noise v ia distant speakers to simulate horizontal auditory motion. In an attempt to delineate the role of the auditory cortex i n localizing moving sound sources, A l t m a n and Ka lmykova (1986) lesioned the auditory cortex of dogs and tested their subsequent abil i ty to lateralize signals s imulat ing 14 auditory movement. Bi la te ra l lesions completely eliminated the abil i ty to discriminate the direction of simulated auditory motion, and uni la teral lesions produced a lateralization deficit on the side contralateral to the lesion. These lesion effects parallel those found wi th static s t imul i (Jenkins & Masterton, 1982; Heffner, 1978; Heffner & Masterton, 1975). However, because different regions of auditory cortex were not selectively lesioned, no conclusions could be drawn regarding which auditory field i n part icular is involved i n processing of information about stimulus motion. Al though these findings have not been replicated i n free-field situations, they s t i l l highlight the importance of the auditory cortex for dynamic sound localization. Because neurons i n the pr imary auditory cortex are sensitive to the location of sound sources but show rapid adaptation to static s t imul i , one might expect that some neurons i n area A l would respond wel l to sound source movement w i th in their spatial receptive fields. Also , given the fact that A l neurons are sharply tuned to b inaura l disparities corresponding to certain sound source locations, and given the propensity of auditory cortical neurons for change, one could presume that the direction and rate of change of binaural disparities (which are correlates of direction and velocity of auditory motion, respectively) could evoke strong responses from these neurons. Surprisingly, there are few reports of sensitivity to movement of sound sources by neurons of the auditory cortex. Sovijarvi and Hyvar inen (1974) presented continuous pure tones moving horizontally and vertically i n a free field situation, and found neurons i n the pr imary auditory cortex of the cat which were sensitive to the direction of sound source movement. A l t m a n (1987) studied the responses of A l neurons to modulations of interaural phase disparity i n a sealed system, and found neurons which responded selectively to the direction of phase change, a correlate of sound source motion i n azimuth. These two reports were the first to 15 point to the existence of motion detecting mechanisms i n the auditory cortex. However, i n neither report was the degree of directional selectivity quantified or further analyzed i n terms of possible underlying mechanisms. In addition, relatively few motion-sensitive units were reported, an indication that such units i n the pr imary auditory cortex of the cat may be relatively rare, as opposed to the more common location-sensitive units (Middlebrooks & Pettigrew, 1981). The a im of this study is twofold: to confirm and assess the existence and prevalence of motion-sensitive neurons i n the pr imary auditory cortex of the cat, and to investigate the mechanisms underlying this sensitivity to auditory motion i n terms of known response characteristics of auditory cortical neurons. Implementation and predictions As previously mentioned, moving sound sources produce a series of changing b inaura l disparities. One correlate of auditory motion i n space is modulation of sound intensity at the receiver's ears. When a sound source moves toward or away from the receiver along the midline, the two ears receive correlated (diotic) increases or decreases i n sound intensity. When a sound source moves across the receiver's auditory field along the horizontal plane, the two ears receive opposite-directed (dichotic) changes i n sound intensity: sound intensity increases i n one ear and simultaneously decreases i n the other ear. Presenting these diotic and dichotic changes i n intensity at the two ears through earphones produces a s imulat ion of auditory motion: a fused auditory image appears to move wi th in the head, as was produced by A l t a i a n and Viskov (1977) wi th modulations of interaural time delay. To determine the sensitivity of auditory neurons to modulated IIDs, one can present this correlate of sound source motion directly into the ears of an animal and simultaneously record the electrical activity of A l neurons evoked by this stimulus. 16 Presenting modulated in teraural intensity differences through earphones can simulate motion of real world sound sources without actually providing that motion. This paradigm has advantages and shortcomings. One obvious l imi ta t ion of using earphones instead of free-field s t imul i is the fact that the modifying effects of the head and pinnae on the incoming signal are bypassed altogether. This results i n a stimulus containing less information, because some sound localization cues normally present i n the free sound field are missing. Another l imi ta t ion is due to the signal itself: modulations of IIDs as the only auditory motion cue is an incomplete st imulus. U s i n g the same paradigm but adding other motion cues to the stimulus (modulations of frequency spectrum, time of a r r iva l and on-going phase) would produce a more accurate s imulat ion of auditory motion. In turn, a more complete stimulus may help uncover a neural mechanism specialized to detect moving sound sources by providing additional information to such a system. The l imitat ions of this paradigm may result i n perceptual ambiguities: for example, i t is impossible for a receiver to dist inguish between the intensity changes associated wi th sound source movement toward or away from the receiver and actual modulation of the intensity of a stationary sound source. O n a more positive side, modulations of IIDs produce an appropriate (albeit simplified) s imulat ion of sound source movement that can be easily implemented i n a calibrated, sealed sound delivery system. In addition, presenting only one motion cue eliminates possible interactions among stimulus parameters and facilitates the interpretation of results. Aside from responses to intensity correlates of auditory motion, other response characteristics of A l neurons w i l l be investigated: aural dominance, b inaura l interaction category, transient on and off responses, and monotonicity of the rate/intensity function. F r o m these response characteristics, some predictions can be made regarding selectivity to direction of auditory motion: 1-17 neurons w i l l prefer simulated auditory motion into the hemifield corresponding to the dominant ear; 2- neurons wi th facilitatory b inaural interactions w i l l prefer simulated auditory motion toward the receiver; 3- neurons wi th inhibi tory b inaura l interactions w i l l prefer simulated auditory motion i n azimuth, away from the ear producing inhibi t ion and toward the ear producing excitation; 4-neurons wi th off responses w i l l prefer simulated auditory motion i n directions opposite those specified above; 5- a neuron's preference for slow or fast simulated auditory motion w i l l depend on the monotonicity of its rate/intensity function. These predictions w i l l be verified, along wi th possible interactions among the response characteristics of the units encountered and their resul t ing sensitivity and selectivity to direction of simulated auditory motion. 1 8 METHODS Animal preparation Acute experiments were performed on 7 healthy adult cats. Surgical anesthesia was induced wi th sodium pentothal (10 mg/kg i.v. in i t ia l ly) ; additional doses were administered during surgery to main ta in areflexia. To prevent excessive salivation and respiratory difficulties, a single dose of atropine sulfate (0.2 mg, i.v.) was administered. Dexamethasone (0.5 mg, i.m.) was administered to prevent bra in edema. A tracheotomy was performed and an endotracheal tube inserted. The animal was supported by a head-holder which left the skul l and pinnae free from obstruction. The sku l l and auditory meatuses were cleared of surrounding tissue. A 5-mm diameter hole was dr i l led i n the skul l overlying the left ectosylvian gyrus (area A l ) , and the intact dura was covered wi th petroleum jel ly to keep i t from drying. The auditory meatuses were transected and the pinnae reflected anteriorly to allow insertion of the stimulus delivery system (hollow a luminum acoustic couplers) directly into the ear canals. A l l wounds and pressure points were infi l t rated wi th a long-acting local anesthetic (bupivacaine hydrochloride 2.5%). When surgery was completed, sodium pentothal anesthesia was discontinued. The an imal was paralyzed (gallamine triethiodide 20 mg, i.v.) and art if icially respired wi th a 70:30 mixture of nitrous oxide and oxygen. The an imal was maintained on a continuous intravenous infusion of gallamine triethiodide (10 mg/kg/hr), sodium pentobarbital (1 mg/kg/hr) and 5% lactated dextrose (10 ml/hr) i n Ringer's. End- t ida l CO2, heart rate, blood pressure and E E G were monitored continuously. Rectal temperature was maintained at 38°C using a feedback-controlled heating blanket; expired CO2 was maintained at about 4% by adjusting the rate of the respiration pump. 19 Stimuli Pure tone sinusoids were generated by a Wavetek model 110 function generator. Signals to the speakers were controlled by two digital-to-analog converters