Localist versus distributed representation of sounds in the auditory cortex controlled by distinct inhibitory neuronal subtypes

Abstract

ABSTRACTCortical neuronal populations can use a multitude of codes to represent information, each with different advantages and trade-offs. The auditory cortex represents sounds via a sparse code, which lies on the continuum between a localist representation with different cells responding to different sounds, and a distributed representation, in which each sound is encoded in the relative response of each cell in the population. Being able to dynamically shift the neuronal code along this axis may help with a variety of tasks that require categorical or invariant representations. Cortical circuits contain multiple types of inhibitory neurons which shape how information is processed within neuronal networks. Here, we asked whether somatostatin-expressing (SST) and vasoactive intestinal peptide-expressing (VIP) inhibitory neurons may have distinct effects on population neuronal codes, differentially shifting the encoding of sounds between distributed and localist representations. We stimulated optogenetically SST or VIP neurons while simultaneously measuring the response of populations of hundreds of neurons to sounds presented at different sound pressure levels. SST activation shifted the neuronal population responses toward a more localist code, whereas VIP activation shifted them towards a more distributed code. Upon SST activation, sound representations became more discrete, relying on cell identity rather than strength. In contrast, upon VIP activation, distinct sounds activated overlapping populations at different rates. These shifts were implemented at the single-cell level by modulating the response-level curve of monotonic and nonmonotonic neurons. These results suggest a novel function for distinct inhibitory neurons in the auditory cortex in dynamically controlling cortical population codes.