Frontal Cortex Gates Distractor Stimulus Encoding in Target Sensory Cortex

Abstract

Frontal cortex suppresses behavioral responses to distractor stimuli. One possible mechanism by which this occurs is by modulating sensory responses in sensory cortex. However, it is currently unknown how frontal cortex modulations of sensory cortex contribute to distractor response suppression. We trained mice to respond to target stimuli in one whisker field and ignore distractor stimuli in the opposite whisker field. During expert task performance, optogenetic inhibition of frontal cortex increased behavioral responses to distractor stimuli. During expert task performance, within sensory cortex we observed expanded propagation of target stimulus responses and contracted propagation of distractor stimulus responses. In contrast to current models of frontal cortex function, frontal cortex did not substantially modulate the response amplitude of preferred stimuli. Rather, frontal cortex specifically suppressed the propagation of distractor stimulus responses, thereby preventing target-preferring neurons from being activated by distractor stimuli. Single unit analyses revealed that wMC decorrelates target and distractor stimulus encoding in target-preferring S1 neurons, which likely improves selective target stimulus detection by downstream readers. Moreover, we observed proactive top-down modulation from frontal to sensory cortex, through the preferential activation of GABAergic neurons. Overall, our study provides important mechanistic details about how frontal cortex gates sensory propagation in sensory cortex to prevent behavioral responses to distractor stimuli. HighlightsO_LIPairing of frontal cortex optogenetic inhibition with sensory cortex recordings during a target-distractor Go/NoGo task. C_LIO_LIDuring expert task performance, we observed target stimulus response expansion and distractor stimulus response contraction. C_LIO_LIOptogenetic inhibition of frontal cortex increased false alarm rates and selectively increased the propagation of distractor evoked responses into target-aligned sensory cortex. C_LIO_LIEven before stimulus onset, frontal cortex preferentially drives GABAergic neurons in distractor-aligned sensory cortex. C_LI