Abstract

It is well established that auditory cortex is plastic on different time scales and that this plasticity is driven by the reinforcement that is used to motivate subjects to learn or to perform an auditory task. Motivated by these findings, we study in detail properties of neuronal firing in auditory cortex that is related to reward feedback. We recorded from the auditory cortex of two monkeys while they were performing an auditory categorization task. Monkeys listened to a sequence of tones and had to signal when the frequency of adjacent tones stepped in downward direction, irrespective of the tone frequency and step size. Correct identifications were rewarded with either a large or a small amount of water. The size of reward depended on the monkeys’ performance in the previous trial: it was large after a correct trial and small after an incorrect trial. The rewards served to maintain task performance. During task performance we found three successive periods of neuronal firing in auditory cortex that reflected (1) the reward expectancy for each trial, (2) the reward-size received, and (3) the mismatch between the expected and delivered reward. These results, together with control experiments suggest that auditory cortex receives reward feedback that could be used to adapt auditory cortex to task requirements. Additionally, the results presented here extend previous observations of non-auditory roles of auditory cortex and shows that auditory cortex is even more cognitively influenced than lately recognized.

Highlights

  • It is widely acknowledged that auditory cortex, like many other cortical regions, remains plastic during adulthood (e.g., Dahmen and King, 2007)

  • Out of a total of 626 multiunits recorded from two macaque monkeys during the performance of an auditory categorization task with a performance-dependent reward schedule, we observed that neuronal firing in auditory cortex reflected: (i) the reward expectancy for the upcoming trial, (ii) the size of the reward obtained in a trial, and (iii) the mismatch between the expected and the received reward in a trial

  • This study clearly demonstrates that the firing of neurons in auditory cortex represents different aspects of the reward feedback that is used to motivate monkeys to perform an auditory categorization task

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Summary

Introduction

It is widely acknowledged that auditory cortex, like many other cortical regions, remains plastic during adulthood (e.g., Dahmen and King, 2007). A prerequisite for many of these changes is the establishment of appropriate cognitive associations between auditory stimuli, behavior, and reinforcement (Blake et al, 2006), which is under control of various neuromodulatory systems (Thiel et al, 2002; Suga and Ma, 2003; Weinberger, 2007). While the conditions resulting in auditory cortex plasticity are well understood, little is known about reinforcement signals reaching auditory cortex or other sensory cortices. Reinforcement is required for learning new tasks and to avoid extinction, i.e., to maintain appropriate sensory motor mappings, in classically and instrumentally conditioned animals, or for selecting between such previously learned mappings. Reinforcement can be mediated both by appetitive (rewarding) and aversive stimuli

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