Independent circuits in the basal ganglia for the evaluation and selection of actions

Stephenson-Jones, M., Kardamakis, A. A., Robertson, B., Grillner, S. (September 2013) Independent circuits in the basal ganglia for the evaluation and selection of actions. Proceedings of the National Academy of Sciences of the United States of America, 110 (38). E3670-E3679. ISSN 0027-8424

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URL: http://www.ncbi.nlm.nih.gov/pubmed/24003130
DOI: 10.1073/pnas.1314815110

Abstract

The basal ganglia are critical for selecting actions and evaluating their outcome. Although the circuitry for selection is well understood, how these nuclei evaluate the outcome of actions is unknown. Here, we show in lamprey that a separate evaluation circuit, which regulates the habenula-projecting globus pallidus (GPh) neurons, exists within the basal ganglia. The GPh neurons are glutamatergic and can drive the activity of the lateral habenula, which, in turn, provides an indirect inhibitory influence on midbrain dopamine neurons. We show that GPh neurons receive inhibitory input from the striosomal compartment of the striatum. The striosomal input can reduce the excitatory drive to the lateral habenula and, consequently, decrease the inhibition onto the dopaminergic system. Dopaminergic neurons, in turn, provide feedback that inhibits the GPh. In addition, GPh neurons receive direct projections from the pallium (cortex in mammals), which can increase the GPh activity to drive the lateral habenula to increase the inhibition of the neuromodulatory systems. This circuitry, thus, differs markedly from the "direct" and "indirect" pathways that regulate the pallidal (e.g., globus pallidus) output nuclei involved in the control of motion. Our results show that a distinct reward-evaluation circuit exists within the basal ganglia, in parallel to the direct and indirect pathways, which select actions. Our results suggest that these circuits are part of the fundamental blueprint that all vertebrates use to select actions and evaluate their outcome.

Item Type: Paper
Uncontrolled Keywords: striosomes reward/aversion pallium/cortex evolution negative reward signals lateral habenula dopamine neurons globus-pallidus evolutionary conservation entopeduncular nucleus substantia innominata gabaergic projections subthalamic nucleus decision-making
Subjects: organism description > animal behavior
organs, tissues, organelles, cell types and functions > tissues types and functions > basal ganglia
organism description > animal behavior > decision making
organs, tissues, organelles, cell types and functions > cell types and functions > cell types > neurons > neuronal circuits
organs, tissues, organelles, cell types and functions > cell types and functions > cell types > neurons > neuronal circuits
organs, tissues, organelles, cell types and functions > cell types and functions > cell types > neurons > neuronal circuits
organs, tissues, organelles, cell types and functions > tissues types and functions
CSHL Authors:
Communities: CSHL labs > Li lab
Depositing User: Matt Covey
Date: September 2013
Date Deposited: 11 Nov 2013 21:31
Last Modified: 21 Dec 2017 15:39
PMCID: PMC3780871
Related URLs:
URI: https://repository.cshl.edu/id/eprint/28862

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