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The Nigrostriatal Pathway in the Rat: A Single-Axon Study of the Relationship between Dorsal and Ventral Tier Nigral Neurons and the Striosome/Matrix Striatal Compartments
Open accessAbstract
Axons from dorsal/ventral tiers of substantia nigra pars compacta (SNc), ventral tegmental area (VTA), and retrorubral field (RRF) were traced after injecting their cell body with biotinylated dextran amine. Fifty-three single axons were reconstructed from serial sagittal sections with a camera lucida, and mu-opiate receptor immunostaining served to differentiate the striosome/matrix striatal compartments. Most dorsal tier SNc axons terminate within the matrix of the dorsal striatum, but their patterns of arborization vary markedly; some axons innervate one specific matriceal area, whereas others arborize in multiple discontinuous loci. Some dorsal tier SNc axons also project to both striosomes and matrix. Other dorsal tier SNc axons, as well as VTA axons, innervate the ventral striatum and send collaterals to striosomes lying ventrally in the dorsal striatum or to the ventral sector of the subcallosal streak (SS). Ventral tier SNc axons arborize principally in striosomes, but some ramify in both compartments or in striosomes and the SS. Ventral tier neurons that form deep clusters in substantia nigra pars reticulata innervate principally the matrix and the SS. The amygdala and ventral pallidum receive secondary collaterals from striatal axons of dorsal/ventral tier neurons or RRF neurons. The subthalamic nucleus receives collaterals from striatal axons of SNc clustered neurons, whereas the globus pallidus gets collaterals from striatal axons of dorsal/ventral tier SNc neurons. These findings reveal that the nigrostriatal pathway is composed of several neuronal subsystems, each endowed with a widely distributed axonal arborization that allows them to exert a multifaceted influence on striatal and/or extrastriatal structures.
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“The projections of these neurons are peculiar in that they are particularly focal – they have been mapped to the bed nucleus of the stria terminals (BST) and central nucleus of the amygdala [13,20], and appear to innervate a much smaller target volume than other DA neurons (e.g. [49] and [50]).”
From Classification of midbrain dopamine neurons using single-cell gene expression profiling approaches (2020) · cites this paper as [50]
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Brignani, S., Raj, D. D. A., Schmidt, E. R. E., Düdükcü, Ö., Adolfs, Y., Ruiter, A. A. D., Rybiczka-Tešulov, M., Verhagen, M. G., van der Meer, C., Broekhoven, M. H., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.037 · Cited by 46
Mengual, E., & Pickel, V. M. (2001) · Synapse · doi:10.1002/syn.10033 · Cited by 47
Matsui, A., & Alvarez, V. A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.076 · Cited by 46
A cadherin‐based code for the divisions of the mouse basal ganglia
Hertel, N., Krishna‐K, Nuernberger, M., & Redies, C. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21696 · Cited by 46
Fortin, G. M., Ducrot, C., Giguère, N., Kouwenhoven, W. M., Bourque, M.-J., Pacelli, C., Varaschin, R. K., Brill, M., Singh, S., Wiseman, P. W., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201800713rr · Cited by 45
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Relationship between axonal collateralization and neuronal degeneration in basal ganglia
Parent, M., & Parent, A. (2006) · Springer eBooks · doi:10.1007/978-3-211-45295-0_14 · Cited by 44
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Metadata
- Authors
- Prensa, L., & Parent, A.
- Affiliations
- Université Laval (CA)
- ORCID
- Prensa, Lucı́a
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2001-09-15
- Volume
- 21
- Issue
- 18
- Pages
- 7247-7260
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6762986
- OpenAlex
- W1925686653
- Cited by
- 238
- References
- 62
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 8 · 2023: 10 · 2022: 8 · 2021: 11 · 2020: 10 · 2019: 8 · 2018: 12 · 2017: 14 · 2016: 16 · 2015: 13 · 2014: 8 · 2013: 6 · 2012: 15
- FWCI
- 4.74
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Medical Research Council Canada
- Medical Research Council
- 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
- nigrostriatal pathway, substantia nigra pars compacta, substantia nigra pars reticulata, ventral tegmental area, retrorubral field, striosomes, striatal matrix, axonal arborization, striatal projections, subthalamic nucleus, globus pallidus, amygdala, ventral pallidum, mu-opioid receptor
- MeSH terms
- Animals, Axons, Biotin, Corpus Striatum, Dextrans, Female, Immunohistochemistry, Male, Neural Pathways, Neurons, Substantia Nigra, Organelles, Rats, Sprague-Dawley, Receptors, Opioid, mu, Rats
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