of the PDP/11 computer, and fed through an analog mul t ip l ier and an amplifier (Technics SU-700 stereo integrated amplifier). The st imulus delivery system consisted of two loudspeakers (Pioneer WXX-172) connected to hollow a luminum acoustic couplers which fitted snugly into the transected auditory meatuses. The s t imul i employed were amplitude modulated pure tones which simulated auditory motion i n four canonical directions. Like-directed changes i n sound intensity at both ears simulated movement toward or away from the head along the midl ine; opposite-directed changes i n sound intensity simulated sound moving along the azimuthal plane, toward one ear and away from the other, and vice versa (figure 3A, B) . Since the duration of the A M ramp was constant at 250 msec, A M ramp rate and excursion i n these experiments are correlates of sound source velocity: increased ramp excursion and rate correspond to higher velocities of sound source motion. Each of the four simulated directions of motion was presented at four different rates of rise of the A M ramp; the four different intensity levels spanned 24 dB, i n four 6 dB increments (figure 3C). The s t imul i were shaped wi th envelope generators to produce rise and fall times of 5 ms; interaural phase was always zero. St imulus time course is shown on figure 3D. St imulus onset occurred at 150 msec and was followed by a 295 ms plateau; the A M ramps s imulat ing auditory motion occurred between 450 and 700 msec, and were followed by another 295 ms plateau and st imulus offset at 1000 msec. Total data collection time was 1300 ms, wi th a 200 ms wait time between each st imulus presentation. There were 40 presentations for each condition, for a total of 640 stimulus presentations (4 directions of motion x 4 2 0 Figure 3 . Representation of s t imul i used to simulate auditory motion i n space. Pure tones are presented to the two ears through a sealed system. A: Correlated increases or decreases i n sound level at the two ears simulate auditory motion i n depth. B: Opposite-directed changes i n sound level at the two ears simulate auditory motion i n azimuth. C: Four different ramp rates and excursions corresponding to the four velocity conditions. D: St imulus time course. 2 1 2 2 ramp excursions x 40 presentations) for each unit . Calibration A probe microphone ( IVIE 1300) was inserted i n the acoustic couplers for in situ measurement of sound pressure levels near the tympanic membrane. A waveform analyzer (DataPrecision Data 6000) produced fast Fourier transforms of the sound spectra. The output of a Brue l and Kjaer pistonphone (124 dB at 250 Hz) was used to convert relative intensity measurements into sound pressure level (dB S P L re 20 ( iN/m 2 ) . Variat ions i n sound intensity at different frequencies were corrected wi th reference to the output of the waveform analyzer. Sound levels were calibrated at the beginning of each experiment and monitored on-line throughout the experiment. Data collection The an imal was located i n a sound-attenuating chamber (IAC Controlled Acoustic Environments) . Except for the sound delivery system, microdrive, stereotaxic apparatus, table and animal , a l l of the equipment used (infusion pump, respirator, computer, etc.) was located outside the chamber. The responses of single neurons i n area A l were recorded extracel lularly using glass-insulated p la t inum-i r id ium microelectrodes wi th impedances of 1-1.5 M Q at 1 k H z (Wolbarsht, MacNichol , & Wagner, 1960). Electrodes were advanced perpendicularly through the dura and cortex using a remote controlled microdrive. Signals from the electrode were bandpass filtered (500 H z to 12 kHz) , amplified (lOOOx), discriminated w i t h a window discriminator and monitored on an oscilloscope and an audio monitor (Grass A M 8 ) . S t imulus presentation and on-line data collection and display were controlled by the PDP/11 computer v ia an I B M P C serving as an intelligent terminal . 2 3 White noise and pure tone bursts were used as search s t imul i . When a uni t was encountered, its characteristic frequency (CF) was determined. St imulus presentation was done at C F , although additional frequencies were sometimes used. The 16 stimulus conditions delineated above were individual ly interleaved and presented i n a randomized order. This process was repeated for a total of 40 trials at which point data collection for an individual unit terminated. The total length of an experiment was 2-3 days; recording time was 12-36 hours. When recording was completed, the an imal was k i l l e d w i t h an intravenous injection of sodium pentobarbital (100 mg/kg). The skul l was opened to verify electrode placement using anatomical landmarks and previous maps of the auditory cortex surface (Schreiner & Cynader, 1984). Data analysis The computer generated post-stimulus histograms and spike counts for a l l s t imulus conditions. A u r a l dominance and binaural interaction category were determined by comparing responses to st imulat ion of the contralateral ear alone, st imulation of the ipsi lateral ear alone and st imulat ion of both ears during st imulus onset. Responses to stimulus offset were examined i n a s imi lar way. Responses to correlates of the four different directions of motion were determined by analyzing responses during the A M ramps. Preferred direction of movement i n depth was determined by comparing responses to simulated sound source movement toward and away from the receiver (correlated binaural increases and decreases i n sound levels, respectively); s imilar ly , preferred direction of movement i n az imuth was determined by comparing responses to ipsi lateral- and contralateral-directed simulated sound source movement (increasing sound level i n one ear and decreasing sound level i n the other ear, and vice versa). Un i t s which gave weak responses to A M ramps (less than one 2 4 spike per sweep) were classified as insufficiently responsive and not evaluated further. A 2:1 ratio between responses to opposed directions of motion along one dimension (depth or azimuth) was taken as the criterion for directional selectivity. In addition, responses to simulated auditory motion i n one dimension had to be at least 1.5 times stronger than those evoked by simulated auditory motion i n the other dimension. For a l l analyses, spontaneous activity was subtracted from the spike counts and response latencies were taken into account. / 2 5 RESULTS Data were obtained for a total of 80 neurons. Nineteen neurons did not respond wel l to the A M ramps and w i l l not be described further. The characteristic frequencies of the remaining 61 units ranged from 2 to 44 k H z . In general, sharp st imulus onsets (5 msec rise times) typically produced strong transient responses; the discharge elicited by the A M ramps was more sustained. Directional selectivity Three-quarters (61/80) of the units encountered responded to correlates of auditory motion. The majority of these AM-sensi t ive units (54/61) responded selectively to the direction of auditory motion and were classified according to preferred direction of simulated sound source motion. Three broad categories of directional selectivity were observed: 1- selectivity for correlates of auditory motion i n depth (toward or away from the receiver), 2- selectivity for correlates of auditory motion i n az imuth (ipsilateral- or contralateral-directed), and 3-selectivity for auditory motion directed both toward the receiver and i n azimuth (monaural-like responses). A smal l number of units (n=7) responded to A M ramps but did not show any selectivity for a particular direction of motion. The distr ibution of units fal l ing into each of the major groups is summarized i n figure 4. In this figure the perspective is from above the head of the animal and the receiver is positioned at the bottom of the figure. The horizontal axis represents az imuth; the vertical axis represents depth. Recordings were made from the left hemisphere; hence the left ear is ipsi lateral to the recording site, and the r ight ear contralateral. The length of each arrow is proportional to the number of uni ts preferring a part icular direction of s imulated sound source 2 6 away 3 monaural-like (contra) 20 toward Figure 4. Summary of directional preferences for all direction-selective units encountered (n=54). The perspective is from directly above the head of the animal. The vertical axis corresponds to depth; the horizontal axis corresponds to azimuth. Recordings are assumed to be made from left hemisphere. The length of each arrow is proportional to the number of units preferring a particular direction of simulated sound source motion; the numeral next to each arrow indicates the number of such units that were encountered. Oblique arrows refer to monaural-like units; these units showed equal preference for increases in sound level in both ears and in one ear alone. Units not included in this figure were those which did not show any directional preference (n=7), and those which did not respond to correlates of sound source motion (n=19). 