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Werker, J.F., & Hensch, T.K. (2015). Critical Periods in Speech Perception: New Directions. Annual Review of Psychology, 66, 173-196.
Werker, Janet Feldman, 1951-
Hensch, Takao K., 1966-
A continuing debate in language acquisition research is whether there are Critical Periods (CPs) in development during which the system is most responsive to environmental input. Recent advances in neurobiology provide a mechanistic explanation of CPs, with the balance between excitatory and inhibitory processes establishing the onset and molecular brakes establishing the offset of windows of plasticity. In this chapter we review the literature on human speech perception development within the context of this CP model, highlighting research that reveals the interplay of maturational and experiential influences at key junctures in development and presenting paradigmatic examples testing CP models in human subjects. We conclude with a discussion of how a mechanistic understanding of CP processes changes the nature of the debate: the question is no longer “are there CPs”, but rather what processes open them, keep them open, close them, or allow them to be reopened.
Critical Periods in Speech Perception: New Directions Janet F. Werker University of British Columbia Department of Psychology jwerker@psych.ubc.ca Takao K. Hensch Harvard University Department of Molecular and Cellular Biology hensch@mcb.harvard.edu Running Title: CRITICAL PERIODS SPEECH PERCEPTION Corresponding Author: Janet F. Werker University of British Columba Department of Psychology 2136 West Mall Vancouver, BC, V6T 1Z4 (604) 822-6741 (Office)(604) 822-6408 (Lab)jwerker@psych.ubc.caThis is the first-submitted version of the manuscript Critical Periods in Speech Perception: New Directions [https://doi.org/10.1146/annurev-psych-010814-015104)], prior to peer-review. Posted with permission from the Annual Review of Psychology, Volume 66 © by Annual Reviews, http://www.annualreviews.orgCRITICAL PERIODS SPEECH PERCEPTION Page 2 of 50 Table of Contents I. INTRODUCTIONII. CONCEPTUAL DEFINITION OF CRITICAL PERIODSIII. BIOLOGICAL DEFINITION OF CRITICAL PERIODSIV. CRITICAL PERIODS IN SPEECH PERCEPTIONPhoneme Perception Audio-Visual Matching and Integration V. PROBING LANGUAGE CRITICAL PERIODSShifting Onset Timing Early Enrichment: Bilingual Experience Early Deprivation: Deafness and Cochlear Implants VI. LASTING IMPACT OF CRITICAL PERIOD DEVELOPMENTLater Language Acquisition Perceptual “Savings” VII. REOPENING CRITICAL PERIODSVIII. CONCLUSIONS & FUTURE DIRECTIONSCRITICAL PERIODS SPEECH PERCEPTION Page 3 of 50 Abstract A continuing debate in language acquisition research is whether there are Critical Periods (CPs) in development during which the system is most responsive to environmental input. Recent advances in neurobiology provide a mechanistic explanation of CPs, with the balance between excitatory and inhibitory processes establishing the onset and molecular brakes establishing the offset of windows of plasticity. In this chapter we review the literature on human speech perception development within the context of this CP model, highlighting research that reveals the interplay of maturational and experiential influences at key junctures in development and presenting paradigmatic examples testing CP models in human subjects. We conclude with a discussion of how a mechanistic understanding of CP processes changes the nature of the debate: the question is no longer “are there CPs”, but rather what processes open them, keep them open, close them, or allow them to be reopened. Keywords: infancy, language acquisition, attention, GABA, parvalbumin, perineuronal net CRITICAL PERIODS SPEECH PERCEPTION Page 4 of 50 I. INTRODUCTION The ability to acquire human language is one of the quintessential characteristics of our species. While many animals have communication systems, only human language allows the construction of an infinite number of new sentences to not only share needs and desires, but also to comment on the past and the future, to consider new possibilities, and to construct poetry and narrative. Human language is able to do this not only because humans have highly developed cognitive capabilities that support such complex thinking, but also because language itself has evolved to be richly structured, with multiple levels of interacting rules, from phonology, through morphology, syntax, and semantics. Remarkably, by 4-5 years of age, young children have mastered nearly all of the rules of their native language, and can produce and understand most structures with subsequent development being primarily one of increasing vocabulary. While infants don’t begin canonical babbling until 7-10 months, and don’t typically produce their first words until this age or later, they begin life with biological biases that support acquisition of language in general, and have already begun – at birth – the process of acquisition of the native language via perception of the surface level properties of the language(s) experienced. In this chapter we review the steps in perceptual development that support acquisition of the native language, and examine these steps within the context of a Critical (or Sensitive) Period framework (see also Doupe & Kuhl, 1999; Kuhl, 2010; and Friederici & Wartenburger, 2010; Werker & Tees, 2005, for earlier reviews). We begin by defining the notion of a critical period at both a conceptual and more recent biological levels. Then, in examining speech perception development, we first review the kinds of perceptual biases infants have for processing language CRITICAL PERIODS SPEECH PERCEPTION Page 5 of 50 prior to exposure to any specific language and the neural systems that are in place, even before birth, to direct and support language use. Next, we describe how perceptual attunement to the properties of the native language unfolds, beginning with the most global rhythmical properties of the native language, the subsequent use of rhythm to segment continuous speech into different sized units, and the perceptual narrowing from broad-based to more language specific discrimination of the speech sound differences that are used to distinguish one word from another in the native language(s). We describe briefly how the knowledge gained in perceptual attunement bootstraps acquisition of language proper. At each juncture, we consider the extent to which the system in question is subject to critical/sensitive period (hereafter referred to as CP) influences, versus the extent to which it is open from the outset and remains open, and what the consequences of openings and closings of CPs are when development and functional use unfold in such a cascading fashion. II. CONCEPTUAL DEFINITION OF CRITICAL PERIODS CPs have been observed in various systems across species (Hensch, 2004; Knudsen, 2004). Primary sensory areas in particular – the brain’s first filters to the outside world – exhibit especially striking examples of experience-induced plasticity during defined windows of early life. Such periods are needed to establish an optimal neural representation of the surrounding environment to guide future action. Given the extraordinary biological resources that must be devoted to rewiring neural circuitry, concentrating the construction of accurate, immutable maps early in life for use throughout adulthood may be an efficient strategy. However, this poses limitations on future revisions to the circuitry. Recent cellular and molecular insights indicate that biological mechanisms are expressed to ensure that adaptive changes are preferentially set in place early in life while leaving the door open for lifelong plasticity (Section III). CRITICAL PERIODS SPEECH PERCEPTION Page 6 of 50 The classic notion of a CP is a window, typically in early development, during which a system is open to structuring or restructuring on