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Distinct prefrontal top-down circuits differentially modulate sensorimotor behavior

View ORCID ProfileRafiq Huda, Grayson O. Sipe, View ORCID ProfileVincent Breton-Provencher, K. Guadalupe Cruz, Gerald N. Pho, View ORCID ProfileElie Adam, Liadan M. Gunter, Austin Sullins, Ian R. Wickersham, Mriganka Sur
doi: https://doi.org/10.1101/307009
Rafiq Huda
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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  • For correspondence: rafiq.huda@rutgers.edu msur@mit.edu
Grayson O. Sipe
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Vincent Breton-Provencher
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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K. Guadalupe Cruz
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Gerald N. Pho
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Elie Adam
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Liadan M. Gunter
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Austin Sullins
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Ian R. Wickersham
2McGovern Institute for Brain Research Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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Mriganka Sur
1Picower Institute for Learning and Memory Department of Brain and Cognitive Sciences Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
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  • For correspondence: rafiq.huda@rutgers.edu msur@mit.edu
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Abstract

Sensorimotor behaviors require processing of behaviorally relevant sensory cues and the ability to select appropriate responses from a vast behavioral repertoire. Top-down 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 top-down 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.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted September 29, 2020.
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Distinct prefrontal top-down circuits differentially modulate sensorimotor behavior
Rafiq Huda, Grayson O. Sipe, Vincent Breton-Provencher, K. Guadalupe Cruz, Gerald N. Pho, Elie Adam, Liadan M. Gunter, Austin Sullins, Ian R. Wickersham, Mriganka Sur
bioRxiv 307009; doi: https://doi.org/10.1101/307009
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Distinct prefrontal top-down circuits differentially modulate sensorimotor behavior
Rafiq Huda, Grayson O. Sipe, Vincent Breton-Provencher, K. Guadalupe Cruz, Gerald N. Pho, Elie Adam, Liadan M. Gunter, Austin Sullins, Ian R. Wickersham, Mriganka Sur
bioRxiv 307009; doi: https://doi.org/10.1101/307009

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