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Prefrontal cortex output circuits guide reward seeking through divergent cue encoding.

Publication ,  Journal Article
Otis, JM; Namboodiri, VMK; Matan, AM; Voets, ES; Mohorn, EP; Kosyk, O; McHenry, JA; Robinson, JE; Resendez, SL; Rossi, MA; Stuber, GD
Published in: Nature
March 2017

The prefrontal cortex is a critical neuroanatomical hub for controlling motivated behaviours across mammalian species. 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 thalamus. While connectivity among these structures contributes to appetitive behaviours, 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.

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Published In

Nature

DOI

EISSN

1476-4687

ISSN

0028-0836

Publication Date

March 2017

Volume

543

Issue

7643

Start / End Page

103 / 107

Related Subject Headings

  • Thalamus
  • Reward
  • Prefrontal Cortex
  • Nucleus Accumbens
  • Neurons
  • Neuronal Plasticity
  • Neural Pathways
  • Molecular Imaging
  • Microscopy, Fluorescence, Multiphoton
  • Mice, Inbred C57BL
 

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Otis, J. M., Namboodiri, V. M. K., Matan, A. M., Voets, E. S., Mohorn, E. P., Kosyk, O., … Stuber, G. D. (2017). Prefrontal cortex output circuits guide reward seeking through divergent cue encoding. Nature, 543(7643), 103–107. https://doi.org/10.1038/nature21376
Otis, James M., Vijay M. K. Namboodiri, Ana M. Matan, Elisa S. Voets, Emily P. Mohorn, Oksana Kosyk, Jenna A. McHenry, et al. “Prefrontal cortex output circuits guide reward seeking through divergent cue encoding.Nature 543, no. 7643 (March 2017): 103–7. https://doi.org/10.1038/nature21376.
Otis JM, Namboodiri VMK, Matan AM, Voets ES, Mohorn EP, Kosyk O, et al. Prefrontal cortex output circuits guide reward seeking through divergent cue encoding. Nature. 2017 Mar;543(7643):103–7.
Otis, James M., et al. “Prefrontal cortex output circuits guide reward seeking through divergent cue encoding.Nature, vol. 543, no. 7643, Mar. 2017, pp. 103–07. Epmc, doi:10.1038/nature21376.
Otis JM, Namboodiri VMK, Matan AM, Voets ES, Mohorn EP, Kosyk O, McHenry JA, Robinson JE, Resendez SL, Rossi MA, Stuber GD. Prefrontal cortex output circuits guide reward seeking through divergent cue encoding. Nature. 2017 Mar;543(7643):103–107.
Journal cover image

Published In

Nature

DOI

EISSN

1476-4687

ISSN

0028-0836

Publication Date

March 2017

Volume

543

Issue

7643

Start / End Page

103 / 107

Related Subject Headings

  • Thalamus
  • Reward
  • Prefrontal Cortex
  • Nucleus Accumbens
  • Neurons
  • Neuronal Plasticity
  • Neural Pathways
  • Molecular Imaging
  • Microscopy, Fluorescence, Multiphoton
  • Mice, Inbred C57BL