the basis of input from the environment. Before and after this period, environmental influences cannot affect the sensitivity or response properties of that particular system. While the timing of the initial opening of CPs is largely constrained by the maturation of underlying circuit readiness, early studies revealed that maturation is not the only contributing factor. Input is also necessary to trigger the opening of CPs: animals reared in the dark remain open to visual influences until a later maturational age, beyond which there is eventually a closing (see Hensch, 2005). Almost as soon as the concept of CPs was introduced, it began to be modified. It was found that even in the visual system, experience can have an impact at time points, outside of the CP, just not as profound. The alternate term, sensitive (or optimal) period was coined, with a focus on the fact that windows do not always open and shut abruptly, and may never close completely. With recent work showing that learning is possible throughout the lifespan (Bavelier & Davidson, 2013), even in systems once thought to be CP like – the debate has been reopened. What distinguishes this review from others is that we situate the age- and experience-related changes in speech perception within the context of newly emerging mechanistic models of how CPs work. III. BIOLOGICAL DEFINITION OF CRITICAL PERIODS Perhaps the best-studied model of a CP is the enduring loss of responsiveness in primary visual cortex (V1) to a “lazy” or otherwise deprived eye. The behavioral consequence, amblyopia (poor visual acuity), afflicts 2-5% of the human population and remains without a known cure in adulthood (Holmes & Clarke, 2006). From the initial discovery by Hubel and Wiesel 50 years ago, a biological picture has emerged wherein the two eyes’ inputs compete with CRITICAL PERIODS SPEECH PERCEPTION Page 7 of 50 each other upon first converging onto individual neurons in V1 (Wiesel & Hubel, 1963). Molecular tools have now begun to unravel the cellular mechanisms that control the onset and closure of such windows for cortical plasticity (see Table 1) (for recent reviews see Espinosa & Stryker, 2012; Levelt & Hübener, 2012; Takesian & Hensch, 2013). Overall, three key concepts have emerged (see Figure 1A): (1) Excitatory-inhibitory (E-I) circuit balance is a trigger. Specific GABA circuit maturation underlies the onset timing of plasticity and is shifted across brain regions consistent with the cascading nature of CPs (Hensch, 2004). Thus, premature gain-of-function by pharmacological agents (benzodiazepines) can trigger precocious onset, while genetic (GAD65 deletion) or environmental disruption (dark-rearing, hearing loss) of GABA circuit function lead to a CP delay (Hensch, 2005; Morales, Choi, & Kirkwood, 2002; Kotak, Takesian, & Sanes, 2008). Likewise, under conditions where sound space remains homogeneous across frequencies (white noise rearing), the tonotopic maps in primary auditory cortex (A1) remain immature and plasticity is delayed (Chang & Merzenich, 2003; de Villers-Sidani, Simpson, Lu, Lin, & Merzenich, 2008). These manipulations are so powerful that they can determine whether an animal is before, at the peak, or past a plastic window regardless of age. In other words, CP timing per se is plastic (see Figure 1B). Amidst the diversity of inhibitory cell types, it is the parvalbumin (PV)-positive large basket cell which serves as the pivotal plasticity switch (Hensch, 2005). Their role is to provide lateral inhibition to the somata of neighboring pyramidal cells, influencing action potential firing, back-propagation and rhythmic oscillations (in particular, at g-frequency; Sohal, Zhang, Yizhar, & Deisseroth, 2009). PV-circuits mature in response to a variety of factors, such as BDNF, PSA-NCAM or Otx2 homeo-protein, which appear just ahead of CP onset (see Takesian & CRITICAL PERIODS SPEECH PERCEPTION Page 8 of 50 Hensch, 2013). Transplantation of embryonic precursors for GABAergic neurons can then induce a second CP once the transplant reaches a particular maturational state (Southwell, Froemke, Alvarez-Buylla, Stryker, & Gandhi, 2010). Importantly, PV-cells mature at different rates across brain regions (Condé, Lund, & Lewis, 1996), potentially contributing to the cascading nature of CPs. How exactly GABA circuit maturation controls CP onset remains to be examined, but on theoretical grounds it has been proposed that inhibition may preferentially suppress responses to spontaneous relative to visually driven input activity, switching learning cues from internal to external sources (Toyoizumi et al., 2013). (2) Synaptic pruning and homeostasis mediate plasticity. Once PV-cells enter an optimal state, local circuit rewiring in response to sensory experience is enabled. They are the first responders to discordant sensory input, shifting their visual response rapidly (see Takesian & Hensch, 2013). Subsequently, a biochemical sequence is triggered, initially freeing synaptic space through the action of secreted proteases (tPA) to cleave cell-adhesion molecules (Hensch, 2005). This prunes away deprived inputs prior to sprouting of open eye connections in V1. Such homeostatic growth requires protein synthesis and glial factors like TNFa (Espinosa & Stryker, 2012). Directly disrupting intercellular adhesion molecules which regulate dendritic spine maturation shortens CP duration (Barkat, Polley, & Hensch, 2011), while enriched environments can extend it (see Figure 1C) (Brainard & Knudsen, 1998; Sale et al., 2007). (3) Molecular “brakes” limit adult plasticity. Eventually, brain plasticity winds down to stabilize the neural networks initially sculpted by experience. As PV-cells age, they gradually acquire an extracellular coating, called the peri-neuronal net (PNN). This structure tightly encapsulates the PV-cell body and proximal neurites, attracting Otx2 persistently from external sources and limiting further brain plasticity (Sugiyama et al., 2008; Spatazza et al., 2013). Thus, CRITICAL PERIODS SPEECH PERCEPTION Page 9 of 50 a second threshold of PV-cell state appears to maintain CP closure. In other words, the closure of CPs may reflect an active process in addition to the long-held view of declining plasticity factors. Late expression of several brake-like factors after the CP acts to limit excessive circuit rewiring (see Table 1) (Bavelier, Levi, Li, Dan, & Hensch, 2010). These include structural obstacles that physically prevent neurite pruning and outgrowth, such as PNN (Crtl1, C4st1) (Carulli et al., 2010; Miyata, Komatsu, Yoshimura, Taya, & Kitagawa, 2012) or myelin-related signals (including NgR and the immune gene PirB) (McGee, Yang, Fischer, Daw, & Strittmater, 2005; Syken, Grandpre, Kanold, & Shatz, 2006). In addition, functional brakes (e.g. Lynx1, serotonin reuptake) dampen the neuromodulatory systems (e.g. acetylcholine, serotonin) which endogenously regulate E-I circuit balance (Morishita, Miwa, Heintz, & Hensch, 2010; Maya Vetencourt et al., 2008). As CPs close, a more general epigenetic silencing of gene programs necessary for synaptic rewiring is observed (Putignano et al., 2007; Maya Vetencourt, Tiraboschi, Spolidoro, Castrén, & Maffei, 2011). Lifting any one of these brakes unmasks potent plasticity in adulthood (see Figure 1D). Windows of plasticity, therefore, arise between the maturation of an optimal E-I balance controlling the machinery of synaptic pruning and a later emerging consolidating set of brake-like factors, which persistently limit rewiring throughout adult life (see Figure 1A). Notably, the same principles are increasingly being observed across brain regions. Developmental pruning of climbing fiber inputs to Purkinje cells in the cerebellum is regulated by E-I balance (Nakayama et al., 2012). Fear extinction is highly labile and complete until PNNs emerge in the basolateral amygdala, rendering fear memories more permanent (Gogolla, Caroni, Lüthi, & Herry, 2009). Likewise, in zebra finches, PNNs emerge in key nuclei as the multi-step CP for song learning closes. Social isolate rearing, which delays CP timing, also delays PNN formation (Balmer, CRITICAL PERIODS SPEECH PERCEPTION Page 10 of 50 Carels, Frisch, & Nick, 2009). Adult mouse prefrontal cortex normally encodes acoustic preferences established during a CP early in life, but can be rendered malleable later by NgR deletion or histone deacetylase (HDAC) inhibitors (Yang, Lin, & Hensch, 2012). More recently, hippocampal learning was found to reflect bistable PV-cell states, focally recapitulating basic CP mechanisms throughout life (Donato, Rompani, & Caroni, 2013). IV. CRITICAL PERIODS IN SPEECH PERCEPTION The definitive examples of CPs involve fundamental sensory systems. Language, however, is an example of a higher level cognitive system governed by CP phenomena. In his classic work, Lenneberg (1967) put forward a maturational model of language acquisition, with a critical period at the onset of puberty. Since that time, it has become apparent that language acquisition is characterized by multiple critical and sensitive periods, with different onsets and offsets and different dynamics. There is a CP for the acquisition of morphosyntax, for example, with a sharp dip after 7-years of age (Johnson & Newport, 1989). There are even multiple sensitive periods for speech perception (which will be discussed in this chapter) which open and close at different points in development, with some apparently closing by the end of the 2nd year of life. And there are some aspects of language, like vocabulary acquisition, that seem to remain open across the life span. Speech processing shows both evolutionary and experience based influences from the earliest points in development at which the brain can support processing of such a complex signal. Anatomical organization that supports speech processing is evident in the human brain from as early as 29 weeks gestation, even prior to specific listening experience (Dehaene-Lambertz, Hertz-Pannier, Dubois, & Dehaene, 2008), with ventral projections from temporal to prefrontal areas at birth but dorsal connections from the auditory cortex terminating in premotor CRITICAL PERIODS SPEECH PERCEPTION Page 11 of 50 cortex (Brauer, Anwander, Perani, & Friederici, 2013). Functional imaging studies of newborn infants using both NIRS (Peña et al., 2003) and fMRI (Dehaene-Lambertz, Dehaene, & Hertz-Pannier, 2002), reveal greater activation over classic temporal and frontal languages areas in response to continuous speech over non-speech, with some studies revealing this specialization to be left hemisphere dominant at birth – as it is in adults (Peña et al., 2003), and other studies indicating it to be initially bilateral with increased left hemisphere specialization over the next several months (Perani et al., 2011). Importantly, while activation is greater to the native than to an unfamiliar language (May, Byers-Heinlein, Gervain, & Werker, 2011; Minagawa et al., 2011), classic language areas in the brain are more activated to both forward familiar and unfamiliar language than to backwards language (a non-speech control stimulus; us, others), and/or to other kinds of non-language, but equally complex signals (see Price, 2012, for a review). Similarly, the newborn brain reveals activation in classic speech processing areas in the left hemisphere in phonetic discrimination tasks (Dehaene-Lambertz & Gliga, 2004). Indeed, even at 28-32 weeks gestation, perisylvian areas are activated in the premature infant when discriminating phonemes (Mahmoudzadeh et al., 2013). Thus, at birth, the marks of broad biological preparedness as well as specific experience are evident. Over the next several months of life, infants become increasingly attuned to other properties of the native language, and the link between perceptual attunement and higher level processing becomes increasingly evident. As one example, at birth, infants can discriminate languages from different rhythmical classes (Mehler et al., 1988). Prenatal listening experience also plays a role: neonates show a preference for listening to languages that are from the same rhythmical class as those heard in utero (Moon, Cooper & Fifer, 1993; Mehler, et al, 1988). It is only at 4-5 months of age that infants are able to discriminate the native language from another CRITICAL PERIODS SPEECH PERCEPTION Page 12 of 50 language within the same rhythmical class, and to show a selective preference for the native language from another from within the same rhythmical class (see Nazzi & Ramus, 2003). The timing of attunement to within-class rhythmical characteristics appears to be maturationally constrained. Infants who are born up to 3 months premature only become capable of discriminating two languages from within the same rhythmical class after 5 months gestational age (8 months from birth in their case), even though they have had 3 more months of postnatal listening experience by that time (Peña, Pittaluga, & Mehler, 2010). These findings support the notion that the onset of this CP is constrained by maturation. As they become attuned to the rhythmical characteristics of the native language, and use that attunement to pull out constituent units, perceptual attunement to finer properties of the native language ensues. By 7 months of age, infants show a preference for the stress, melody, and phonotactics used in the native language (see Jusczyk, 2002) and can also use statistical regularities such as transitional probabilities to pull out probable units (Saffran, Aslin, & Newport, 1996). These sensitivities work together to enable infants to focus perceptual attention on individual words, and this in turn, may support the perceptual narrowing to the speech sound categories of the native language. Phoneme Perception The strongest evidence for CPs in perceptual attunement to the properties of the native language comes from work on phoneme discrimination. While the standard understanding is that experience functions to induce or sharpen initial perceptual sensitivities – and while this is indeed evident in speech perception development (see Kuhl, 2010, for a review), the vast majority of studies indicate that the ability to discriminate many of the consonant distinctions used across the world’s languages is present in young infants prior to specific listening CRITICAL PERIODS SPEECH PERCEPTION Page 13 of 50 experience, with the effect of listening experience to maintain (and sharpen) sensitivity to those distinctions used in the native language, and to show a decline in discrimination of non-native ones (see Maurer & Werker, 2014, for a review). Moreover, the onset of the opening of plasticity (of the CP) appears to be maturationally determined. The languages of the world use different speech sound inventories to distinguish meaning. English, but not Japanese, distinguishes /r/ from /l/ in words such as “rate” versus “late, and Japanese adults have difficulty discriminating this distinction. At birth, infants can discriminate sounds such as /ba/ versus /da/ (a place of articulation difference) or /da/ versus /ta/ (a voicing distinction), and do so using the same neural systems as activated in adult phoneme discrimination (Dehaene-Lambertz & Gliga, 2004). More importantly, discrimination sensitivity extends to non-native speech sound differences that the young infant has never before heard (Streeter, 1976; Trehub, 1976; Werker & Tees, 1984). The classic example of maintenance came from work reported by Werker and Tees in 1984. Young English-learning infants were shown to be able to discriminate two different d sounds that are used to contrast meaning in Hindi, but not English, but by 10-12 months, the English infants no longer succeeded while the Hindi-learning infants maintained sensitivity. This decline in non-native