Abstract

The brain processes sensory information in a context- and learning-dependent manner for adaptive behavior. Through reward-based learning, relevant sensory stimuli can become linked to execution of specific actions associated with positive outcomes. The neuronal circuits involved in such goal-directed sensory-to-motor transformations remain to be precisely determined. Studying simple learned sensorimotor transformations in head-restrained mice offers the opportunity for detailed measurements of cellular activity during task performance. Here, we trained mice to lick a reward spout in response to a whisker deflection and an auditory tone. Through two-photon calcium imaging of retrogradely labeled neurons, we found that neurons located in primary whisker somatosensory barrel cortex projecting to secondary whisker somatosensory cortex had larger calcium signals than neighboring neurons projecting to primary whisker motor cortex in response to whisker deflection and auditory stimulation, as well as before spontaneous licking. Longitudinal imaging of the same neurons revealed that these projection-specific responses were relatively stable across 3 days. In addition, the activity of neurons projecting to secondary whisker somatosensory cortex was more highly correlated than for neurons projecting to primary whisker motor cortex. The large and correlated activity of neurons projecting to secondary whisker somatosensory cortex might enhance the pathway-specific signaling of important sensory information contributing to task execution. Our data support the hypothesis that communication between primary and secondary somatosensory cortex might be an early critical step in whisker sensory perception. More generally, our data suggest the importance of investigating projection-specific neuronal activity in distinct populations of intermingled excitatory neocortical neurons during task performance.

Highlights

  • Neocortical neuronal activity is thought to contribute to sensory perception and volitional motor control, but the precise neuronal circuits underlying goal-directed sensory-to-motor transformations remain to be fully delineated

  • Through two-photon calcium imaging of retrogradely labeled neurons, we found that neurons located in primary whisker somatosensory barrel cortex projecting to secondary whisker somatosensory cortex had larger calcium signals than neighboring neurons projecting to primary whisker motor cortex in response to whisker deflection and auditory stimulation, as well as before spontaneous licking

  • The activity of neurons projecting to secondary whisker somatosensory cortex was more highly correlated than for neurons projecting to primary whisker motor cortex

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Summary

Introduction

Neocortical neuronal activity is thought to contribute to sensory perception and volitional motor control, but the precise neuronal circuits underlying goal-directed sensory-to-motor transformations remain to be fully delineated. Two-photon imaging of neurons expressing genetically encoded calcium indicators, such as GCaMP6,29 allows measurement of neuronal network activity with cellular resolution over long periods of time during whisker-dependent head-restrained mouse behavior[7,8,10] and can readily be combined with retrograde labeling of projection neurons.[10,11,12,13] Previous such imaging studies during a whisker detection task found evidence supporting enhanced reciprocal signaling between wS1 and wS2,13,22 consistent with the electrophysiological study.[21] these previous imaging studies during whisker detection tasks did not directly compare S2p and M1p neurons. We advance current understanding through longitudinal imaging across days, finding relatively stable representations, and carrying out cross-correlation analyses, finding highly correlated spontaneous activity among S2p neurons

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