Abstract

The responses of sensory cortical neurons are shaped by experience. As a result perceptual biases evolve, selectively facilitating the detection and identification of sensory events that are relevant for adaptive behaviour. Here we examine the involvement of human visual cortex in the formation of learned perceptual biases. We use classical aversive conditioning to associate one out of a series of oriented gratings with a noxious sound stimulus. After as few as two grating-sound pairings, visual cortical responses to the sound-paired grating show selective amplification. Furthermore, as learning progresses, responses to the orientations with greatest similarity to the sound-paired grating are increasingly suppressed, suggesting inhibitory interactions between orientation-selective neuronal populations. Changes in cortical connectivity between occipital and fronto-temporal regions mirror the changes in visuo-cortical response amplitudes. These findings suggest that short-term behaviourally driven retuning of human visual cortical neurons involves distal top–down projections as well as local inhibitory interactions.

Highlights

  • The responses of sensory cortical neurons are shaped by experience

  • The present study examined to what extent these structural features are reflected in population activity evoked in human visual cortex by a gradient of orientations in which only one orientation predicts aversive behavioural outcomes

  • We examined the steady-state visual evoked potential elicited in visual neurons by rapidly and regularly phasereversing Gabor gratings differing in orientation, during differential fear conditioning

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Summary

Introduction

The responses of sensory cortical neurons are shaped by experience. As a result perceptual biases evolve, selectively facilitating the detection and identification of sensory events that are relevant for adaptive behaviour. Induced or acquired prioritization among healthy participants has been demonstrated in the laboratory during discriminative classical conditioning[14], wherein neutral stimuli (that is, the CS þ ) paired with a noxious event (the unconditioned stimulus (US), for example, a loud noise) elicit facilitated sensory responses, compared with non-paired stimuli (that is, the CS À ) If such prioritization leads to sustained amplification in the population activity of neurons sensitive to a specific stimulus feature, fear conditioning can be utilized to examine lateral interactions among neuronal populations with differential sensitivity to that feature. Such a ‘Mexican hat’ tuning pattern is in contrast to the alternative hypothesis of a generalization gradient, in which ssVEP amplitude is expected to gradually decrease with angular distance from the CS þ

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