Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes

Striosomes, neurochemically specialized modules in the striatum, are thought to be nodes in circuits extending, via basal ganglia pathways, from mood-related neocortical regions to dopamine-containing neurons of the substantia nigra. Yet striosomes have remained beyond the reach of electrophysiologi...

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Main Authors: Hong, Simon, Amemori, Satoko, Chung, Emily, Gibson, Daniel J., Amemori, Ken-ichi, Graybiel, Ann M.
Other Authors: McGovern Institute for Brain Research at MIT
Format: Article
Language:English
Published: Elsevier BV 2020
Online Access:https://hdl.handle.net/1721.1/125131
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author Hong, Simon
Amemori, Satoko
Chung, Emily
Gibson, Daniel J.
Amemori, Ken-ichi
Graybiel, Ann M.
author2 McGovern Institute for Brain Research at MIT
author_facet McGovern Institute for Brain Research at MIT
Hong, Simon
Amemori, Satoko
Chung, Emily
Gibson, Daniel J.
Amemori, Ken-ichi
Graybiel, Ann M.
author_sort Hong, Simon
collection MIT
description Striosomes, neurochemically specialized modules in the striatum, are thought to be nodes in circuits extending, via basal ganglia pathways, from mood-related neocortical regions to dopamine-containing neurons of the substantia nigra. Yet striosomes have remained beyond the reach of electrophysiological methods to identify them, especially in non-human primates. Such work is needed for translational as well as for basic science. Here we introduce a method to identify striosomes on-line in awake, behaving macaques. We combined electrical microstimulation of the striatum with simultaneous electrophysiological recording in the lateral habenula (LHb) followed by immunohistochemistry. We demonstrate that striosomes provide the predominant striatal input to the macaque pallido-habenular circuit, which is known to function in relation to reinforcement signaling. Further, our experiments suggest that striosomes from different striatal regions may convergently influence the lateral habenula. This work now opens the way to defining the functions of striosomes in behaving primates in relation to mood, motivation, and action. Keywords: basal ganglia; dopamine; motivation; non-human primate; mood; learning; microstimulation
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spelling mit-1721.1/1251312022-09-29T20:55:25Z Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes Hong, Simon Amemori, Satoko Chung, Emily Gibson, Daniel J. Amemori, Ken-ichi Graybiel, Ann M. McGovern Institute for Brain Research at MIT Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Striosomes, neurochemically specialized modules in the striatum, are thought to be nodes in circuits extending, via basal ganglia pathways, from mood-related neocortical regions to dopamine-containing neurons of the substantia nigra. Yet striosomes have remained beyond the reach of electrophysiological methods to identify them, especially in non-human primates. Such work is needed for translational as well as for basic science. Here we introduce a method to identify striosomes on-line in awake, behaving macaques. We combined electrical microstimulation of the striatum with simultaneous electrophysiological recording in the lateral habenula (LHb) followed by immunohistochemistry. We demonstrate that striosomes provide the predominant striatal input to the macaque pallido-habenular circuit, which is known to function in relation to reinforcement signaling. Further, our experiments suggest that striosomes from different striatal regions may convergently influence the lateral habenula. This work now opens the way to defining the functions of striosomes in behaving primates in relation to mood, motivation, and action. Keywords: basal ganglia; dopamine; motivation; non-human primate; mood; learning; microstimulation National Institutes of Health (U.S.) (Grant (R01 NS025529) CHDI Foundation (Grant A-5552) United States. Army Research Office (Grant W911NF-16-1-0474) 2020-05-08T14:25:00Z 2020-05-08T14:25:00Z 2018-12 2018-09 2020-01-21T16:20:16Z Article http://purl.org/eprint/type/JournalArticle 0960-9822 https://hdl.handle.net/1721.1/125131 Hong, Simon et al. "Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes." Current biology 9, 1 (January 2019): 51-61 © 2018 Elsevier Ltd en http://dx.doi.org/10.1016/j.cub.2018.11.008 Current Biology Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier BV PMC
spellingShingle Hong, Simon
Amemori, Satoko
Chung, Emily
Gibson, Daniel J.
Amemori, Ken-ichi
Graybiel, Ann M.
Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes
title Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes
title_full Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes
title_fullStr Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes
title_full_unstemmed Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes
title_short Predominant Striatal Input to the Lateral Habenula in Macaques Comes from Striosomes
title_sort predominant striatal input to the lateral habenula in macaques comes from striosomes
url https://hdl.handle.net/1721.1/125131
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