27 motion; the accompanying numeral indicates the number of units i n each category. Oblique arrows refer to units which responded equally wel l to motion directed toward the receiver and i n one azimuthal direction (monaural-like units; see section C). Not included i n this figure are seven units which showed no directional preference, and nineteen units which d id not respond to A M r a m p s . A . Motion in depth Uni t s preferring simulated sound source motion i n depth comprised 37% (23/61) of a l l motion-sensitive units sampled. M a n y more of these units responded selectively to increases than to decreases i n sound level (more toward-than away-preferring units were found; see figure 4). Toward-preferring units gave transient responses to binaural st imulus onset and sustained responses dur ing A M ramps i n both ears. Figure 5 shows post-stimulus t ime histograms depicting the t iming of a toward-preferring neuron's discharge i n relation to the t ime course of the st imulus (shown below each histogram), for the four directions of s imulated auditory motion. This neuron responds wel l to monaural st imulus onset i n the contralateral ear (top left panel) but gives weak responses to stimulus onset i n the ipsi lateral ear (bottom left panel). The response to binaural stimulus onset is stronger than the sum of both monaural responses (bottom right panel), indicat ing strong facilitation ( E E binaural interaction type). O n each histogram, a horizontal l ine marks the responses to intensity correlates of auditory motion. There is v i r tua l ly no response above background for ipsilateral-directed auditory motion, when the st imulus increases i n amplitude i n the ipsi lateral ear and decreases i n the contralateral ear (top left panel); the reversed condition, i n which sound level increases i n the contralateral ear and decreases i n the ipsi lateral ear, produces a weak response (bottom left panel). B y contrast, the 2 8 I P S I L A T E R A L - D I R E C T E D T O W A R D 4> M "5. Z 100-o 6 G 100-200 400 600 800 1000 1200 200 400 600 800 1000 1200 C O N T R A L A T E R A L - D I R E C T E D o 100-200 400 600 800 1000 1200 time (msec) 1 A W A Y 300-200-100-200 400 600 800 1000 1200 time (msec) i 4***St<**^. SE06.015 16 kHz Figure 5. Post-stimulus time histograms showing the responses of a single neuron i n relation to the time course of the s t imul i , for the four direction of auditory motion. Responses are collapsed across the four values of ramp excursion; b in width is 10 msec. A horizontal l ine indicates the responses dur ing the A M ramp; these responses are subject to further analysis. This unit is defined as a toward-preferring uni t because the responses dur ing correlated A M ramps i n the two ears (top right panel) are the strongest. 2 9 response obtained dur ing correlated increases i n stimulus amplitude i n the two ears (top right panel) is quite vigorous, and contrasts markedly wi th the lack of response observed wi th correlated decreases i n amplitude i n the two ears (bottom right panel). Panel A of figure 6 illustrates the responses of the unit described i n figure 5 i n the form of a polar plot. In this panel the perspective is from above and the receiver is positioned at the bottom of the open circle. Directional conventions are the same as i n figure 4. The filled inner circle represents the spontaneous activity of the unit . The length of each arrow is proportional to the response evoked by the A M portion of the 40 stimulus presentations; the accompanying numeral refers to the actual number of spikes (minus spontaneous activity). For this unit , 329 spikes above spontaneous activity were evoked during correlated increases i n sound level at the two ears and only 70 spikes were evoked by correlated decreases i n sound level at the two ears. Marked ly weaker responses were evoked when sound level increased i n one ear and decreased i n the other ear (corresponding to ipsi lateral- or contralateral-directed azimuthal motion), indicated by the shorter side arrows. The breadth of tuning for this correlate of direction of sound source motion could vary from neuron to neuron. Panels B-D of figure 6 show the responses of two other toward-preferring units, both of which responded most vigorously dur ing correlated increases i n st imulus amplitude i n the two ears. In some neurons l ike that i l lustrated i n panel B , responses to the other directions of motion tested (aside from directly toward the receiver) were less than spontaneous activity, indicat ing inhibi t ion below spontaneous levels i n the non-preferred directions. The neuron i n panel C showed responses that were much more broadly tuned than those of the cells of panels A and B , but responses to other directions of motion were s t i l l clearly weaker than those evoked by simulated motion toward the receiver. ( 3 0 Figure 6. Plots of spike counts dur ing A M ramps s imulat ing four directions of auditory motion. Each plot refers to a different unit . The perspective is from directly above the head of the animal; the filled inside circle indicates spontaneous activity. The vertical axis represents depth (toward/away), and the horizontal axis represents az imuth (ipsilateral/contralateral). The ipsi lateral ear is on the left side i n a l l cases. The length of each arrow is proportional to the spike count dur ing the A M ramp for each direction of motion; the accompanying numeral refers to the number of spikes evoked during the same period (minus spontaneous activity). These four toward-preferring units have different breadths of tuning for simulated motion toward the receiver. A: Polar plot for the uni t shown i n figure 5. B-D: Toward-preferring units wi th different breadth of tuning for motion toward the receiver. The added response to sideways motion becomes more apparent i n more broadly tuned units (D). JL 13.002 5 kHz JL24.013 20 kHz 3 2 As i l lus t ra ted i n figure 4, neurons preferring simulated auditory motion away from the an imal were relatively less common than those preferring motion toward the animal . Figure 7 shows post-stimulus time histograms for an away-preferring neuron. Note the absence of response to monaural or b inaura l sound onset and the transient response to sound offset i n the ipsi lateral ear (top left panel), i n the contralateral ear (bottom left panel) and i n both ears (top right panel). Most away-preferring units responded to sound offset i n both ears more vigorously than did the population of toward-preferring units. Figure 8 shows polar plots representing the responses of two neurons that responded most vigorously to simulated motion directed away from the receiver; panel A illustrates the responses of the uni t described i n figure 7. Fo r away-preferring neurons, the degree of selectivity also appeared to vary i n strength from neuron to neuron. The neuron i n panel A of figure 8 showed almost no response to motion toward the animal while the neuron i n panel B was more broadly tuned for motion i n depth. Figure 9 plots the preferred direction of motion i n depth against the preference for b inaura l sound onset or offset, for the population of depth-preferring units. A quantitative index of the motion i n depth preference is obtained by dividing the difference between the toward and away responses by the sum of these responses: motion i n depth index = (toward - away)/(toward + away) Thus, i n figure 9, units wi th positive abscissa values have stronger toward responses than away responses, and conversely for units w i t h negative values. S imi la r ly , preference for binaural onset or offset is measured by dividing the difference between the responses to binaural onset and offset by the sum of these responses: on off index = (binaural on - off)/(binaural on + off) 3 3 rPSILATERAL-DIRECTED « 50-200 400 600 800 1000 1200 100- TOWARD 50-200 400 600 800 1000 1200 1 100-1 M '3. 50-CONTRALATERAL-DIRECTED 200 400 600 800 1000 1200 time (msec) AWAY 50-200 400 600 800 1000 1200 time (msec) $ ' ^ < < * * * < < < _ t r r ....... AU22.067 13 kHz Figure 7. Conventions are the same as in figure 5. Post-stimulus time histograms showing the responses of a single neuron in relation to the time course of the stimuli, for the four direction of auditory motion. This unit is defined as an away-preferring unit because the responses during correlated AM ramps in the two ears (bottom right panel) are the strongest. 3 4 Figure 8. Conventions are the same as i n figure 6. Polar plots of spike counts dur ing A M ramps s imulat ing four directions of auditory motion for two away-preferring uni ts . 