and maintenance or improvement in native perception, which has now been shown to be ubiquitous across a wide variety of speech sound contrasts (Maurer & Werker, 2013) as well as other aspects of perceptual development (Scott, Pascalis, & Nelson, 2007), is referred to as “perceptual narrowing”. In consonant discrimination, narrowing is seen between 8 and 10 months of age. Up to 8 months, infants reliably discriminate both native and non-native speech sound differences, but by 10-12 months of age, they have difficulty discriminating acoustically similar non-native contrasts (see Maurer & Werker, 2013, for a review). Similar CRITICAL PERIODS SPEECH PERCEPTION Page 14 of 50 effects have been shown for vowel discrimination (Polka & Werker, 1994), for discrimination of lexical tone (Mattock, Molnar, Polka, & Burnham, 2008), and for discrimination of the kinds of hand signs that are used in sign languages (Baker, Idsardi, Golinkoff, & Petitto, 2005). The fact that perception of so many different types of speech sound contrasts narrows at the same point in development is consistent with one of the characteristics of a CP. However, it should be noted that there is variability as well. Vowel perception may reorganize slightly earlier in development than does consonant perception, with changes in the internal structure of vowel categories evidence by as early as 6-8 months (Kuhl, Williams, Lacerda, Stevens, & Lindblom, 1992), and the beginnings of recognition of familiar vowel sounds even at birth (Moon, Lagercrantz, & Kuhl, 2013). Nonetheless, the decline in discrimination of two different non-native vowels occurs closer to the 10 month period seen for narrowing of consonants (Polka & Werker, 1994). Similarly, while the ability to discriminate between non-native lexical tones appears to narrow only between 6-8 and 8-10 months of life (Mattock et al., 2008; Yeung, KH Chen, & Werker, 2013), familiarity based changes in preference are evident months earlier (Yeung et al., 2013). Thus the nervous system is accruing and registering experience, yet discrimination sensitivity – even of non-native and never before heard speech sounds – is maintained until around 10-12 months. This 10-12 month time period appears to be under maturational control. Up to 10 months of age, infant perception of speech sounds is fairly easy to change. In a distributional learning paradigm, infants 6-8 months of age (Maye, Werker, & Gerken, 2002) show changes in speech sound categorization following as little as two minutes of exposure, with a bimodal frequency distribution during exposure leading them to bifurcate a continuum into two categories, and a unimodal distribution to collapse it into one. At 10-months of age, however, once native speech CRITICAL PERIODS SPEECH PERCEPTION Page 15 of 50 sound categories have begun to solidify, double the exposure is needed to bring about the same amount of change (Yoshida, Pons, Maye, & Werker, 2010). Thus 10-months appears to coincide with the beginning of the consolidation period (see Figure 1A). As the system moves toward consolidation, experiences that are more engaging are better able to bring about perceptual change than is passive listening experience. When exposed to Chinese speech in a contingent, interpersonal interaction, English infants aged 9-10 months maintain and reacquire sensitivity to Chinese (non-English) fricative contrasts (Kuhl, Tsao, & Liu, 2003), but do not do so with equivalent non-contingent input. Similarly, if two non-native consonants sounds are paired with two different objects in a quasi word-learning situation, infants aged 9-10 months also regain sensitivity to a non-native speech sound contrast (Yeung & Werker, 2009). Thus while 10-months may mark the beginning of the decline in plasticity, the closing appears to be more gradual (see Knudsen, 2004 for a discussion of such sensitive periods). Once native speech sound categories are in place, infants are able to use them to segment words (Jusczyk & Aslin, 1995), and to recognize familiar words (Mani & Plunkett, 2010; Swingley & Aslin, 2002). While there is instability in the first few months in infant’s ability to use native phonological categories to guide the learning of new words (Stager & Werker, 1997), they are able to succeed at 17 months (Werker, Fennell, Corcoran, & Stager, 2002) and beyond, and at younger ages when the computational load is made lighter (see Werker & Curtin, 2005 for a review). Audio-Visual Matching and Integration The mouth movements we make when we speak convey information that is consistent with that conveyed by the auditory signal. Adults integrate this seen information with what they CRITICAL PERIODS SPEECH PERCEPTION Page 16 of 50 hear. For example, it is easier to understand degraded speech if visual information from talking faces is also provided (Sumby & Pollack, 1954). Infants are sensitive to the visual information in speech from a very young age (e.g. Rosenblum, Schmuckler, & Johnson, 1997), and show neural integration of heard and seen speech from 10 weeks of age (Bristow et al., 2009; Kushnerenko, Teinonen, Volein, & Csibra, 2008). When presented with two side by side images of the same woman’s face either articulating “ee” or “ouu”, infants of 4 months (Kuhl & Meltzoff, 1982) and 2 months (Patterson & Werker, 2003), and possibly even newborns (Aldridge, Braga, Walton & Bower, 1999) look longer to the side that is articulating the sound that they hear. Infants this young can also match heard and seen consonants (MacKain, Studdert-Kennedy, Spieker, & Stern, 1983), and do so best when the matching face is on the right side, indicating involvement of the left hemisphere language areas. Just as infants can discriminate speech sound differences they have never before heard, they can also match heard (auditory, A) and seen (visual, V) vowels (Aldridge, Walton, & Bower, 1999) and consonants (Pons, Lewkowicz, Soto-Faraco, & Sebastián-Gallés, 2009) they have never before experienced. Moreover, there is perceptual narrowing by the end of the first year of life in AV matching just as there is in non-native speech phonetic discrimination. In Spanish, there is not a distinction between /ba/ and /va/. Spanish-learning infants can match heard and seen /ba/ and /va/ at 6 months old, but no longer do so at 10 months old (Pons et al., 2009). Young infants can also discriminate languages just by watching the articulatory movements in silent talking faces, and this capability also narrows in the first year of life. Following habituation to three bilingual French-English female speakers producing novel CRITICAL PERIODS SPEECH PERCEPTION Page 17 of 50 sentences in one of their native languages, and then tested with these same three speakers producing new sentences either in the old language (control condition) or the other language (the experimental condition) English-learning infants aged 4 and 6 months – but not 8 months – can discriminate the change, as evident in a recovery of looking time in the experimental but not the control conditions. However, infants growing up bilingual in English and French maintain sensitivity to the change in language at 8-months (Weikum et al., 2007), consistent with the ubiquitous ‘perceptual narrowing’ pattern. V. PROBING LANGUAGE CRITICAL PERIODS Shifting Onset Timing The most compelling evidence for a biologically determined onset to the sensitive period for phonetic attunement comes from a study with infants born approximately 12 weeks premature, but otherwise healthy. If perceptual narrowing to speech sound contrasts used only in the native language were driven entirely by amount of exposure, irrespective of age, one would predict that infants born premature would stop discriminating non-native contrasts at a younger age than full term infants. However, in an ERP study of discrimination of the Hindi /da/-/Da/ distinction, Peña, Werker and Dehaene (2012) found