Prefrontal cortex output circuits guide reward seeking through divergent cue encoding

James M. Otis, Vijay M. K. Namboodiri, Ana M. Matan, Elisa S. Voets, Emily P. Mohorn, Oksana Kosyk, Jenna A. McHenry, J. Elliott Robinson, Shanna L. Resendez, Mark A. Rossi and Garret D. Stuber ()
Additional contact information
James M. Otis: University of North Carolina at Chapel Hill
Vijay M. K. Namboodiri: University of North Carolina at Chapel Hill
Ana M. Matan: University of North Carolina at Chapel Hill
Elisa S. Voets: University of North Carolina at Chapel Hill
Emily P. Mohorn: University of North Carolina at Chapel Hill
Oksana Kosyk: University of North Carolina at Chapel Hill
Jenna A. McHenry: University of North Carolina at Chapel Hill
J. Elliott Robinson: University of North Carolina at Chapel Hill
Shanna L. Resendez: University of North Carolina at Chapel Hill
Mark A. Rossi: University of North Carolina at Chapel Hill
Garret D. Stuber: University of North Carolina at Chapel Hill

Nature, 2017, vol. 543, issue 7643, 103-107

Abstract: Abstract The prefrontal cortex is a critical neuroanatomical hub for controlling motivated behaviours across mammalian species1,2,3. In addition to intra-cortical connectivity, prefrontal projection neurons innervate subcortical structures that contribute to reward-seeking behaviours, such as the ventral striatum and midline thalamus4. While connectivity among these structures contributes to appetitive behaviours5,6,7,8,9,10,11,12,13, how projection-specific prefrontal neurons encode reward-relevant information to guide reward seeking is unknown. Here we use in vivo two-photon calcium imaging to monitor the activity of dorsomedial prefrontal neurons in mice during an appetitive Pavlovian conditioning task. At the population level, these neurons display diverse activity patterns during the presentation of reward-predictive cues. However, recordings from prefrontal neurons with resolved projection targets reveal that individual corticostriatal neurons show response tuning to reward-predictive cues, such that excitatory cue responses are amplified across learning. By contrast, corticothalamic neurons gradually develop new, primarily inhibitory responses to reward-predictive cues across learning. Furthermore, bidirectional optogenetic manipulation of these neurons reveals that stimulation of corticostriatal neurons promotes conditioned reward-seeking behaviour after learning, while activity in corticothalamic neurons suppresses both the acquisition and expression of conditioned reward seeking. These data show how prefrontal circuitry can dynamically control reward-seeking behaviour through the opposing activities of projection-specific cell populations.

Date: 2017
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DOI: 10.1038/nature21376

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