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Cortico-basal ganglia circuits involved in different motivation disorders in non-human primates

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Abstract

The ventral striatum (VS) is of particular interest in the study of neuropsychiatric disorders. In this study, performed on non-human primates, we associated local perturbation with monosynaptic axonal tracer injection into medial, central and lateral VS to characterize anatomo-functional circuits underlying the respective expression of sexual manifestations, stereotyped behaviors and hypoactive state associated with loss of food motivation. For the three behavioral effects, we demonstrated the existence of three distinct cortico-basal ganglia (BG) circuits that were topographically organized and overlapping at some cortical (orbitofrontal cortex, anterior cingulate cortex) and subcortical (caudal levels of BG) levels, suggesting interactions between motivation domains. Briefly, erection was associated with a circuit involving the orbitofrontal cortex, medial prefrontal cortex (areas 10, 11) and limbic parts of BG, i.e. medial parts of the pallidal complex and the substantia nigra pars reticulata (SNr). Stereotyped behavior was linked to a circuit involving the lateral orbitofrontal cortex (area 12/47) and limbic parts of the pallidal complex and of the SNr, while the apathetic state was underlined by a circuit involving not only the orbital and medial prefrontal cortex but also the lateral prefrontal cortex (area 8, 45), the anterior insula and the lateral parts of the medial pallidal complex and of the ventro-medial SNr. For the three behavioral effects, the cortico-BG circuits mainly involved limbic regions of the external and internal pallidum, as well as the limbic part of the substantia nigra pars reticulata (SNr), suggesting the involvement of both direct and indirect striatal pathways and both output BG structures. As these motivation disorders could still be induced in dopamine (DA)-depleted monkeys, we suggest that DA issued from the substantia nigra pars compacta (SNc) modulates their expression rather than causes them. Finally, this study may give some insights into the structure to target to achieve therapeutic benefits from deep brain stimulation in motivation disorders.

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Abbreviations

AC:

Anterior commissure

BDA:

Biotin dextran amine

cc:

Corpus callosum

BG:

Basal ganglia

Cd:

Caudate nucleus

CP:

Cerebellar peduncle

CM/Pf:

Centromedian and parafascicular nuclei

Cx:

Cortex

DBS:

Deep brain stimulation

fMRI:

Functional magnetic resonance imaging

GPe:

External pallidum

GPi:

Internal pallidum

ic:

Internal capsule

Ins:

Insula

Lv:

Lateral ventricle

MD:

Mediodorsal nucleus of the thalamus

MPTP:

1-Methyl 4-phenyl 1,2,3,6-tetrahydropyridine

NHP:

Non-human primates

OCD:

Obsessive compulsive disorders

OPAI:

Orbital periallocortex

PD:

Parkinson’s disease

PARV:

Parvalbumin

PET:

Positron emission tomography

Put:

Putamen

SNc:

Substantia nigra pars compacta

SNr:

Substantia nigra pars reticulata

STN:

Subthalamic nucleus

Temp:

Temporal cortex

TH:

Tyrosine hydroxylase

VA:

Ventral anterior nucleus of the thalamus

VL:

Ventral lateral nucleus of the thalamus

VS:

Ventral striatum

WM:

White matter

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Acknowledgments

This work was supported by grants from Agence Nationale de la Recherche (Grant Number ANR-09-MNPS-018) and Labex Cortex. Dr. Y. Worbe has been supported by Lilli institute and FYSSEN foundation. Dr. V. Sgambato-Faure is supported by INSERM (Institut National de la Santé et de la Recherche Médicale).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Centre de Neuroscience Cognitive, UMR5229 CNRS, Université Lyon I, 69675, Bron Cedex, France

    Véronique Sgambato-Faure, Justine Epinat & Léon Tremblay

  2. Centre de Recherche de l’Institut du Cerveau et de la Moelle épinère, UMR-S975, Université Paris VI, 75013, Paris, France

    Yulia Worbe & Jean Féger

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  1. Véronique Sgambato-Faure
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  2. Yulia Worbe
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  3. Justine Epinat
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Correspondence to Véronique Sgambato-Faure.

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V. S.-F. and Y. W. contributed equally to this work.

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Sgambato-Faure, V., Worbe, Y., Epinat, J. et al. Cortico-basal ganglia circuits involved in different motivation disorders in non-human primates. Brain Struct Funct 221, 345–364 (2016). https://doi.org/10.1007/s00429-014-0911-9

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