Neuronal On- and Off-type heterogeneities improve population coding of envelope signals in the presence of stimulus-induced noise.

Understanding the mechanisms by which neuronal population activity gives rise to perception and behavior remains a central question in systems neuroscience. Such understanding is complicated by the fact that natural stimuli often have complex structure. Here we investigated how heterogeneities within a sensory neuron population influence the coding of a noisy stimulus waveform (i.e., the noise) and its behaviorally relevant envelope signal (i.e., the signal). We found that On- and Off-type neurons displayed more heterogeneities in their responses to the noise than in their responses to the signal. These differences in heterogeneities had important consequences when quantifying response similarity between pairs of neurons. Indeed, the larger response heterogeneity displayed by On- and Off-type neurons made their pairwise responses to the noise on average more independent than when instead considering pairs of On-type or Off-type neurons. Such relative independence allowed for better averaging out of the noise response when pooling neural activities in a mixed-type (i.e., On- and Off-type) than for same-type (i.e., only On-type or only Off-type), thereby leading to greater information transmission about the signal. Our results thus reveal a function for the combined activities of On- and Off-type neurons towards improving information transmission of envelope stimuli at the population level. Our results will likely generalize because natural stimuli across modalities are characterized by a stimulus waveform whose envelope varies independently as well as because On- and Off-type neurons are observed across systems and species.