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The role of neural correlations in information coding Metzen, Michael


The role of correlated neural activity in neural coding remains controversial. Here we show that correlated neural activity can provide information about particular stimulus features independently of single neuron activity using the weakly electric fish, Apteronotus leptorhynchus as an animal model. These fish generate an electric organ discharge (EOD) surrounding their body, the amplitude of which is encoded in the discharge of electroreceptors (P-units) that synapse onto pyramidal neurons in the hindbrain electrosensory lateral line lobe (ELL) that in turn synapse onto neurons within the midbrain Torus semicircularis (TS). When two conspecifics come into close proximity, each fish experiences a sinusoidal amplitude modulation (i.e. beat) with a frequency that is equal to the difference between both EOD frequencies. The beat can be further modulated due to movements of the animals, thus creating an envelope. Furthermore, these fish can generate communication signals or chirps (i.e. electrosensory “objects”) that consist of transient increases in EOD frequency and always occur simultaneously with the beat under natural conditions. The pairwise correlation coefficient but not single neuron spiking activity: 1) can reliably be used to predict the stimulus envelope and 2) allows for the emergence of a feature invariant representation of natural communication stimuli that is actually exploited by the electrosensory system. Moreover, information carried by correlated neural activity at the periphery is decoded and further refined in downstream brain areas. Finally, this gives rise to similar behavioral responses to stimulus waveforms associated with a given electrosensory object. As such, correlated activity codes for stimulus attributes that are distinct from those coded by firing rate and provide a novel role for neural variability. Furthermore, correlated neural activity is invariant to identity preserving transformations of natural stimuli. This reveals how a sensory system exploits this fact in order to implement the emergence and refinement of invariant neural representations of natural stimuli and how these mediate perception and behavior. The associated neural circuits are generic and thus likely to be found across systems and species.

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