Plasticity of Temporal Pattern Codes for Vocalization Stimuli in Primary Auditory Cortex

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Abstract
It has been suggested that “call-selective” neurons may play an important role in the encoding of vocalizations in primary auditory cortex (A1). For example, marmoset A1 neurons often respond more vigorously to natural than to time-reversed twitter calls, although the spectral energy distribution in the natural and time-reversed signals is the same. Neurons recorded in cat A1, in contrast, showed no such selectivity for natural marmoset calls. To investigate whether call selectivity in A1 can arise purely as a result of auditory experience, we recorded responses to marmoset calls in A1 of naive ferrets, as well as in ferrets that had been trained to recognize these natural marmoset calls. We found that training did not induce call selectivity for the trained vocalizations in A1. However, although ferret A1 neurons were not call selective, they efficiently represented the vocalizations through temporal pattern codes, and trained animals recognized marmoset twitters with a high degree of accuracy. These temporal patterns needed to be analyzed at timescales of 10–50 ms to ensure efficient decoding. Training led to a substantial increase in the amount of information transmitted by these temporal discharge patterns, but the fundamental nature of the temporal pattern code remained unaltered. These results emphasize the importance of temporal discharge patterns and cast doubt on the functional significance of call-selective neurons in the processing of animal communication sounds at the level of A1.