Auditory cortex reflects goal-directed movement but is not necessary for behavioral adaptation in sound-cued reward tracking

J Neurophysiol. 2020 Oct 1;124(4):1056-1071. doi: 10.1152/jn.00736.2019. Epub 2020 Aug 26.

Abstract

Mounting evidence suggests that the role of sensory cortices in perceptual decision making goes beyond the mere representation of the discriminative stimuli and additionally involves the representation of nonsensory variables such as reward expectation. However, the relevance of these representations for behavior is not clear. To address this issue, we trained rats to discriminate sounds in a single-interval forced-choice task and then confronted the animals with unsignaled blockwise changes of reward probabilities. We found that unequal reward probabilities for the two choice options led to substantial shifts in response bias without concomitant reduction in stimulus discrimination. Although decisional biases were on average less extreme than required to maximize overall reinforcement, a model-based analysis revealed that rats managed to harvest >97% of rewards. Neurons in auditory cortex recorded during task performance weakly differentiated the discriminative stimuli but more strongly the subsequent goal-directed movement. Although 10-20% of units exhibited significantly different firing rates between task epochs with different response biases, control experiments showed this to result from inflated false positive rates due to unspecific temporal correlations of spiking activity rather than changing reinforcement contingencies. Transient pharmacological inactivation of auditory cortex reduced sound discriminability without affecting other measures of performance, whereas inactivation of medial prefrontal cortex affected both discriminability and bias. Together, these results suggest that auditory cortex activity only weakly reflects decisional variables during flexible updating of stimulus-response-outcome contingencies and does not play a crucial role in sound-cued adaptive behavior, beyond the representation of the discriminative stimuli.NEW & NOTEWORTHY Recent evidence suggests that sensory cortex represents nonsensory variables such as reward expectation, but the relevance of these representations for behavior is not well understood. We show that rat auditory cortex (AC) is modulated during movement and reward anticipation in a sound-cued reward tracking task, whereas AC inactivation only impaired discrimination without affecting reward tracking, consistent with a predominantly sensory role of AC.

Keywords: adaptation; cognitive model; criterion setting; decision bias; signal detection theory.

MeSH terms

  • Adaptation, Psychological*
  • Animals
  • Auditory Cortex / physiology*
  • Auditory Perception
  • Choice Behavior
  • Cues
  • Discrimination, Psychological
  • Goals*
  • Male
  • Movement*
  • Prefrontal Cortex / physiology
  • Rats
  • Rats, Long-Evans
  • Reward*