Distinct prefrontal top-down circuits differentially modulate sensorimotor behavior

Rafiq Huda,Vincent Breton-Provencher,Ian R Wickersham,K Guadalupe Cruz,Gerald N Pho,Mriganka Sur,Liadan M Gunter,Elie Adam,Austin Sullins,Grayson O Sipe

doi:10.1038/s41467-020-19772-z

Rafiq Huda, Vincent Breton-Provencher + Show 8 more

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https://doi.org/10.1038/s41467-020-19772-z

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Sensorimotor behaviors require processing of behaviorally relevant sensory cues and the ability to select appropriate responses from a vast behavioral repertoire. Modulation by the prefrontal cortex (PFC) is thought to be key for both processes, but the precise role of specific circuits remains unclear. We examined the sensorimotor function of anatomically distinct outputs from a subdivision of the mouse PFC, the anterior cingulate cortex (ACC). Using a visually guided two-choice behavioral paradigm with multiple cue-response mappings, we dissociated the sensory and motor response components of sensorimotor control. Projection-specific two-photon calcium imaging and optogenetic manipulations show that ACC outputs to the superior colliculus, a key midbrain structure for response selection, principally coordinate specific motor responses. Importantly, ACC outputs exert control by reducing the innate response bias of the superior colliculus. In contrast, ACC outputs to the visual cortex facilitate sensory processing of visual cues. Our results ascribe motor and sensory roles to ACC projections to the superior colliculus and the visual cortex and demonstrate for the first time a circuit motif for PFC function wherein anatomically non-overlapping output pathways coordinate complementary but distinct aspects of visual sensorimotor behavior.

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Sensorimotor behaviors require processing of behaviorally relevant sensory cues and the ability to select appropriate responses from a vast behavioral repertoire
Comparing behavioral deficits induced by projection-specific inactivation of anterior cingulate cortex (ACC) output pathways across task contingencies shows that ACC projections to the superior colliculus (SC) modulate specific motor responses, while projections to the visual cortex (VC) contribute to sensory processing
We demonstrate that the ACC modulates visual sensorimotor behaviors by using anatomically distinct but functionally complementary populations of projection neurons to facilitate sensory processing (ACC-VC) and specific actions (ACC-SC)

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Sensorimotor behaviors require processing of behaviorally relevant sensory cues and the ability to select appropriate responses from a vast behavioral repertoire. Our results ascribe motor and sensory roles to ACC projections to the superior colliculus and the visual cortex and demonstrate for the first time a circuit motif for PFC function wherein anatomically nonoverlapping output pathways coordinate complementary but distinct aspects of visual sensorimotor behavior. The ACC provides outputs to the VC and motor-related layers of the superior colliculus (SC)[27,28,29,30,31], a crucial midbrain structure for response selection and other functions[9,32,33,34,35,36,37,38,39,40] These outputs originate from non-overlapping populations of ACC projection neurons[29], raising the possibility that these output pathways differentially modulate sensorimotor behavior. By using two-photon calcium imaging of ACC inputs/outputs, virus-mediated anatomical tracing, and optogenetics, we delineate specific circuit mechanisms mediating this novel effect

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