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Cited by 430Neurological disorders and treatmentsMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

The organization of the basal ganglia-thalamocortical circuits: Open interconnected rather than closed segregated

Joel, D., Weiner, I.·1994·Neuroscience
DOI 10.1016/0306-4522(94)90536-3
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Abstract

Anatomical findings in primates and rodents have led to a description of several parallel segregated basal ganglia-thalamocortical circuits leading from a distinct frontocortical area, via separate regions in the basal ganglia and the thalamus, back to the frontocortical area from which the circuit originates. One of the questions raised by the concept of parallelism is whether and how the different circuits interact. The present Commentary proposes that interaction is inherent in the neural architecture of the basal ganglia-thalamocortical circuits. This proposal is based on the re-examination of the data on the topographical organization of the frontocortical-basal ganglia connections which indicates that each circuit-engaged striatal region sends divergent projections to parts of both substantia nigra pars reticulata and the internal segment of the globus pallidus (each ventral striatal region sends divergent projections to parts of ventral pallidum, substantia nigra pars reticulata and globus pallidus), and this segregation is maintained at subsequent thalamic and frontocortical levels. This results in an asymmetry in the frontal cortex-basal ganglia relationships, so that while each frontocortical subfield innervates one striatal region, each striatal region influences the basal ganglia output to two frontocortical subfields. Because of this asymmetry, at least one of the frontocortical targets of a given circuit-engaged striatal region is not the source of its frontocortical input. Since this organization is inconsistent with an arrangement in closed segregated circuits we introduce the concept of a "split circuit". A split circuit emanates from one frontocortical area, but terminates in two frontocortical areas. Thus, a split circuit contains at least one "open" striato-fronto-cortical pathway, that leads from a circuit-engaged striatal region to a frontocortical area which is a source of a different circuit. In this manner split circuits are interconnected via their open pathways. The second striato-fronto-cortical pathway of a split circuit can be another open pathway, or it can re-enter the frontocortical area of origin, forming a closed circuit. On the basis of the available anatomical data we tentatively identified a motor, an associative, and a limbic split circuit, each containing a closed circuit and an open pathway. The motor split circuit contains a closed motor circuit that re-enters the motor and premotor cortical areas and an open motor pathway that terminates in the associative prefrontal cortex. The associative split circuit contains a closed associative circuit that re-enters the associative prefrontal cortex and an open associative pathway that terminates in the premotor cortex.(ABSTRACT TRUNCATED AT 400 WORDS)

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Crossref · 10.1016/0306-4522(94)90536-3

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  • Different cortical areas project to different domains of striatum and thalamus with some degree of topography.

    “Different cortical areas project to different domains of striatum and thalamus with some degree of topography33–35.”

    From A mesoscale connectome of the mouse brain (2014) · cites this paper as [34]

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Authors
Joel, D., & Weiner, I.
Affiliations
Tel Aviv University (IL)
Corresponding author
Weiner, I.
ORCID
Joel, D.
Venue
Neuroscience
Publisher
Elsevier BV
Published
1994-11
Volume
63
Issue
2
Pages
363-379
ISSN
0306-4522 (ISSN-L)
DOI
10.1016/0306-4522(94)90536-3
OpenAlex
W2065509982
Cited by
430
References
148
Citations by year
2026: 2 · 2025: 7 · 2024: 4 · 2023: 4 · 2022: 5 · 2021: 9 · 2020: 5 · 2019: 5 · 2018: 22 · 2017: 15 · 2016: 21 · 2015: 14 · 2014: 14 · 2013: 13 · 2012: 25
FWCI
2.54
Type
journal article
Language
en
Open access
closed
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Neurology › Neurological disorders and treatments
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
basal ganglia-thalamocortical circuit, parallel circuits, substantia nigra pars reticulata, globus pallidus internus, ventral pallidum, thalamocortical connections, frontal cortex, topographic organization
MeSH terms
Animals, Basal Ganglia, Cerebral Cortex, Humans, Neural Pathways, Thalamus

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