A corticostriatal path targeting striosomes controls decision-making under conflict

Alexander Friedman, Daigo Homma, Leif G. Gibb, Ken Ichi Amemori, Samuel J. Rubin, Adam S. Hood, Michael H. Riad, Ann M. Graybiel

Research output: Contribution to journalArticlepeer-review

206 Scopus citations

Abstract

A striking neurochemical form of compartmentalization has been found in the striatum of humans and other species, dividing it into striosomes and matrix. The function of this organization has been unclear, but the anatomical connections of striosomes indicate their relation to emotion-related brain regions, including the medial prefrontal cortex. We capitalized on this fact by combining pathway-specific optogenetics and electrophysiology in behaving rats to search for selective functions of striosomes. We demonstrate that a medial prefronto-striosomal circuit is selectively active in and causally necessary for cost-benefit decision-making under approach-avoidance conflict conditions known to evoke anxiety in humans. We show that this circuit has unique dynamic properties likely reflecting striatal interneuron function. These findings demonstrate that cognitive and emotion-related functions are, like sensory-motor processing, subject to encoding within compartmentally organized representations in the forebrain and suggest that striosome-targeting corticostriatal circuits can underlie neural processing of decisions fundamental for survival.

Original languageEnglish
Pages (from-to)1320-1333
Number of pages14
JournalCell
Volume161
Issue number6
DOIs
StatePublished - 4 Jun 2015
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2015 Elsevier Inc.

Funding

The authors thank Jannifer Lee, Dan Hu, Henry Hall, Yasuo Kubota, and Xiaojian Li for their help in many aspects of this work, Prof. Drazen Prelec for his valuable comments, and the undergraduate students who assisted in these experiments. This work was funded by NIH/NIMH (R01 MH060379 to A.M.G.), the CHDI Foundation (A-5552 to A.M.G.), the Defense Advanced Research Projects Agency and the U.S. Army Research Office (W911NF-10-1-0059 to A.M.G.), the Bachmann-Strauss Dystonia and Parkinson Foundation (to A.M.G.), the William N. and Bernice E. Bumpus Foundation (RRDA Pilot: 2013.1 to A.M.G.), and the Uehara Memorial Foundation and Japan Society for the Promotion of Science (to D.H.).

FundersFunder number
Bachmann-Strauss Dystonia and Parkinson Foundation
CHDI Foundation
Defense Advanced Research Projects Agency
National Institute of Mental Health
National Institutes of Health
William N. and Bernice E. Bumpus Foundation2013.1
National Institutes of Health
National Institute of Mental HealthR01MH060379
Army Research OfficeW911NF-10-1-0059
Defense Advanced Research Projects Agency
Bachmann-Strauss Dystonia and Parkinson Foundation
CHDI FoundationA-5552
Uehara Memorial Foundation
Japan Society for the Promotion of Science

    Fingerprint

    Dive into the research topics of 'A corticostriatal path targeting striosomes controls decision-making under conflict'. Together they form a unique fingerprint.

    Cite this