Spatiotemporal refinement of signal flow through association cortex during learning

Ariel Gilad,Fritjof Helmchen

doi:10.1038/s41467-020-15534-z

Ariel Gilad, Fritjof Helmchen

Open Access

https://doi.org/10.1038/s41467-020-15534-z

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Abstract

Association areas in neocortex encode novel stimulus-outcome relationships, but the principles of their engagement during task learning remain elusive. Using chronic wide-field calcium imaging, we reveal two phases of spatiotemporal refinement of layer 2/3 cortical activity in mice learning whisker-based texture discrimination in the dark. Even before mice reach learning threshold, association cortex—including rostro-lateral (RL), posteromedial (PM), and retrosplenial dorsal (RD) areas—is generally suppressed early during trials (between auditory start cue and whisker-texture touch). As learning proceeds, a spatiotemporal activation sequence builds up, spreading from auditory areas to RL immediately before texture touch (whereas PM and RD remain suppressed) and continuing into barrel cortex, which eventually efficiently discriminates between textures. Additional correlation analysis substantiates this diverging learning-related refinement within association cortex. Our results indicate that a pre-learning phase of general suppression in association cortex precedes a learning-related phase of task-specific signal flow enhancement.

Highlights

Association areas in neocortex encode novel stimulus-outcome relationships, but the principles of their engagement during task learning remain elusive
We find learning-related cortical changes—especially in posterior association areas—that we divide into two phases: First, a pre-learning phase, showing suppression in several association areas, followed secondly by an enhancement of a specific task-related cortical activation sequence that emerges in parallel to increasing task proficiency
They were punished with white noise for incorrectly licking for the no-go texture (‘false alarm’ trials, FA) and neither rewarded nor punished when they withheld licking for the go and no-go textures (‘Miss’ and ‘correct-rejection’, CR, trials, respectively)

Summary

Introduction

Association areas in neocortex encode novel stimulus-outcome relationships, but the principles of their engagement during task learning remain elusive. Using chronic wide-field calcium imaging, we reveal two phases of spatiotemporal refinement of layer 2/3 cortical activity in mice learning whisker-based texture discrimination in the dark. With respect to spatial dimension, we previously measured large-scale cortical dynamics with wide-field calcium imaging in mice trained to discriminate two texture types with their whiskers in a go/no-go task[11]. Regarding the third dimension of learning progression, most studies either only compare expert to naïve mice[1,2,3,5,13,25] (i.e. two time points) or sample learning daily (i.e. 3–8 time points[4,6,7]; but see[9,26]) Such low sampling frequency precludes resolving the trial-by-trial development of learning, which in some animals is rather rapid. We study spatiotemporal cortical dynamics during learning by performing wide-field calcium imaging across neocortex in mice learning a whisker-based texture discrimination task. We find learning-related cortical changes—especially in posterior association areas—that we divide into two phases: First, a pre-learning phase, showing suppression in several association areas, followed secondly by an enhancement of a specific task-related cortical activation sequence that emerges in parallel to increasing task proficiency

Methods

Results

Conclusion