Invariant neural responses for sensory categories revealed by the time-varying information for communication calls

Although information theoretic approaches have been used extensively in the analysis of the neural code, they have yet to be used to describe how information is accumulated in time while sensory systems are categorizing dynamic sensory stimuli such as speech sounds or visual objects. Here, we present a novel method to estimate the cumulative information for stimuli or categories. We further define a time-varying categorical information index that, by comparing the information obtained for stimuli versus categories of these same stimuli, quantifies invariant neural representations. We use these methods to investigate the dynamic properties of avian cortical auditory neurons recorded in zebra finches that were listening to a large set of call stimuli sampled from the complete vocal repertoire of this species. We found that the time-varying rates carry 5 times more information than the mean firing rates even in the first 100 ms. We also found that cumulative information has slow time constants (100–600 ms) relative to the typical integration time of single neurons, reflecting the fact that the behaviorally informative features of auditory objects are time-varying sound patterns. When we correlated firing rates and information values, we found that average information correlates with average firing rate but that higher-rates found at the onset response yielded similar information values as the lower-rates found in the sustained response: the onset and sustained response of avian cortical auditory neurons provide similar levels of independent information about call identity and call-type. Finally, our information measures allowed us to rigorously define categorical neurons; these categorical neurons show a high degree of invariance for vocalizations within a call-type. Peak invariance is found around 150 ms after stimulus onset. Surprisingly, call-type invariant neurons were found in both primary and secondary avian auditory areas.Author summary: Just as the recognition of faces requires neural representations that are invariant to scale and rotation, the recognition of behaviorally relevant auditory objects, such as spoken words, requires neural representations that are invariant to the speaker uttering the word and to his or her location. Here, we used information theory to investigate the time course of the neural representation of bird communication calls and of behaviorally relevant categories of these same calls: the call-types of the bird’s repertoire. We found that neurons in both the primary and secondary avian auditory cortex exhibit invariant responses to call renditions within a call-type, suggestive of a potential role for extracting the meaning of these communication calls. We also found that time plays an important role: first, neural responses carry significantly more information when represented by temporal patterns calculated at the small time scale of 10 ms than when measured as average rates and, second, this information accumulates in a non-redundant fashion up to long integration times of 600 ms. This rich temporal neural representation is matched to the temporal richness found in the communication calls of this species.