Orbitofrontal Circuits Control Multiple Reinforcement-Learning Processes

Stephanie M. Groman, C. Keistler, Alex J. Keip, Emma Hammarlund, Ralph J. DiLeone, Christopher Pittenger, Daeyeol Lee, Jane R. Taylor

Research output: Contribution to journalArticlepeer-review

26 Scopus citations

Abstract

Adaptive decision making in dynamic environments requires multiple reinforcement-learning steps that may be implemented by dissociable neural circuits. Here, we used a novel directionally specific viral ablation approach to investigate the function of several anatomically defined orbitofrontal cortex (OFC) circuits during adaptive, flexible decision making in rats trained on a probabilistic reversal learning task. Ablation of OFC neurons projecting to the nucleus accumbens selectively disrupted performance following a reversal, by disrupting the use of negative outcomes to guide subsequent choices. Ablation of amygdala neurons projecting to the OFC also impaired reversal performance, but due to disruptions in the use of positive outcomes to guide subsequent choices. Ablation of OFC neurons projecting to the amygdala, by contrast, enhanced reversal performance by destabilizing action values. Our data are inconsistent with a unitary function of the OFC in decision making. Rather, distinct OFC-amygdala-striatal circuits mediate distinct components of the action-value updating and maintenance necessary for decision making. The orbitofrontal cortex (OFC) plays a critical role in guiding decisions in dynamic environments. Groman et al. use a directionally specific viral ablation approach to demonstrate that OFC circuits encode separable reinforcement-learning processes that guide decisions.

Original languageEnglish (US)
Pages (from-to)734-746.e3
JournalNeuron
Volume103
Issue number4
DOIs
StatePublished - Aug 21 2019
Externally publishedYes

Bibliographical note

Funding Information:
This research was supported by Public Health Service grants from the National Institute on Drug Abuse ( DA041480 , DA043443 ), the National Institute of Mental Health ( MH091861 ), the National Institute on Alcohol Abuse and Alcoholism ( AA012870 ), a NARSAD Young Investigator Award from the Brain and Behavior Research Foundation , and the State of Connecticut through its support of the Ribicoff Research Facilities.

Funding Information:
This research was supported by Public Health Service grants from the National Institute on Drug Abuse (DA041480, DA043443), the National Institute of Mental Health (MH091861), the National Institute on Alcohol Abuse and Alcoholism (AA012870), a NARSAD Young Investigator Award from the Brain and Behavior Research Foundation, and the State of Connecticut through its support of the Ribicoff Research Facilities. Conceptualization, S.M.G. C.K. and J.R.T.; Investigation, S.M.G. C.K. E.H. and A.J.K.; Funding Acquisition, S.M.G. and J.R.T.; Resources, C.P. and R.J.D.L.; Methodology, S.M.G. and D.L.; Writing ? Original Draft, S.M.G.; Writing ? Editing, S.M.G. D.L. and J.R.T.; Writing ? Review, S.M.G. C.K. A.J.K. E.H. C.P. R.J.D.L. D.L. and J.R.T. The authors declare no competing interests.

Keywords

  • amygdala
  • decision making
  • nucleus accumbens
  • orbitofrontal cortex
  • reinforcement learning

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