that infants born premature continued discriminating the Hindi (non-native) consonants at a chronological age that was approximately 12 weeks older than that of the full-term infants, that is, when they had reached the same gestational age (time from conception) as had the full-term infants. Similarly, a recent ERP study indicates that when listening to consonant-vowel syllables, the spontaneous neural responses to speech in premature infants does not show obvious effects of listening experience in the first several months after birth (Key, Lambert, Aschner, & Maitre, 2012). Thus it appears CRITICAL PERIODS SPEECH PERCEPTION Page 18 of 50 that prior to a critical point in maturation, even when environmental input is provided, the developing human brain does not begin to settle on the native speech sound categories. An understanding of the biological pathways that trigger the onset and offset of CPs positions one to probe those pathways to reinstate plasticity. In collaboration with W.M. Weikum and T.F. Oberlander, we did just that in a study of the timing of narrowing to the non-English, retroflex/dental (/da/-/Da/) distinction in English learning infants who had been exposed to different pharmacological or hormonal influences while in utero. We worked with a group of mothers who had experienced depression throughout their pregnancy and had chosen to either take anti-depressant (serotonin reuptake inhibitors) or to seek treatment without SRIs, and compared the speech perception development of their infants to the infants of a control group of mothers who had not experienced depression. The control infants discriminated the Hindi dental /da/ versus retroflex /Da/ at 6 but not 10 months of age, as in our previous work. As in the work from other labs, at 36 weeks gestation, when tested in utero using heart rate decline as the dependent variable, fetuses discriminated a minimal pair vowel contrast, but did not discriminate a minimal pair consonant difference, the voiced /da/ versus the voiceless /ta/. In the group of infants whose mothers had taken SRI throughout their pregnancy, results indicated that that prenatal exposure to SRIs had accelerated the entire speech perception trajectory: SRI exposed fetuses, at 36 weeks gestation, discriminated the vowel distinction but also already discriminated the /da/ versus /ta/ voicing contrast. Moreover, by 6 months of age SRI exposed infants had already stopped discriminating the Hindi dental /da/ versus retroflex /Da/ distinction. In comparison to the acceleration that SRI exposure seemed to cause, infants exposed to maternal depression that was not treated with SRIs continued to discriminate the CRITICAL PERIODS SPEECH PERCEPTION Page 19 of 50 Hindi dental /da/ versus retroflex /Da/ at 10 months of age (Weikum, Oberlander, Hensch, & Werker, 2012). An identical effect was seen for visual language discrimination. The control infants, whose mothers were not depressed, discriminated visual French from visual English at 6 but not at 10 months of age. Infants whose mothers had taken SRI medication had already stopped discriminating visual English and visual French at 6-months of age, while those infants whose depressed mothers had not taken SRIs, continued to discriminate the change even at 10 months, suggesting that their CP had been extended. Late gestational SRI exposure is known to disrupt auditory map formation in rodent A1 (Simpson et al., 2011). Developing circuits transiently express ectopic serotonergic receptors and transporters (Gaspar, Cases, & Maroteaux, 2003). While the primary effect of SRIs is to regulate the serotonergic system, a secondary effect may also boost GABAA receptor function like benzodiazepines. Thus, exposure to SRIs in utero may have adjusted E-I circuit balance to open the CP at a much earlier age (see Figure 1B). It is more difficult to postulate why exposure to maternal depression not treated with SRIs may have led to a delay in perceptual narrowing. One possibility is that maternal depression has its own hormonal sequelae to slow CP circuits from closing (see Figure 1D). The other, and equally likely explanation, is that maternal depression is like dark rearing. We know that depressed mothers use less “infant directed speech” (e.g. Kaplan, Bachorowski, Smoski, & Zinser, 2001) and interact with their infants in a less engaging, less contingent manner, and that highly engaging, contingent speech can boost learning (Kuhl, 2007). Thus, the infants of depressed mothers may not have had enough exposure to engaging speech to accrue the amount of experience necessary to trigger CP onset (see Figure 1B). CRITICAL PERIODS SPEECH PERCEPTION Page 20 of 50 Diet can also change CP timing. Exclusively breast-fed infants of vegetarian mothers who are missing essential fatty acids in their diet continue discriminating the non-native dental /da/ versus retroflex /Da/ after 10 months of age (Innis, Gilley, & Werker, 2001; see also Pivik, Andres, & Badger, 2012, for a more recent study showing an effect of diet on the neural response to speech). Thus, while CP onset is typically constrained by maturation, certain types of exposure/experience can accelerate the opening of plasticity. Early Enrichment: Bilingual Experience Infants who grow up bilingual ultimately narrow on to two sets of phonemic categories, one for each of their languages (Burns, Yoshida, Hill, & Werker, 2007). While most studies indicate such narrowing occurs in the same time frame as does narrowing for monolingual infants (Albareda-Castellot, Pons, & Sebastián-Gallés, 2011; Sundara, Polka, & Molnar, 2008) some studies indicate that bilingual-learning infants take longer to establish native phonetic catgories (Bosch & Sebastián-Gallés, 2003), and/or maintain sensitivity to non-native speech sound differences until an older age than do monolingual infants (Pi, Sebastián-Gallés, Werker, & Bonatti, in preparation; Petitto et al., 2012). Similarly, bilingual infants maintain the ability to discriminate two non-native languages visually after the age that monolingual infants can no longer do so (Sebastián-Gallés, Albereda, Weikum, & Werker, 2012). A later age of perceptual narrowing could result from the CP staying open longer because of less input in each language for the bilingual infant (see Figure 1B), or it could result from enhanced executive function and attentional focus. Some neuroimaging studies indicate that the neural circuitry supporting phonetic discrimination is less mature in bilingual than in same-aged monolingual infants (Garcia-Sierra et al., 2011), and/or is equally mature but involves different circuitry, specifically with greater connectivity to prefronal areas (Petitto et al., 2012). Similarly, CRITICAL PERIODS SPEECH PERCEPTION Page 21 of 50 some behavioral studies suggest phonetic discrimination is boosted in bilingual infants by attentional, executive abilities (see Conboy, Sommerville, & Kuhl, 2008) that come from being bilingual (Kovács & Mehler, 2009). Unpublished data (W.M. Weikum, personal communication) are more consistent with an “attentional advantage” over an “impoverished input” explanation, as bilingual infants are not delayed in the decline in visual language discrimination. Rather, they continue to discriminate languages visually even months beyond the age at which monolingual infants fail. Early Deprivation: Deafness and Cochlear Implants Under typical circumstances, the timing of opening of a CP determines the timing of its closing. However, as illustrated above with the visual system, both maturation and experience work together to bring about the end of a CP. This appears to be the case in speech perception as well, both for the timing of narrowing in general, and the timing of narrowing to specific instances. Infants who are born deaf are at considerable risk for permanent language impairment. As will be discussed below, while there is enormous