Genetically distinct parallel pathways in the entopeduncular nucleus for limbic and sensorimotor output of the basal ganglia
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The basal ganglia (BG) integrate inputs from diverse sensorimotor, limbic, and associative regions to guide action-selection and goal-directed behaviors. The entopeduncular nucleus (EP) is a major BG output nucleus and has been suggested to channel signals from distinct BG nuclei to target regions involved in diverse functions. Here we use single-cell transcriptional and molecular analyses to demonstrate that the EP contains at least three classes of projection neurons-glutamate/GABA co-releasing somatostatin neurons, glutamatergic parvalbumin neurons, and GABAergic parvalbumin neurons. These classes comprise functionally and anatomically distinct output pathways that differentially affect EP target regions, such as the lateral habenula (LHb) and thalamus. Furthermore, LHb- and thalamic-projecting EP neurons are differentially innervated by subclasses of striatal and pallidal neurons. Therefore, we identify previously unknown subdivisions within the EP and reveal the existence of cascading, molecularly distinct projections through striatum and globus pallidus to EP targets within epithalamus and thalamus.
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LHb-projecting EP/GPi neurons were later found to transmit both glutamate and GABA and to be capable of exciting and inhibiting LHb neurons.
“Later, they were found to simultaneously transmit both glutamate and GABA and to be capable of both exciting and inhibiting LHb neurons 40,26 (Figure 1A).”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [40]
GABA/glutamate coreleasing neurons in mouse EP and human GPi are marked by Sst expression, enabling specific targeting.
“GABA/glutamate coreleasing neurons in the EP of mice and GPi in humans were found to be marked by expression of Sst, facilitating specific targeting of these neurons in functional studies.40”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [40]
Most analyses in these single-cell sequencing studies are performed on populations of neurons.
“An important caveat to these findings is that most analyses performed in these studies are performed on populations of neurons.”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [40]
Single-cell sequencing studies in the brain have shown that neuron types with the genetic constituents required for releasing more than one neurotransmitter are ubiquitous.
“These studies have also shown the ubiquity of neuron types that have the genetic constituents required for the release of more than one neurotransmitter.6,7,9,40,131”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [40]
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Updating the striatal–pallidal wiring diagram
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Electrophysiological properties of neurons and synapses in the lateral habenular complex (LHb)
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Optogenetic stimulation of striatal patches modifies habit formation and inhibits dopamine release
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Social isolation uncovers a circuit underlying context-dependent territory-covering micturition
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- Authors
- Wallace, M. L., Saunders, A., Huang, K. W., Philson, A. C., Goldman, M., Macosko, E. Z., McCarroll, S. A., & Sabatini, B. L.
- Affiliations
- Howard Hughes Medical Institute (US)
- Broad Institute (US)
- Corresponding author
- Sabatini, Bernardo L.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2017-04
- Volume
- 94
- Issue
- 1
- Pages
- 138-152.e5
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC5439268
- OpenAlex
- W2604170318
- Cited by
- 205
- References
- 66
- Citations by year
- 2026: 18 · 2025: 20 · 2024: 32 · 2023: 20 · 2022: 19 · 2021: 17 · 2020: 28 · 2019: 24 · 2018: 16 · 2017: 11
- FWCI
- 15.23
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Neurological Disease and Stroke (NS007484-15, NS046579-13)
- Stanley Center for Psychiatric Research at the Broad Institute
- Helen Hay Whitney Foundation
- Topics
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- entopeduncular nucleus, basal ganglia, lateral habenula, thalamus, somatostatin neurons, parvalbumin neurons, globus pallidus, striatum, epithalamus, action selection, single-cell transcriptomics
- MeSH terms
- Animals, Basal Ganglia, Globus Pallidus, Humans, Limbic System, Neurons, Parvalbumins, Somatostatin, Thalamus, Neostriatum, In Situ Hybridization, Fluorescence, Glutamic Acid, Habenula, Entopeduncular Nucleus, Gene Expression Profiling, Mice, Single-Cell Analysis, GABAergic Neurons, Sensorimotor Cortex
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