35 Motion in depth versus binaural on off response 3 ca cu i ca + 1 o X <u C •8 2-1 -0 • • • -1 0 1 on off index i^m-£g,°% (both on + both off) Figure 9. Plot of the preferred direction of motion i n depth versus the response to b inaura l sound onset and offset, for the population of depth-preferring neurons. Un i t s wi th positive abscissa values prefer motion toward the receiver, and units w i t h negative abscissa values prefer motion away from the receiver. S imi lar ly , units wi th positive ordinate values give stronger transient on responses, and units w i th negative ordinate values give stronger transient off responses. Toward-preferring units are also on units; away-preferring units can be both on or off. 3 6 Uni t s w i th positive ordinate values greater have stronger transient on responses than off responses, and conversely for units w i th negative values. The plot shows that a l l units which gave transient responses to stimulus onset i n both ears also preferred correlated increases i n sound source intensity at the two ears (simulated sound source motion toward the receiver). Un i t s which responded to sound offset preferred correlated decreases i n sound source intensity at the two ears (simulated sound source motion away from the receiver); one away-preferring neuron did not respond to sound offset and did not follow this pattern. Because relatively few away neurons were encountered i t was not possible to quantify the relationship between preferred direction of motion i n depth and binaural on/off response beyond the obvious relationship noted i n figure 3. Most depth-preferring units have facilitatory (EE) b inaural interactions: the response to st imulation of both ears together is greater than st imulat ion of either ear alone. This holds for the sharp stimulus onsets as well as the A M ramps: responses to increases i n sound level i n both ears together is greater than response to increases i n either ear alone. The degree of binaural facilitation seen i n depth-sensitive units ranged a l l the way from units w i th very strong facilitatory interaction to units which responded to sound i n each ear alone but showed no b inaura l facilitation at a l l (termed occlusive cells by Imig and Adr ian , 1977). The strength of binaural interaction was related to the breadth of directional tuning for simulated motion i n depth: units w i th very strong facilitatory binaural interactions responded exclusively to motion toward the receiver; units w i th medium or weak binaural interactions showed broader tuning, responding to sideways motion i n addition to motion toward the receiver. Figure 10 plots the breadth of tuning against the degree of facilitatory binaural interaction for a l l depth-preferring units. Breadth of tuning for motion i n depth is calculated by dividing the strongest response to depth by the strongest response 3 7 Breadth of tuning for motion in depth versus binaural interaction 5-•o 1 4-2-!' • El a • • 1 0 I 1 1— 1 2 both contra + ipsi (on or off) Figure 10. Plot of the breadth of tuning for motion i n depth versus the strength of b inaura l interaction, for the population of depth-preferring units. Breadth of tuning of measured by taking the ratio of the strongest responses to simulated motion i n depth and i n azimuth. B inau ra l interaction is measured by dividing the b inaural response by the sum of both monaural responses. For toward units, this ratio is calculated using the onset responses; for away units, response offset are used instead. 38 i n azimuth. The strength of binaural interaction is calculated by dividing the b inaural response by the sum of both monaural responses. For toward units, this ratio is calculated using the transient onset response; for away units, the response to sound offset is used. Al though the scatter between these two measures is rather broad (r=0.21), there is a general trend for units w i th weaker b inaura l interactions to show broader tuning for movement i n depth. B. Motion in azimuth Uni t s which responded exclusively to simulated sound source motion i n azimuth comprised 10% of our sample (6/61). Un i t s selective for azimuthal motion appeared relatively more rare than units preferring motion toward the an imal (see figure 4) and tended to be characterized by inhibitory binaural interactions (EI or I E cells) and strong excitatory responses v i a only one of the two ears. A z i m u t h a l selective neurons gave transient responses to sound onset i n the dominant ear, sometimes accompanied by transient responses to sound offset i n the non-dominant ear. A l l units preferred motion directed toward the dominant ear. Figure 11 shows post-stimulus time histograms for a uni t preferring ipsilateral-directed auditory motion. This uni t gives strong transient responses to stimulus onset i n the ipsi lateral ear (lower left panel) and does not respond at a l l st imulus to onset i n the contralateral ear (top left panel). Binaura l sound onset produces a diminished response (bottom right panel), indicat ing inhibi t ion (IE b inaura l interaction type). In addition, this neuron responds to st imulus offset i n the contralateral ear (bottom left panel). The strongest response dur ing the A M ramps is elicited by an increase i n sound level at the ipsi la teral (dominant) ear and a simultaneous decrease i n sound level at the contralateral (non-dominant) ear (bottom left panel). Figure 12 shows polar plots i l lus t ra t ing the responses of four neurons 3 9 I P S I L A T E R A L - D I R E C T E D 200 400 600 800 1000 1200 T O W A R D 501 *i f'r-r 200 400 600 800 1000 1200 C O N T R A L A T E R A L - D I R E C T E D A W A Y . 3 1001 O e 50" Ik • • L f y !• i i i i i i I I 200 400 600 800 1000 1200 time (msec) 50 r T " T r T ' i — f i i i' i i i 200 400 600 800 1000 1200 time (msec) AU22.026 10 kHz F i g u r e 11. Conventions are the same as i n figure 5. Post-stimulus time histograms showing the responses of an ipsilateral-preferring neuron, for the four directions of auditory motion. This uni t is an ipsilateral-preferring uni t because the responses dur ing opposite-directed A M ramps increasing i n the ipsi lateral ear and decreasing i n the contralateral ear are the strongest (top left panel). 4 0 Figure 12. Conventions are the same as i n figure 6. Polar plots of spike counts dur ing A M ramps s imulat ing four directions of auditory motion, for four units preferring az imuthal motion. A -B: Uni t s preferring ipsilateral-directed motion. C-D: Un i t s preferring contralateral-directed motion. 41 AU22.075 2 kHz SE 13.003 16 kHz 4 2 which responded most vigorously to contralateral-directed simulated sound source motion (panels A and B) and ipsilateral-directed simulated sound source motion (panels C and D). The degree of directional selectivity among azimuth-preferring units showed some var iabi l i ty . In some cases, responses to the opposite direction of motion could be either non-existent or less than spontaneous activity. In other cases, responses to the opposite direction of motion could be fair ly vigorous. For a l l units responding wel l to sideways motion (including monaural-like units; see section C), there was a strong relationship between the transient onset response i n the dominant ear and the preferred direction of simulated sound source motion i n azimuth: units wi th strong onset responses i n the contralateral ear preferred increases i n sound intensity i n the contralateral ear and simultaneous decreases i n the ipsi lateral ear, and vice versa for ipsi lateral-preferring units . Figure 13 plots the preferred direction of simulated auditory motion i n az imuth against the response to sound onset i n the ipsi lateral and contralateral ear (a measure of ear dominance) for a l l units displaying selectivity for one direction of motion i n azimuth. Preferred direction of motion i n az imuth is measured by dividing the difference between the ipsilateral- and contralateral-directed responses during the A M ramps by the sum of these responses: motion i n az imuth index = (contra A M - ipsi AM)/(contra A M + ips i A M ) Uni t s w i t h positive abscissa values have stronger contralateral-directed responses than ipsilateral-directed responses, and conversely for units wi th negative values. The ordinate values refer to ear dominance, which is measured by dividing the difference between both transient monaural responses to sound onset by the sum of these responses: ear dominance = binaural on/(contra on + ips i on) Un i t s wi th positive ordinate values give stronger responses to contralateral onset 4 3 Motion in azimuth versus ear dominance • Q. 2 -•- i A + tl 0 -1 -• 0 B a • • _ B B B a • a a • -2 -1 0 (contra on - ipsi on) (contra on + ipsi on) Figure 13. Plot of preferred direction of simulated azimuthal auditory motion versus ear dominance (measured using both responses to monaural sound onset), for a l l units displaying selectivity for one direction of motion i n azimuth, inc luding monaural- l ike units. Uni t s wi th positive abscissa values prefer contralateral-directed motion, and units wi th negative abscissa values prefer ipsilateral-directed motion. S imi la r ly , units w i th positive ordinate values give stronger transient responses to contralateral sound onset, and units w i th negative ordinate values give stronger transient responses to ipsi lateral sound onset. There is a strong l inear relationship between the two measures (r=0.81). 