Neuronal activity in sensory cortex predicts the specificity of learning in mice

Katherine C Wood,Maria N Geffen,Karmi Oxman,Claudia Clopath,Christopher F Angeloni

doi:10.1038/s41467-022-28784-w

Katherine C Wood, Maria N Geffen + Show 3 more

Open Access

https://doi.org/10.1038/s41467-022-28784-w

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Abstract

Learning to avoid dangerous signals while preserving normal responses to safe stimuli is essential for everyday behavior and survival. Following identical experiences, subjects exhibit fear specificity ranging from high (specializing fear to only the dangerous stimulus) to low (generalizing fear to safe stimuli), yet the neuronal basis of fear specificity remains unknown. Here, we identified the neuronal code that underlies inter-subject variability in fear specificity using longitudinal imaging of neuronal activity before and after differential fear conditioning in the auditory cortex of mice. Neuronal activity prior to, but not after learning predicted the level of specificity following fear conditioning across subjects. Stimulus representation in auditory cortex was reorganized following conditioning. However, the reorganized neuronal activity did not relate to the specificity of learning. These results present a novel neuronal code that determines individual patterns in learning.

Highlights

Learning to avoid dangerous signals while preserving normal responses to safe stimuli is essential for everyday behavior and survival
We found that the changes in stimulus representation in auditory cortex (AC) following fear conditioning were not correlated with the level of learning specificity across subjects, suggesting that the role of AC in fear learning is restricted to the consolidation period and changes in AC do not represent fear memory
Longitudinal imaging of neuronal activity in large ensembles of neurons in layers 2 and 3 of AC before and after conditioning (Fig. 1a) allowed us to compare the representation of the CS stimuli before and after learning

Summary

Introduction

Learning to avoid dangerous signals while preserving normal responses to safe stimuli is essential for everyday behavior and survival. Our second goal was to test the role of changes in auditory cortex in shaping fear learning specificity across subjects To address these goals, we imaged the activity of neuronal ensembles in layers 2 and 3 of AC over weeks, before and after differential fear conditioning with pure tones. We found that the changes in stimulus representation in AC following fear conditioning were not correlated with the level of learning specificity across subjects, suggesting that the role of AC in fear learning is restricted to the consolidation period and changes in AC do not represent fear memory These findings refine our understanding of the neuronal code for variability in fear learning across subjects and reconcile seemingly conflicting previous results on the function of the auditory cortex in fear learning

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