variability across individuals, hearing aids and/or cochlear implants can enable many individuals to develop spoken language perception and production skills close to those of the hearing population, particularly if provided early in life (see Lyness, Woll, Campbell, & Cardin, 2013, for a review). Moreover, even without the reinstatement of hearing, the typical trajectory of language development can be achieved if a visual language (such as sign language) is provided early in life (Mayberry, Lock, & Kazmi, 2002). Thus, successful language acquisition, and its cascading CPs are independent of modality. CRITICAL PERIODS SPEECH PERCEPTION Page 22 of 50 People who are born congenitally deaf and only have their hearing reinstated via augmentation (hearing aids) or cochlear implants at some later point in development, can have been deprived of listening experience for several months. Yet, for these infants, both ERP measures of central auditory discrimination (Kral & Sharma, 2012) and behavioral measures of speech discrimination (e.g. Faulkner & Pisoni, 2013) indicate that plasticity may remain for a longer period of time than it does in infants who have been hearing from birth, with close to full recovery seen at the group level up to at least 3.5 years of age. Beyond that age, variability increases with some children deriving benefit and others not from CIs. By adulthood, it is very rare for substantial benefit to occur, although some variability is still seen. On the other hand, infants who have only partial deafness, for example through recurrent ear infections, may receive just enough input to allow reorganization to occur, but in this case, with impoverished input and subsequent sub-optimal phonetic perception (Clarkson, Eimas, & Marean, 1989). This may be akin to the distorting effects of noise versus silence on auditory organization in rats deprived of typical acoustic input in early life (Chang & Merzenich, 2003; de Villers-Sidani et al., 2008). Children who are born deaf have early access to visual, but not acoustic, speech. A higher percentage of these individuals will become proficient lip readers than hearing controls (Auer & Bernstein, 2007), and as a group, will show a life-time visual dominance in language processing and a life-time deficit in auditory-visual speech integration if their hearing was not corrected by 2-3 years of age (Schorr, Fox, van Wassenhove, & Knudsen, 2005). The advantage proffered is that across the life span, they maintain the ability to use visual information to augment a distorted (or masked) speech signal (Rouger et al., 2007). CRITICAL PERIODS SPEECH PERCEPTION Page 23 of 50 In illustration, Schorr and colleagues compared children 5-14 years old who had been born deaf but had received a cochlear implant at least a year prior to the time of testing to matched age children who had been hearing from birth. Children were tested on their ability to identify auditory only, visual only, and matching AV /pa/ and /ka, as well as the non-matching audio /pa/ with visual /ka/ (which results in a ‘ta’ percept for most adults). Children in both groups reliably identified the correct syllable in the single modality and matching AV conditions, but significantly more children from the hearing than the early deaf group reported an integrated /ta/ AV percept. Moreover, within the early deaf group, it was only those children who received a cochlear implant after age 2.5 years who showed significantly more difficulty in integration. And finally, when the hearing children failed to integrate, they showed auditory dominance and reported what they heard (audio /pa/) whereas when the early deaf children failed to integrated, they exhibited visual dominance and reported what they saw (visual /ka/) (Schorr et al., 2005). The reason for this CP effect can be explained at many levels. Behaviorally, while overall infants have a preference for looking at eyes, between 6 and 10-12 months of age, there is a shift to longer looking to the mouth (Lewkowicz & Hansen-Tift, 2012), a shift that arguably helps infants establish a better representation of the visual articulatory movements that coincide with heard speech (Lewkowicz & Hansen-Tift, 2012). In support, the most significant difference in looking to the mouth over the eyes is evident when the heard and seen stimuli do NOT match (Tomalski et al., 2013). Without the opportunity to listen at the same time that they watched, infants who were unable to hear during this period of development would have missed the opportunity to listen while watching. There is some indication from infants born deaf and later given cochlear implants that the CP for establishing higher level auditory objects, like phonological categories, may close earlier CRITICAL PERIODS SPEECH PERCEPTION Page 24 of 50 than the CP for establishing native phonetic sensitivities. Indeed, the few studies that have tested toddler’s ability to use phonological categories to guide word learning, suggest a CP for implantation by 12-14 months (Houston, Stewart, Moberly, Hollich, & Miyamoto, 2012). Infants who are implanted prior to 12 months old show no deficits in learning new words when taught and tested in standard laboratory tasks at 18-30 months old (Houston et al., 2012). However, infants who are implanted after 12-15 months perform significantly more poorly at learning new words in the toddler and preschool years. Moreover, there are lasting effects. Even across childhood, those children who were implanted prior to 1 year of age continue to achieve higher scores on both productive and receptive vocabulary tests than do children implanted even 6 months after that time (Houston, Ying, Pisoni, & Kirk, 2001). Thus while sensitivities established at earlier ages facilitate acquisition of higher level aspects of language in hearing infants, the early establishment of impoverished or distorted categories can have negative cascading effects in infants born deaf and who fail to receive early auditory input. A controversial question is the extent to which cross-modal plasticity in the auditory cortex, in particular activation by visual language input, might compromise subsequent auditory plasticity. According to some studies, without either acoustic or visual language input, metabolic activity in the language areas of the auditory cortex remains low and, akin to dark rearing, keeps plasticity open. Exposure to any language stimulus, including visual (sign) language, increases metabolic activity, leading to commitment to that input, and a subsequent decrease in openness to auditory language, and hence compromised success following cochlear implant (Lee et al., 2001). However, in the Lee and colleagues (2001) study, the children were 4 years and older – already beyond the optimal age for CIs. CRITICAL PERIODS SPEECH PERCEPTION Page 25 of 50 In more recent work, Lee and colleagues found that when degree of deafness, biological age, and age at implantation were controlled, hypermetabolic activity in prefrontal areas prior to implant (supporting executive, attentional processes), rather than hypometabolic activity in auditory cortex, was the best predictor of CI success (Lee et al., 2005). Moreover, many studies now indicate that rather than interfering with success, it is the cross-modal utilization of visual speech along with auditory speech that is the best predictor of success in post-CP implanted CI users (Doucet, Bergeron, Lassonde, Ferron, & Lepore, 2006). VI. LASTING IMPACT OF CRITICAL PERIOD DEVELOPMENT Later Language Acquisition Sensitivity to phonetic detail is necessary for learning the speech sound categories of the native language, and ultimately for using those reorganized speech sound categories to guide language acquisition. Molfese and Molfese (1985) were the first to provide evidence that speech discrimination in neonates (using ERPs) predicts language proficiency in. More recently, Tsao, Liu, and