4 4 and units w i t h negative ordinate values give stronger responses to ipsi lateral onset. The relationship between preferred direction of azimuthal motion and ear dominance is strongly l inear, w i th a correlation coefficient of 0.81. C. Monaural-like units It is important to understand the response of a neuron wi th no binaural interaction under the stimulus conditions used i n this experiment. If a neuron prefers st imulus onset i n the contralateral ear (and therefore responds to increasing st imulus amplitude v ia that ear) and has no input at a l l from the ipsi lateral ear, then that neuron w i l l respond wel l i n two of the four conditions employed. These include the conditions i n which s t imul i increase i n amplitude i n both ears (because of the increase i n amplitude i n the contralateral ear) and the az imuthal motion condition i n which the stimulus increases i n amplitude i n the contralateral ear and decreases i n the ipsi lateral ear. Monaura l - l ike units were the most numerous, comprising nearly 41% of our sample (25/61). These units exhibited strong directional preferences along both axes (depth and azimuth), and responded equally wel l to increases i n sound source intensity i n one ear alone or i n both ears together; the response to simulated sound source motion toward the receiver and the preferred ear were often indist inguishable. Figure 14 shows post-stimulus time histograms depicting the t iming of a monaural-l ike unit 's discharge i n relation to the time course of the stimulus. The transient response to sound onset i n the contralateral ear (top left panel) and i n both ears together (bottom right panel) is essentially the same, hence there is no binaural interaction (EO binaural interact ion type). Increasing A M ramps i n the contralateral ear produces strong responses regardless of the input of the ipsi lateral ear: the response to an increase i n st imulus amplitude i n the contralateral ear is the same whether i t is 4 5 I P S I L A T E R A L - D I R E C T E D 8 400H 'S. 200H ijnllj-i, ! n r < f - f l l | ,•• y n r . | 200 400 600 800 1000 1200 T O W A R D 400-200" 200 400 600 800 1000 1200 ^ L C O N T R A L A T E R A L - D I R E C T E D A W A Y 8 ^ 400-Q. O B 200-200 400 600 800 1000 1200 time (msec) 1 400-200-200 400 600 800 1000 1200 time (msec) AU22.008 4.5 kHz Figure 14. Conventions are the same as i n figure 5. Post-stimulus time histograms showing the responses of a contralateral-ear-dominated, monaural-l ike neuron, for the four directions of auditory motion. This uni t is defined as a monaural- l ike uni t because the response dur ing increasing A M ramps i n the contralateral ear is not influenced by the input from the ipsi lateral ear (top right and bottom left panels). 4 6 accompanied by a corresponding increase or decrease i n s t imulus amplitude i n the ipsi lateral ear. The responses during the A M ramps i n the bottom left and top right panels of figure 14 are essentially the same. Figure 15A is a polar plot representation of a contralateral-dominated monaural-l ike uni t (the same unit as i n figure 14). This uni t responds equally wel l to increases i n sound level i n the contralateral ear alone and i n both ears together; the responses to the two preferred directions of motion are s imi lar i n magnitude. Two arrows of equal length for az imuthal and radia l motion are the signature of a monaural-l ike unit . A ipsilateral-dominated monaural-like unit is shown i n figure 15B; the response to ipsilateral-directed azimuthal motion is v i r tua l ly the same as that directed directly toward the receiver. A l l monaural- l ike units preferred increases i n intensi ty rather than decreases; no monaural-l ike away units (units preferring decreases i n intensity) were encountered. N ine units preferred simulated sound source motion directed toward the receiver and the ipsi lateral ear, and 16 units preferred simulated sound source motion directed toward the receiver and the contralateral ear (refer to figure 4). It should be stressed that monaural-like units are not necessarily entirely monaural; at certain intensity levels these units respond as though they receive input from one ear only, and therefore respond wel l to sound level increases i n the dominant ear regardless of what happens at the other ear. About ha l f of the monaural-l ike units (12/25) were t ruly monaural , w i th no response evoked by the non-dominant ear and no binaural interaction (EO binaural interaction type) at any of the intensity levels tested i n our study; the remaining 13 units had unequal thresholds and intensi ty functions for the two ears, producing monaural-l ike responses at certain intensity levels. A l l units showed strong ear dominance and preferred increases i n sound level i n the dominant ear. Few of these units had Figure 15. Conventions are the same as i n figure 6. Polar plots of spike counts dur ing A M ramps s imulat ing four directions of auditory motion. A: Polar plot for the uni t shown i n figure 13. B: Ipsilateral-ear-dominated monaural-l ike unit . In both cases, the responses to simulated sound source motion toward the receiver and i n the preferred azimuthal direction are approximately equivalent. 4 8 strong b inaura l interactions; when present, input from the non-dominant ear was slightly facilitatory. The parameters influencing the strong preference of monaural-l ike units for correlates of azimuthal motion were examined i n section B . D. Distribution of unit types A total of 21 penetrations, roughly normal to the cortical surface, were made. Neurons found along most electrode penetrations normal to the surface of the cortex showed s imi lar directional preferences, which indicates that units w i th constant responses to simulated sound source motion may occur i n clusters or columns w i t h i n the cortex. Four schematic reconstructed penetrations are shown on figure 16. Each polar plot il lustrates the directional preference of a different unit . Neurons encountered along penetrations A and B responded best to simulated sound source motion toward the receiver; some units also responded to sideways motion as wel l , to varying degrees. Neurons encountered along penetration C responded best to simulated ipsilateral-directed sound source motion. Neurons encountered along penetration D preferred simulated motion toward the receiver and ipsilateral-directed (monaural-like). Al though no histological information is available to confirm that penetrations were orthogonal to the cortical surface, this clustering of units wi th s imi lar directional preferences is an indication of possible columnar organization i n the pr imary auditory cortex wi th respect to preferred direction of sound source motion. Velocity selectivity Most AM-sensi t ive neurons also showed selectivity for the speed and amplitude of A M ramp excursion. These are intensity correlates of sound source velocity. The majority of units (41/61, or 67% of a l l motion-sensitive units Figure 16. A-D: Schematic reconstruction of 4 electrode penetrations made roughly normal to the cortical surface i n area A l , showing units encountered and their directional preferences. Each polar plot corresponds to one unit; directional conventions are the same as i n previous figures. 5 0 200 u AUO8.0O4 5.5 kHz AU08.0O5 4.5 kHz AU08.006 5 kHz B JL24.025 20 kHz 200 y. D AU22.027 8kHz AU22.028 10 kHz 200 U JL24.0O3 2kHz JL24.006 2kHz JL24.008 2kHz JL24.010 2kHz JL24.012 2kHz 5 1 Figure 17. A: Polar plots representations of the responses during the A M ramps at the four values of ramp excursion. The four plots refer to the responses of one uni t at four different ramp excursions. Ramp excursion increases from left to right; the corresponding ramp excursion i n dB per 250 msec is printed below each plot. B: Monaura l and binaural rate/intensity functions of the same neuron for the transient onset response. This uni t is a defined as a monotonic, velocity-dependent unit : increases i n ramp excursion produce stronger responses i n the preferred direction of motion. The rate/intensity function is also monotonic and parallels the response to the A M ramp i n the preferred direction. SE06.024 15 kHz onset excursion (dB/5 msec) 5 3 sampled) responded best to the highest ramp excursion used and were termed monotonic, velocity-dependent units. Figure 17 shows polar plots (A) of the responses dur ing A M ramps at the four values of ramp excursion (printed below each plot) for a monotonic, toward-preferring unit, and the rate/intensity function (B) of the same unit for the monaural and binaural responses evoked by sharp stimulus onsets at four different intensity levels. The responses to A M ramps increase wi th greater ramp excursions, and louder b inaura l s t imulus onset also evokes a stronger response. The two measures are monotonic and paral lel each other. Such units are called monotonic, velocity-dependent units. A small number of units (10/61 or 16%) preferred one part icular ramp excursion, and smaller or greater ramp excursions evoked weaker responses. These units were termed non-monotonic, velocity-dependent units. F igure 18 shows polar plots of the responses during A M ramps (A), and the rate/intensity function (B) for monaural and b inaura l onset response for a non-monotonic, monaural-l ike unit . The intensity functions and the response to the A M ramp are both non-monotonic (for the range of intensity tested). The remaining ten units (16%) gave responses which were either independent of ramp excursion or idiosyncratic, sometimes w i t h changes i n preferred direction. Figure 19A shows the polar plots for a neuron which prefers away at the smallest ramp excursion but whose directional selectivity changes as ramp excursion increases. The accompanying graph (figure 19B) show the rate/intensity functions for the binaural onset and offset responses. The binaural offset response is strongest at low intensity levels and progressively diminishes at higher intensities; the onset response is weak at low intensities and gradually becomes stronger as st imulus amplitude increases. Therefore this uni t prefers decreasing A M ramps (away) at lower ramp excursions and increasing A M ramps (toward) at