Cortical Recruitment Determines Learning Dynamics and Strategy

Sebastian Ceballo,Jacques Bourg,Simon Rumpel,Brice Bathellier,Alexandre Kempf,Aurrlie Daret,Zuzanna Piwkowska,Thomas Deneux

doi:10.2139/ssrn.3155899

Abstract

Salience is a broad and widely used concept in neuroscience whose neuronal correlates, however, remain elusive. In behavioral conditioning, salience is used to explain various effects, such as stimulus overshadowing, and refers to how fast and strongly a stimulus is associated to a conditioned event. Here, we show that sounds of diverse quality, but equally intense and perceptually detectable, recruit surprisingly different levels of population activity in mouse auditory cortex. When using these sounds as cues in a Go/NoGo discrimination task, the degree of cortical recruitment matches the salience parameter of a reinforcement learning model used to analyze learning speed. Moreover, we confirm a generic prediction of the model by training mice to discriminate light sculpted optogenetic activity patterns in auditory cortex verifying that cortical recruitment causally determines association or overshadowing of the stimulus components. This demonstrates that cortical recruitment captures major aspects of stimulus salience during reinforcement learning.

Highlights

Salience is a broad and widely used concept in neuroscience whose neuronal correlates, remain elusive
Using auditory discrimination tasks of sounds with different global cortical response strengths, we show that cortical recruitment impacts learning dynamics[24,25] to the salience parameter of a reinforcement learning model
Large scale two-photon imaging, optogenetics, and theoretical modeling, we have shown that sounds of different quality but equal mean pressure levels can recruit highly variable levels of neuronal activity in auditory cortex, measured as the mean amount of activity in a representative subsample of neurons

Summary

Introduction

Salience is a broad and widely used concept in neuroscience whose neuronal correlates, remain elusive. When behavior reaches maximal performance and learning stops, the more salient of the two stimuli has been associated more strongly with the unconditioned stimulus, leading to overshadowing While this theory captures a number of phenomena and is the basis for important frameworks such as reinforcement learning[4,5], the neural underpinnings of the salience parameter remain elusive. To explore this result in more precise experimental settings, we trained mice to discriminate optogenetically driven response patterns that elicit different levels of cortical activity Using this paradigm, we directly demonstrate that cortical recruitment determines which part of a compound stimulus drives a learned association while “overshadowing” other parts of the stimulus. This validates a generic prediction of reinforcement learning models and causally establishes the role of cortical recruitment as a neuronal correlate of stimulus salience

Methods

Results

Conclusion