Impact of precisely-timed inhibition of gustatory cortex on taste behavior depends on single-trial ensemble dynamics.

Narendra Mukherjee,Donald B Katz,Joseph Wachutka

doi:10.7554/elife.45968

Abstract

Sensation and action are necessarily coupled during stimulus perception - while tasting, for instance, perception happens while an animal decides to expel or swallow the substance in the mouth (the former via a behavior known as 'gaping'). Taste responses in the rodent gustatory cortex (GC) span this sensorimotor divide, progressing through firing-rate epochs that culminate in the emergence of action-related firing. Population analyses reveal this emergence to be a sudden, coherent and variably-timed ensemble transition that reliably precedes gaping onset by 0.2-0.3s. Here, we tested whether this transition drives gaping, by delivering 0.5s GC perturbations in tasting trials. Perturbations significantly delayed gaping, but only when they preceded the action-related transition - thus, the same perturbation impacted behavior or not, depending on the transition latency in that particular trial. Our results suggest a distributed attractor network model of taste processing, and a dynamical role for cortex in driving motor behavior.

Highlights

One of the primary purposes of sensory processing is to drive action, such that the source of sensory information is either acquired or avoided
Our results provide strong support for the hypothesized importance of the transition time itself, and in addition suggest that important pre-transition taste processing is performed within gustatory cortex (GC)
Our results demonstrate that the impact of brief optogenetic perturbation of GC activity depends both on when that perturbation occurs and on precisely what state the brain has achieved prior to that perturbation

Summary

Introduction

One of the primary purposes of sensory processing is to drive action, such that the source of sensory information is either acquired or avoided (in the process generating new sensory input; Prinz, 1997; Wolpert and Kawato, 1998; Wolpert and Ghahramani, 2000). Ensemble analyses further reveal that the transition between these two epochs happens suddenly and coherently within neural ensembles (Jones et al, 2007; Sadacca et al, 2016). This ensemble transition to palatability coding, though highly variable in latency (between 0.5 and 1.5s post stimulus, depending on the trial), is Mukherjee et al eLife 2019;8:e45968.

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Results

Conclusion