Kuhl (2004) found not only a positive relation between perception of native speech sound distinctions at 7 months of age and vocabulary growth at 18-24 months, but also a negative relation with sensitivity to non-native phonetic contrasts. A similar relation has been reported between infant speech perception and later reading success (see Kuhl, 2010). There are also relations between the ability to use phonological categories to guide word learning at 18 months and language proficiency at 3-4 years (Bernhardt, Kemp, & Werker, 2007). Moreover, those toddlers who are better able to use native phonological categories to guide word learning are better at rhyming and alliteration at 3 and 4 years old (Kemp, Berhnardt, Scott, & Werker, in preparation), both predictors of reading success. As such, the relation between phonetic perception in infancy and later reading is likely not direct, but instead is likely CRITICAL PERIODS SPEECH PERCEPTION Page 26 of 50 mediated through phonological processes (see Figure 2), as suggested as well in a recent review of neuroimaging data (Ramus, in press). Perceptual “Savings” Animal studies have revealed that early sensory experience may leave lasting traces that can be tapped when similar environments are encountered later in life. Barn owls raised with prisms acquire novel maps of inter-aural timing difference to match the displaced visual scene, which revert to the original map when the prisms come off (Knudsen, 2004). However, when faced with the same prisms in adulthood, the learned map is swiftly re-engaged despite not having been used for years (Knudsen, 1998). Similarly, a history of monocular vision enhances sensitivity of adult circuits to deprivation a second time even beyond the CP for amblyopia (Hofer, Mrsic-Flogel, Bonhoeffer, & Hübener, 2006) It is difficult to test whether there are lasting effects of early language experience, as, in most cases, there is interference from the first. However, studies of speech perception in adults who were adopted from one country to another as children, provide one way to test for lasting effect. The results indicate that with only occasional exposure to the first language, no more than an hour or so a month, sensitivity to the speech sound distinctions of the native language can be maintained (Oh, Jun, Knightly, & Au, 2003). However, if such exposure is not provided, there is little evidence of saving. Adults who had been adopted from Korea as children, into French families in isolated villages and thus had little further access to Korean after adoption, were no better able than French adults at discriminating the voicing distinctions used in Korean (Ventureya, Pallier, & Yoo, 2004). On the other hand, when retraining procedures are used, evidence of a lasting effect is seen. Following only 2 weeks of Korean study, adult Americans who had been adopted from CRITICAL PERIODS SPEECH PERCEPTION Page 27 of 50 Korea before 1 year of age were better able, following two weeks of Korean study at the university level, to discriminate the lenis versus aspirated Korean consonant distinctions than English L1 speakers with the same amount of Korean training (Oh, Au, & Jun, 2010). Similar findings were shown for children who had been adopted from India into American English homes (Singh, Liederman, Mierzejewski, & Barnes, 2011). And in our work, we found similar results for adult students of Hindi who had had exposure to Hindi in the first few years of life via a short family stay in India or a grandmother living with them in the first two years of their lives (Tees & Werker, 1984). Of interest, there may be an upper age limit beyond which reactivation of latent phonetic sensitivity can be successful, with one study showing success in adults under, but not over 40 years of age (Bowers, Mattys, & Gage, 2009). The evidence is even clearer for a lasting effect of early experience on visual language discrimination. While adults are much less able than infants to discriminate languages while watching silent talking faces, they do perform better than chance (Soto-Faraco et al., 2007). In a recent study, we found that in achieve those levels of success, the adults needed to have learned one of the two languages in early childhood (Weikum et al, 2013). VII. REOPENING CRITICAL PERIODS Animal models now indicate that the mature brain is intrinsically plastic and actively stabilized by a variety of brake-like factors in adult life (see Table 1). As a result, it is possible to reopen CP levels of plasticity by judicious lifting of these brakes. Two potent pathways by which to do this involve focused attention and epigenetics. The action of neuromodulators, such as the serotonin and nicotinic acetylcholine receptor signaling onto particular GABA neurons, acutely regulates E-I balance (Lee et al., 2010), effectively disinhibiting the local circuitry to enable adult learning (Letzkus et al., 2011; Donato et al., 2013; Brown, Sweetnam, Beange, CRITICAL PERIODS SPEECH PERCEPTION Page 28 of 50 Nahhirney, & Nashmi, 2012). In adult barn owls, active hunting can extend CP plasticity (Bergan, Ro, Ro, & Knudsen, 2005). Video games are particularly potent in engaging attentional mechanisms, which can be leveraged for enhanced learning (Bavelier & Davidson, 2013). Stimulation of the basal forebrain or vagus nerve raises neuromodulatory tone to produce CP plasticity in adult A1 (Kilgard & Merzenich, 1998; Engineer et al., 2011), sufficient to correct a rodent model of tinnitus. In V1, the Lynx1 protein was further identified as a brake-like factor that actively suppresses adult plasticity (Morishita, Miwa, Heintz, & Hensch, 2010). Genetic removal of Lynx1 or acetylcholinesterase inhibitor treatment of adult wild-type animals restores CP plasticity enabling recovery from amblyopia in adulthood. Likewise, phase 2 clinical trials with SRI are proceeding for the treatment of amblyopia, as these drugs were found to rescue amblyopia in a rodent model by acutely perturbing E-I balance, perhaps epigenetically (Maya Vetencourt et al., 2008; 2011). Interestingly, contemplative practices to focus attention may also achieve plasticity enhancement non-invasively both by engaging neuromodulatory systems (Slagter, Davidson, & Lutz, 2011), as well as producing epigenetic changes (Kaliman et al., 2014). Epigenetic signatures, such as DNA methylation, histone acetylation and phosphorylation accompany the closure of CPs (Putignano et al., 2007). Treating adult rodents with HDAC inhibitors also reopens plasticity and rescues amblyopia in V1 (Silingardi, Scali, Belluomini, & Pizzorusso, 2010), as well as alters preference to paired acoustic stimuli (Yang et al., 2012). Inspired by this biology, the same valproic acid (VPA) treatment of healthy young adult humans enables the acquisition of absolute pitch, again when trained concurrently (Gervain et al., 2013). Elimination of inhibitory synapses is a major component of adult visual plasticity (van Versendaal et al., 2012; Takesian & Hensch, 2013). Interestingly, prolonged sensory CRITICAL PERIODS SPEECH PERCEPTION Page 29 of 50 deprivation, such as dark-rearing or white-noise in adulthood may have related acute consequences on E-I balance (He, Hodos, & Quinlan, 2006; Zhou, Panizutti, de Villers-Sidani, Madeira, & Merzenich, 2011; Duffy & Mitchell, 2013). Whether comparable manipulations would reopen CPs in language acquisition remains to be determined. A continuing question is whether the age-related changes in phonetic perception involve a full loss of sensitivity, or whether there is still residual plasticity. Those consonant contrasts, such as the English/r/-/l/ and the Hindi /d/-/D/ that show the most robust evidence of perceptual attunement in infancy are the same ones that show the most resistance to training in adulthood. The loss is not absolute, however. With systematic training significant improvement on discrimination