higher ramp excursions. Figure 20 shows polar plots (A) and rate/intensity functions (B) for a 5 4 Figure 18. Conventions are the same as i n figure 17. A: Polar plots representations of the responses during the A M ramps at the four values of ramp excursion. B: Monaura l and binaural rate/intensity functions of the same neuron for the transient onset response. This uni t is a defined as a non-monotonic, velocity-dependent unit: a part icular ramp excursion produces the strongest response; increases or decreases i n ramp excursion d imin i sh responding. The rate/intensity function is also non-monotonic but does not paral lel the response to the A M ramp i n the preferred direction. AU22.018 5 kHz ramp excursion (dB/250 msec) onset excursion (dB/S msec) 5 6 Figure 19. Conventions are the same as i n figure 17. A: Polar plots representations of the responses during the A M ramps at the four values of ramp excursion. B: B i n a u r a l rate/intensity functions of the same neuron for the transient onset and offset responses. This uni t is defined as an idiosyncratic, velocity dependent unit: at lower ramp excursion, this uni t prefers away; as ramp excursion increases, this uni t gradually changes directional preference and prefers toward. This change i n preferred direction wi th increasing ramp excursion can be explained by the rate/intensity functions for the onset and offset transients: the offset transient does not vary wi th changes i n intensity, while the onset transient is weak at low intensities and becomes progressively stronger at higher intensit ies. AU22.001 3 kHz ramp excursion (dB/250 msec) onset and offset excursion (dB/S msec) 5 8 Figure 20 . Conventions are the same as i n figure 17. A: Polar plots representations of the responses during the A M ramps at the four values of ramp excursion. B: Monaura l and binaural rate/intensity functions of the same neuron for the transient onset response. This uni t is defined as a velocity-independent unit: changes i n ramp rate and excursion have l i t t le or no influence on the strength of responding or on the directional preference of this unit . A 38 44 50 ramp excursion (dB/250 msec) AU22.052 5 kHz onset and offset excursion (dB/5 msec) 6 0 velocity-independent neuron. This neuron showed l i t t le selectivity for A M correlates of stimulus velocity, over the range of ramp excursion employed; the four ramp excursions evoked s imi lar responses. For about ha l f of a l l direction-selective units, the preferred value of ramp excursion could be predicted from a unit 's rate/intensity function for sharp sound onset. This is part icularly true of most toward-preferring neurons i n which the responses to sharp and gradual (AM) binaural sound onset across intensity levels usual ly monotonic. The remaining units had intensity functions for the ramp and sharp onset which differed and the preferred ramp excursion could not be directly predicted from the rate/intensity function for sound onset. This was especially true of non-monotonic, velocity-independent, and idiosyncratic units . Effect of changing frequency Several units were examined at a variety of frequencies. A total of 33 cells were tested at best frequency plus one or more additional frequencies. A l l four magnitudes of ramp excursion were used at each frequency tested. Al though this parameter was not systematically investigated for a l l neurons encountered, directional preference seemed to a first approximation independent of the frequency used for testing. Only four of these 33 cells appeared to clearly change directional preference over this admittedly l imi ted range of frequencies. However, some of these cells changes b inaural interaction class at different frequencies, and as might be expected, rate/intensity functions were could be different at different frequencies. In addition, for the entire population of direction-selective units, there was no overall effect of frequency on directional preference, i.e., units w i th h igh or low characteristic frequencies were not confined to a part icular class of directional preference. 61 DISCUSSION The results of these experiments indicate that single neurons i n the pr imary auditory cortex of the cat can be highly sensitive to at least one correlate of auditory stimulus motion, namely relative modulation of sound intensity at the two ears of the receiver. These neurons are quite common, constituting three-fourths of our sample. They respond selectively to certain directions of simulated sound source motion and can be classified according to their preferred direction of motion. Depth-selective units respond best to correlated increases or decreases i n sound source intensity at the two ears; azimuth-selective units prefer opposite-directed changes i n sound source intensity at the two ears. Monaural - l ike units respond equally wel l to changes i n sound intensity i n one ear alone or i n both ears. Direction-selective neurons are spatially segregated from each other and may occur i n clusters wi th in the cortex. These units also respond selectively to A M ramps of different speeds and excursions, a correlate of sound source velocity and range of movement. Mechanisms of direction and velocity selectivity The responses of A l neurons to simulated sound source motion can be explained i n terms of response characteristics which are normally studied separately, but which interact to produce selectivity to the correlates of direction and velocity of sound source motion i n space. A . Motion in depth Neurons wi th facilitatory binaural interactions (E/E cells) respond best to the diotic intensi ty changes corresponding to motion directly toward the head. Neurons preferring motion directly toward the receiver gave strong responses to 6 2 binaural sound onset and to diotic increasing A M ramps. The degree of directional selectivity is correlated wi th the amount of b inaura l facilitation, wi th strongly facilitatory cells being the most selective. E / E neurons w i t h off responses respond to motion away from the head; binaural facilitation of offset components may also be present and increases selectivity i n the preferred direct ion. The high percentage of neurons (39%) responding best to simulated motion i n depth may be a reflection of the fact that the majority of cortical neurons give their greatest response when IID is very small or equal to zero (Phil l ips & Irvine, 1981b). Thus sound sources located near the midline would receive the largest representation i n the cortex. The more transitory nature of the response (compared wi th the azimuth units) may be a reflection of the fact that IIDs do not unambiguously code for movement i n space but also signal intensi ty changes i n a stationary sound source. B. Motion in azimuth Neurons wi th inhibi tory b inaural interactions (E/I and I/E cells) respond best to the dichotic intensity changes corresponding to az imuthal auditory motion. E a r dominance determines the preferred direction of azimuthal motion. E / I units which give transient responses to sound onset i n the contralateral ear respond best to intensity correlates of motion i n azimuth directed toward the contralateral ear. Sound source motion directed toward the ipsi lateral ear evokes selective responses from I/E units which give transient responses to sound onset i n the ipsi la teral ear. Whi le these response properties are sufficient to confer selectivity to these neurons, some units also give responses to sound offset i n the non-dominant ear; this feature enhances selectivity for the detection of azimuthal mot ion. 63 C. Monaural-like units M a n y cells w i th l i t t le or no binaural interaction, either facilitatory or inhibitory, responded equally well to sound becoming louder i n both ears and to sound becoming louder i n the dominant ear. The contralateral ear dominated i n 64% of these units and the ipsi lateral ear i n 36%. Monaural - l ike units comprised the largest group of neurons i n this study (41% of direction-selective units). Most behaved as i f they were only influenced by one ear; a few responded weakly to sound i n the non-dominant ear, but the binaural response was equal to the response evoked by the dominant ear alone. These units appeared monaural but i t is l ike ly that some of them would have shown binaural interactions wi th varied IID levels. In this study, a l l stimulus presentation was performed at a reference IID level of 0 dB , wi th both ears receiving equally loud st imulation. However, since many E/ I and I/E cells show binaural interactions only when the input to the non-dominant ear is louder than that to dominant ear, presenting s t imul i w i th different sound levels i n the two ears may reveal stronger, more specific b inaura l interactions i n this neuronal population. D. Velocity selectivity Most units exhibited monotonic rate/intensity functions over the range of A M ramp excursions used i n this study. This reflects the monotonic rate/intensity functions for the onset portion of the stimulus; monotonic cells prefer faster velocities of auditory motion where the higher ramp excursions begin to resemble sharp onsets. About one-third of the units were selective for one of the smaller A M ramps; these cells wound be suitable for encoding specific velocities of moving sound. B y and large, the responses to sharp sound