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The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum
Abstract
This Commentary compares the connections of the dopaminergic system with the striatum in rats and primates with respect to two levels of striatal organization: a tripartite functional (motor, associative and limbic) subdivision and a compartmental (patch/striosome-matrix) subdivision. The topography of other basal ganglia projections to the dopaminergic system with respect to their tripartite functional subdivision is also reviewed. This examination indicates that, in rats and primates, the following observations can be made. (1) The limbic striatum reciprocates its dopaminergic input and in addition innervates most of the dopaminergic neurons projecting to the associative and motor striatum, whereas the motor and associative striatum reciprocate only part of their dopaminergic input. Therefore, the connections of the three striatal subregions with the dopaminergic system are asymmetrical, but the direction of asymmetry differs between the limbic versus the motor and associative striatum. (2) The limbic striatum provides the main striatal input to dopamine cell bodies and proximal dendrites, with some contribution from a subset of neurons in the associative and motor striatum (patch neurons in rats; an unspecified group of neurons in primates), while striatal input to the ventrally extending dopamine dendrites arises mainly from a subset of neurons in the associative and motor striatum (matrix neurons in rats; an unspecified group of neurons in primates). (3) Projections from functionally corresponding subdivisions of the striatum, pallidum and subthalamic nucleus to the dopaminergic system overlap, but the specific targets (dopamine cells, dopamine dendrites, GABA cells) of these projections differ. Major differences include the following. (1) In rats, neurons projecting to the motor and associative striatum reside in distinct regions, while in primates they are arranged in interdigitating clusters. (2) In rats, the terminal fields of projections arising from the motor and associative striatum are largely segregated, while in primates they are not. (3) In rats, patch- and matrix-projecting dopamine cells are organized in spatially, morphologically, histochemically and hodologically distinct ventral and dorsal tiers, while in primates there is no (bi)division of the dopaminergic system that results in two areas which have all the characteristics of the two tiers in rats. Based on the anatomical data and known dopamine cell physiology, we forward an hypothesis regarding the influence of the basal ganglia on dopamine cell activity which captures at least part of the complex interplay taking place within the substantia nigra between projections arising from the different basal ganglia nuclei. Finally, we incorporate the striatal connections with the dopaminergic system into an open-interconnected scheme of basal ganglia-thalamocortical circuitry.
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“This leads to a flow of information from ventral to dorsal striatal circuits via communication with dopamine neurons, and enables information processed within the VS to iteratively influence dorsal striatal computations (Figure 2).”
From A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors (2015) · cites this paper as Joel and Weiner, 2000
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“One influential proposal is that a protracted exposure to addictive drugs recruits dopamine-dependent striato-nigro-striatal ascending spirals (Haber et al., 2000; Joel and Weiner, 2000) from the nucleus accumbens to more dorsal regions of the striatum (Everitt et al., 2008).”
From Goals and Habits in the Brain (2013) · cites this paper as Joel and Weiner, 2000
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Metadata
- Authors
- Joel, D., & Weiner, I.
- Affiliations
- Tel Aviv University (IL)
- Corresponding author
- Joel, D
- ORCID
- Joel, D
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2000-03
- Volume
- 96
- Issue
- 3
- Pages
- 451-474
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W1967784117
- Cited by
- 614
- References
- 300
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 13 · 2023: 15 · 2022: 23 · 2021: 12 · 2020: 16 · 2019: 15 · 2018: 13 · 2017: 28 · 2016: 24 · 2015: 24 · 2014: 30 · 2013: 25 · 2012: 45
- FWCI
- 3.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Deep Brain Stimulation and Movement Disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- dopaminergic system, striatum, basal ganglia, limbic striatum, globus pallidus, subthalamic nucleus, rats, primates, comparative neuroanatomy
- MeSH terms
- Animals, Corpus Striatum, Dopamine, Humans, Neural Pathways, Primates, Rats
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