of non-native contrasts can be induced (e.g. Bradlow, Pisoni, Akahane-Yamada, & Tokhura, 1997; McCandliss, Fiez, Protopapas, Conway & McClelland, 2002; Lively, Pisoni, Yamada, Tokhura, & Yamade, 1994), particularly when feedback is provided (Lively et al., 1994) or the training progresses from the easiest to the most difficult tokens (Ingvalson, Holt, & McClelland, 2012). Notably, there are large individual differences in performance following training (McCandliss et al., 2002), with one predictor of success the thickness of white matter tracts in Heschel’s Gyrus in the left hemisphere (Golestani, Molko, Dehaene, LeBihan, & Pallier, 2007). Nonetheless, even when significant improvement is induced, training seldom leads to improvements to the level of native speakers (e.g. Bradlow et al., 1997). Finally, the improvements reported at the level of speech sound (phonetic) discrimination are seldom generalizable to new syllables or new speakers (Ingvalson, McClelland, & Holt, 2011), nor can the phonetic sensitivities that have been trained be used to segment or recognize words in continuous speech (e.g. Pallier, Bosch, & Sebastián-Gallés, 1997). Thus the limited recovery in phonetic discrimination that is seen does not facilitate phonological use. CRITICAL PERIODS SPEECH PERCEPTION Page 30 of 50 VIII. CONCLUSIONS & FUTURE DIRECTIONS In summary, infants begin life with a set of perceptual biases, learning mechanisms, and neural systems that orient them to language, that provide an initial foundation for categorization, and that allow them to learn the properties of the native language. Infants become attuned to these properties in a sequential fashion, beginning with the most global prosodic characteristics of the native language and eventually to detailed phonetic analysis. In at least some cases, the timing of attunement appears to under maturational control, suggesting the operation of a critical or sensitive period. The perceptual attunement to native language characteristics supports acquisition of the relevant structures, for example, of cues to word order or of word-meaning mappings. Moreover attunement of the properties at each tier enables more focused attention to the next level of specificity. It is often claimed that because there is lifetime plasticity, CPs are moot – but that misses the point. There are biologically verifiable CPs, beyond which the brain works hard to maintain stability. By understanding what the processes are that function to maintain stability (molecular “brakes”), we may figure out how to remove those brakes and reopen plasticity. The opening and closing of a CP is like opening and then locking a door. Once the key is turned or combination set, the door is locked. However, if one has the key, or knows the combination, the door can be unlocked. The exciting work in neurobiology over the last 15 years has provided information on how that unlocking is done (Takesian & Hensch, 2013). Based on these new advances in neurobiology, a more objective mechanistic definition of CP timing as a consequence of maturational state is within reach. Future directions may combine animal models with human work as illustrated above. For example, despite the long-postulated parallels of birdsong and human language acquisition (Doupe & Kuhl, 1999), only CRITICAL PERIODS SPEECH PERCEPTION Page 31 of 50 recently has mechanistic work been done with respect to CPs (Balmer et al., 2009). In the barn owl system, incremental training is effective in producing cumulative large changes in auditory maps (Linkenhoker & Knudsen, 2002). In addition, one can now carefully examine human populations with molecular markers in mind (see Table 1). Methods borrowed from experimental neuroscience, such as serendipitous pharmacology or epigenetic profiling, can be applied to track the trajectory of human language acquisition. Notably, many mental illnesses that include language impairment are of neurodevelopmental origin, such as schizophrenia and autism, and share defects in the triggers and brakes that normally regulate CP timing (Insel, 2010; Rubenstein & Merzenich, 2003; Gogolla et al., 2009b). 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Natural restoration of critical period plasticity in the juvenile and adult primary auditory cortex. J Neurosci. 31:5625-34 CRITICAL PERIODS SPEECH PERCEPTION Page 48 of 50 Acknowledgements The authors thank Dr. Padmapriya Kandhadai for the invaluable comments she provided on an earlier version of the manuscript, and Savannah Nijeboer for creation of the figures. The authors also gratefully acknowledge support from the Canadian Institute for Advanced Research (JFW and TKH), the Human Frontier Science Program (JFW and TKH), the National Sciences and Engineering Research Council of Canada (JFW), the Bezos Family Foundation (TKH), and the National Institute of Mental Health (TKH). CRITICAL PERIODS SPEECH PERCEPTION Page 49 of 50 Figure Captions Figure 1. This figure illustrates recent biological insight into CP time course. Slow maturation of E-I circuit balance (in particular PV-cells) determines the initial onset and ultimate closure of a window of brain plasticity (A). As a result, CP timing per se is malleable, allowing for precocious, delayed, extended, dampened or reopened plasticity (B-D). The latter involves the removal of molecular “brakes” which are expressed in adulthood to stabilize and consolidate otherwise plastic circuitry. Figure 2. This figure illustrates the cascading nature [dotted arrows] of the steps in perceptual development [colored boxes] that guide acquisition of the native language. Each step has a different critical (or sensitive) period [solid line curves]. The opening, closing, and duration of each of these periods can be altered by sensory deprivation, pharmacological exposure, and linguistic experience [dashed lined curves], ultimately influencing language outcomes (e.g. vocabulary size, reading). CRITICAL PERIODS SPEECH PERCEPTION Page 50 of 50 Table Table 1. Summary of the biological and linguistic manipulations that alter critical period states Critical period state Biological manipulation Linguistic manipulation Onset • Sensory deprivation (e.g. white noise / dark-rearing) • E-Ia circuit maturation (GAD65b, BDNFd, Otx2c, PSA-NCAMe) • Premature birth • SRIf exposure • Maternal depression • Cochlear implant Duration • Synapse pruning / homeostasis (e.g. tPAg, Icam5h, TNFai protein synthesis) • Environmental enrichment • Bilingual experience • Diet Closure • Molecular brakes (e.g. myelin, PNNj, Crtl1k, C4st1l, NgRm, PirBn, Lynx1o, HDACp) • Attentional arousal • Valproate exposure • Video games a Abbreviation: E-I, excitatory-inhibitory. b Abbreviation: GAD65, glutamic acid decarboxylase 65kDa isoform. c Abbreviation: BDNF, brain-derived neurotrophic factor. d Abbreviation: Otx2, orthodenticle homeobox 2. e Abbreviation: PSA-NCAM, polysialylated-neuronal cell adhesion molecule. f Abbreviation: SRI, serotonin reuptake inhibitor. g Abbreviation: tPA, tissue plasminogen activator. h Abbreviation: Icam5, intercellular adhesion molecule 5. i Abbreviation: TNFa, tissue necrosis factor a. j Abbreviation: PNN, perineuronal net. k Abbreviation: Crtl1, cartilage link protein. l Abbreviation: C4st1, chondroitin 4-O-sulfotransferase-1. m Abbreviation: NgR, Nogo receptor. n Abbreviation: PirB, paired-immunoglobulin like receptor-B. o Abbreviation: Lynx1, Ly6/neurotoxin 1. p Abbreviation: HDAC, histone deacetylase. Age E I E I E I Neural Plasticity CRITICAL PERIOD Immature Plastic Consolidated BRAKES PV FUNCTION BRAKES Plas%city Extended Precocious Delayed / Reopened Plas%city Never opened Never closed Plas%city B. C. D. Age Age Age A. Dampened Narrowed WORD FORMS LANGUAGE OUTCOMES PHONOLOGICAL CATEGORIES LANGUAGE DISCRIMINATION Plasticity Age (months) 0 4 6 8 10 12 14 16 18 20 NATIVE PHONETIC CATEGORIES
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