onsets (5 msec rise time) and ramps s imulat ing auditory motion (250 msec rise time) were s imi lar across intensity levels. Monotonic units responded wel l to the 6 4 highest ramp excursions and non-monotonic units preferred lower ramp excursions. However, the preferred velocity could not always be predicted from the rate/intensity function for the onset responses; additional temporal response characteristics may account for this discrepancy. E. A model for direction and velocity selectivity The results of this experiment show that the selectivity for sound source motion reported i n this study can be related to particular combinations of monaural and b inaura l response properties that have been studied extensively (in isolation) by other workers. These response properties of neurons i n the pr imary auditory cortex can be shown to act synergistically, providing an underlying mechanism for selectivity to the binaural intensity correlates of auditory motion. Figure 21 i l lustrates how the response characteristics of cortical neurons interact to produce response selectivity for the direction and velocity of moving sound sources. The ma in determinants of direction selectivity are b inaura l interaction class, on/off responses and ear dominance; monotonicity of rate/intensity function for sound onset (and offset, to a lesser extent) determines velocity selectivity. Several generalizations from this hypothetical mechanism arise from these data: 1- Neurons wi th facilitatory b inaural interactions prefer motion i n depth: neurons wi th on responses prefer motion toward the receiver, and neurons wi th off responses prefer motion away from the receiver. 2- Neurons wi th inhibitory binaural interactions respond best to motion i n az imuth, directed into the hemifield corresponding to the dominant ear: neurons wi th contralateral on responses and/or ipsi lateral off responses prefer motion into the contralateral hemifield (and vice versa for ipsilateral-on and/or contralateral-off neurons). 3- Neurons wi th no binaural interaction (monaural) prefer motion directed toward the receiver and into the hemifield corresponding 65 Figure 21. A model of direction and velocity selectivity for auditory movement, based on interactions of response characteristics of neurons in the primary auditory cortex. The major determinants of the direction selectivity of Al neurons are interactions between binaural interaction type, ear dominance and transient onset and offset responses. Directional preferences resulting from these interactions are indicated by arrows; the vertical axis represents depth, and the horizontal axis represents azimuth. Arrows pointing down and up represent auditory motion directed toward and away from the receiver (along the midline), respectively; arrows pointing to the right and left represent auditory motion directed into the contralateral and ipsilateral hemifield, respectively (assuming recordings are made from the left side). The monotonicity of the rate/intensity function determines preference for velocity of auditory motion. Asterisks refer to classes of direction- and velocity- selective neurons encountered, whose responses to simulated auditory motion could be predicted from response characteristics listed above. 6 6 to the dominant ear; neurons wi th off responses prefer the opposite directions of motion (away from the receiver and into the hemifield corresponding to the non-dominant ear). 4- Neurons wi th monotonic rate/intensity functions prefer higher velocities; neurons wi th non-monotonic rate/intensity functions respond best at lower velocities. The asterisks i n figure 21 refer to classes of direction- and velocity-selective neurons that were encountered i n this study, and whose responses to intensity correlates of auditory motion could be predicted from the previously l is ted responses characteristics and/or combinations of these responses characteristics. Technical considerations It is important to recognize the l imitations of the conditions used i n this experiment to simulate of sound source movement. In the free-field case, changes i n in teraural time differences and i n spectral content would accompany the alterations i n stimulus intensity that were used i n this study. In addition, the patterns of interaural intensity changes used i n this experiment are not entirely unique wi th regard to particular directions of motion. A full account of the relationship between alterations i n relative aural amplitude and the direction of motion of a sound source of constant strength i n three-dimensional space has been provided by Zakarauskas and Cynader (1990). They have carried out a mathematical analysis of the set of amplitude modulations associated wi th motion of a constant intensity sound source moving i n three dimensions. This analysis has revealed that certain changes i n sound level at the two ears are not necessarily associated wi th one specific sound source trajectory but may also result from a variety of other stimulus conditions. It is possible, for instance, that correlated increases i n sound level are associated wi th s t imul i moving tangentially to the receiver as well as directly toward her, result ing i n possible 67 perceptual ambiguities. In addition, the s t imul i used i n this experiment do not represent the full set of binaural intensity modulations produced by sound sources moving i n azimuth or i n depth. The analysis cited above demonstrated that unlike the A M ramps used i n this study to simulate auditory motion, the rates of intensity change associated wi th sound source movement are not necessarily l inear, nor do intensity changes occur at the same rate at the two ears (in the case of auditory motion i n azimuth). In spite of this, s t imul i wi th constant rates of change and wi th s imilar b inaural time courses were used because they produce an appropriate simulation of sound source movement that can be easily implemented i n a sealed sound delivery system. One must be wel l aware of the unavoidable l imitations and ambiguities inherent i n efforts to simulate motion of real world sound sources without actually providing that motion. This study deals only wi th binaural sound intensity modulation; i t is by no means the only cue available to a neural system detecting moving sound sources. A s t r ik ing result that can be derived from the acoustic analysis described above (Zakarauskas & Cynader, 1990) is that the rate of change of monaural intensity function is found to be directly proportional to the velocity scaled by the distance of a sound source for omnidirectional sources of constant intensities. This emphasizes the importance of a system that uses amplitude modulation as a component of a specialized motion detection system. This contention is supported by the neurophysiological evidence presented i n this study indicating that i n addition to responding selectively to the correlates of direction of motion, auditory neurons also show selectivity to correlates of sound source velocity. In this neuronal population, some neurons seemed to be sensitive to different rates of intensi ty change i n the two ears. Some neurons preferred low rates of change, while others preferred higher rates of change, corresponding to faster motion. 68 There was a distinct preponderance of neurons that responded best to the highest rates of A M that were employed. This is i n agreement wi th psychophysical evidence that shows that low rates of change of amplitude are poorly resolved by human receivers (Small , 1977). Analogies to vision This study has provided evidence for specialized systems dealing wi th correlates of auditory motion i n three-dimensional space. It is interesting to note that s imi lar mechanisms appear to exist i n vis ion and that l ike the auditory system, both systems appear to operate by dynamically comparing parameters of the s t imul i i n the paired end organs. Abundant psychophysical evidence indicates that the human visual system contains specialized channels for dealing wi th three-dimensional motion and that these channels are distinct from those that process static depth (Beverley & Regan, 1973, 1975; Regan, Beverley & Cynader, 1979; Richards & Regan, 1973). In addition, neurophysiological studies have shown that single cells i n cat visual cortex can be highly sensitive to the direction of st imulus motion i n three dimensional space (Cynader & Regan 1978, 1982). In the v isua l system, the relative velocity of the two ret inal images has been shown to be a sensitive cue to the direction of stimulus motion i n three dimensional space (Beverley & Regan, 1973, 1975; Regan, Beverley & Cynader, 1979) and v isua l cortex neurons (Cynader & Regan, 1978) show differential sensitivity depending on relative stimulus velocity. This provides a s t r ik ing paral le l wi th the mechanisms that we have uncovered here i n which single cells i n the auditory cortex appear sensitive to the relative rate of change of intensity i n the two ears. It appears that both sensory systems use s imi lar principles to extract three dimensional motion. The neurophysiological parallels between the two systems are supported by psychophysical evidence indicat ing that the 6 9 resolving capacities of the visual and auditory systems for st imulus motion are str ikingly s imi lar (Perrott, Buck, Waugh & Strybel, 1979; Waugh, Strybel & Perrott, 1979). Perception of stimulus motion i n the visual and auditory modalities appear to depend on s imi lar central mechanisms of motion detection. Specialized motion-detecting mechanisms in the auditory system? Considerable, highly specific information is available to the auditory system concerning the trajectory of a moving sound source. Obviously, there is a survival advantage for an organism i n detecting movement i n its environment as quickly and efficiently as possible. Aside from their obvious ut i l i ty for avoiding collisions and compensating for self-generated movements, motion detection mechanisms may be important for extracting information about the form of a sound source. In principle, one can imagine two different methods to infer sound source motion from the signals at the two ears. One method would be to s imply use the same system which is used to localize stationary sound sources, to register the position of the sources at different times, and then compare them to extract direction and velocity of motion. In this case, specialized systems for detecting motion are not needed or employed, but such a system requires extensive sequential processing of changing binaural patterns to extract motion information. The other method would be to use a specialized motion channel, working i n paral le l w i t h mechanisms extracting information about stimulus position. One advantage of calculating sound source velocity from position is economy of specialized hardware, because the same neural mechanisms are involved is extracting information about stimulus position and motion. O n the other hand, there is a distinct survival disadvantage for an organism to have to explicit ly calculate sound source position before knowing whether or not a sound source is moving, since this method is l ike ly to be slower than a paral lel , 7 0 dedicated auditory motion channel. Several investigators have gathered psychophysical data suggesting that the human auditory system infers motion without the use of specialized motion-detecting mechanisms. According to this view, the b inaural auditory system is relatively insensitive to motion, and position and distance are more salient cues than motion and velocity (Grantham, 1986). Psychophysical studies have compared the abili ty of the auditory system to resolve position and motion of sound sources, by measuring the smallest angular separation between two sound sources that a listener can detect (min imum audible angle or M A A ) and the m i n i m u m arc swept by a moving source which can be detected as moving (min imum audible movement angle or M A M A ) . The argument against the necessity of specialized motion detecting mechanisms is based on the observation that performance of human subjects i n detecting sound source motion varies i n the same way as i n static sound localization when st imulus frequency, duration or velocity are varied: the M A A and M A M A are affected by these stimulus parameters i n s imilar , predictable ways (Al tman & Viskov , 1977; Grantham, 1984,1986; Perrott & Musicant, 1977; Perrott & Tucker, 1988). Therefore the M A M A is only a blurred estimate of the M A A , a measurement error on the part of the receiver caused by movement of the sound source. In addition, because a serial system of position comparison has a l imi ted capacity to process changing inputs, a m i n i m u m integration time is necessary to resolve sound source motion, resul t ing i n larger M A M A s wi th increasing st imulus velocity because the system is approaching its upper processing l imi t . According to a serial method of extracting motion information, one can generalize directly to the dynamic sound field from known parameters defining static auditory localization. Therefore both static and dynamic sound localization depend on the same underlying mechanism, and there is no need to postulate specialized 7 1 motion detectors i n the auditory system. O n the other hand, psychophysical and neurophysiological evidence point to the existence of specialized motion-selective mechanisms i n the auditory system, i.e., that the detection of auditory motion involves more than the coding of successive localization judgements. Har r i s and Sergeant (1971) found that the monaural M A M A was almost as good as the b inaural M A M A for slowly moving sound sources. In the monaural mode, the auditory system can only use frequency and intensity information to detect motion; the b inaural cues normally used by the auditory system to infer sound source position are unavailable, and horizontal sound localization acuity is poorer (Butler, 1969). Nevertheless, subjects were able to detect auditory motion i n the monaural mode, indicat ing that specialized motion detecting mechanisms can use monaural information to detect motion. This is an indication that the auditory system uses time history, and possibly the time derivative of sound intensity, to detect motion (Zakarauskas & Cynader, 1990). In addition, range (or distance) cannot be calculated directly from binaural disparities, and motion of a source moving directly toward or away from the receiver cannot be inferred by a position comparison system. Hence, mechanisms specialized for detecting motion would be the only ones available to an organism i n this case. Perrott and Marlborough (1989) found that sound localization performance of moving broadband free-field s t imul i is superior to that which would be predicted i f the subject were simply comparing the location of the sound source at signal onset and offset. M A M A s obtained when the sound source was actually moving were significantly lower than when only the end-points of the arc of travel were marked. Therefore M A M A discrimination is not solely based on successive comparisons of sound source location at onset and offset. Al though this finding does not necessarily confirm the existence of specialized motion 7 2 detecting mechanisms, i t indicates that such mechanisms cannot be reduced to simple position comparators. Perrott and Musicant (1981) measured the M A A under dynamic conditions by asking subjects to estimate the position of a moving sound source at onset. The dynamic M A A was almost independent of sound source velocity, and almost as good as for stationary sources, indicat ing that localization precision is not affected by motion of the source, and pointing to a possible distinction between the coding of auditory spatial position and motion. Waugh et a l . (1979) measured the capacity of listeners to subjectively estimate suprathreshold auditory velocity i n the dark, and found that the abil i ty to discriminate sound source velocity is a well defined feature of the dynamic binaural system. In addition, auditory and v isual velocity judgement capabilities were nearly identical. This degree of s imilar i ty i n the perception of velocity by the visual and auditory systems is quite surprising, given the fact that the spatial resolving power of the visual system is much higher than that of the auditory system. These findings suggest that velocity judgements are drawn from similar specialized central motion-detecting mechanisms (Perrott et a l . , 1979; Waugh et al . , 1979). Neurophysiological studies have provided some support for the notion that auditory neurons respond selectively to sound source motion or correlates of such sounds. Neurons which appear to detect motion of sound sources and which could be part of specialized motion-detecting mechanisms i n the auditory system have been found i n the inferior colliculus (Altman, 1968), the medial geniculate body (Altman, Syka , & Shmigidina, 1970), the superior colliculus (Altman, 1971), the cerebellum (Altman, Bechterev, Radionova, Shmigidina, & Syka , 1976; Bechterev, Syka & Al tman , 1975) and the auditory cortex (Altman, 1987; Sovijarvi & Hyvar inen , 1974). The data presented i n this thesis also points to the existence of motion-detecting mechanisms i n the pr imary auditory cortex. 7 3 Future research should investigate the parameters governing the activity of specialized motion-detecting channels i n the auditory system, and the role of these channels i n the processing of motion information i n the free sound field. The interrelations between location-, motion- and velocity-sensitive auditory units are also of interest. Presumably, information about sound source motion is integrated wi th other types of spatial information from the auditory, v isual and somatosensory systems, and combined w i t h vestibular, proprioceptive and motor information to produce an integrated and cohesive perception of reality, and i f Dav id M a r r was around he'd probably take up audition as a hobby and solve a l l our problems. REFERENCES Al ta i an , J . A . (1968). Are there neurons detecting direction of sound source motion? Experimental Neurology, 22,13-25. Al ta i an , J . A . (1971). Neurophysiological mechanisms of sound source localization. In G.V. Gersuni (Ed.), Sensory processes at the neuronal and behavioral levels (pp. 221-244). New York: Academic Press. A l t a i a n , J . A . (1987). Information processing concerning moving sound sources i n the auditory centers and its ut i l izat ion by bra in integrative and motor structures. In J . Syka & R . B . 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