Abstract

Neural representation in the auditory cortex is rapidly modulated by both top-down attention and bottom-up stimulus properties, in order to improve perception in a given context. Learning-induced, pre-attentive, map plasticity has been also studied in the anesthetized cortex; however, little attention has been paid to rapid, context-dependent modulation. We hypothesize that context-specific learning leads to pre-attentively modulated, multiplex representation in the auditory cortex. Here, we investigate map plasticity in the auditory cortices of anesthetized rats conditioned in a context-dependent manner, such that a conditioned stimulus (CS) of a 20-kHz tone and an unconditioned stimulus (US) of a mild electrical shock were associated only under a noisy auditory context, but not in silence. After the conditioning, although no distinct plasticity was found in the tonotopic map, tone-evoked responses were more noise-resistive than pre-conditioning. Yet, the conditioned group showed a reduced spread of activation to each tone with noise, but not with silence, associated with a sharpening of frequency tuning. The encoding accuracy index of neurons showed that conditioning deteriorated the accuracy of tone-frequency representations in noisy condition at off-CS regions, but not at CS regions, suggesting that arbitrary tones around the frequency of the CS were more likely perceived as the CS in a specific context, where CS was associated with US. These results together demonstrate that learning-induced plasticity in the auditory cortex occurs in a context-dependent manner.

Highlights

  • State-dependent neural representation is found in both the sensory (e.g., [1,2,3]) and motor systems [4], suggesting that neurons multiplex their function to perform different analyses according to context

  • We performed a context-dependent auditory fear conditioning, in which a mild electrical foot shock as unconditioned stimulus (US) was associated with 20kHz conditioned stimulus (CS) tone under the noise condition, while only the CS was presented in the silent condition

  • We demonstrated that this conditioning changed both behavior and auditory cortical activities in a context-dependent manner

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Summary

Introduction

State-dependent neural representation is found in both the sensory (e.g., [1,2,3]) and motor systems [4], suggesting that neurons multiplex their function to perform different analyses according to context. Pre-attentively (under anesthesia), the receptive fields are rapidly modulated by bottom-up stimulus properties [8] such as stimulus density [9], bandwidth [10], envelope [11], and context [12] Such context-dependent modulation of receptive fields is critically involved for contrast gain control [13], possibly through synaptic depression [14], [15] and/or other network mechanisms [11], [16]. Past experiences such as passive sound exposure and active learning influence the pre-attentive cortical representation (for reviews: [17,18,19]). Little attention has been paid to the rapid, context-dependent modulation of such plasticity

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