Deviance Distraction and Stimulus-Specific Adaptation in the Somatosensory Cortex Reduce with Experience

Automatic detection of a surprising change in the sensory input is a central element of exogenous attentional control. Stimulus-specific adaptation (SSA) is a potential neuronal mechanism detecting such changes and has been robustly described across sensory modalities and different instances of the ascending sensory pathways. However, little is known about the relationship of SSA to perception. To assess how deviating stimuli influence target signal detection, we used a behavioral cross-modal paradigm in mice and combined it with extracellular recordings from the primary somatosensory whisker cortex. In this paradigm, male mice performed a visual detection task while task-irrelevant whisker stimuli were either presented as repetitive “standard” or as rare deviant stimuli. We found a deviance distraction effect on the animals' performance: Faster reaction times but worsened target detection was observed in the presence of a deviant stimulus. Multiunit activity and local field potentials exhibited enhanced neuronal responses to deviant compared with standard whisker stimuli across all cortical layers, as a result of SSA. The deviant-triggered behavioral distraction correlated with these enhanced neuronal deviant responses only in the deeper cortical layers. However, the layer-specific effect of SSA on perception reduced with increasing task experience as a result of statistical distractor learning. These results demonstrate a layer-specific involvement of SSA on perception that is susceptible to modulation over time. SIGNIFICANCE STATEMENT Detecting sudden changes in our immediate environment is behaviorally relevant and important for efficient perceptual processing. However, the connection between the underpinnings of cortical deviance detection and perception remains unknown. Here, we investigate how the cortical representation of deviant whisker stimuli impacts visual target detection by recording local field potential and multiunit activity in the primary somatosensory cortex of mice engaged in a cross-modal visual detection task. We find that deviant whisker stimuli distract animals in their task performance, which correlates with enhanced neuronal responses for deviants in a layer-specific manner. Interestingly, this effect reduces with the increased experience of the animal as a result of distractor learning on statistical regularities.