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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

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Prensa, Lucı́a, Parent, André·2001·The Journal of Neuroscience

DOI 10.1523/jneurosci.21-18-07247.2001PMC PMC6762986

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Abstract

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 rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585
Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures.
Hsu, S. M., Raine, L., & Fanger, H. (1981) · Journal of Histochemistry & Cytochemistry · doi:10.1177/29.4.6166661 · Cited by 14,075
EVIDENCE FOR THE EXISTENCE OF MONOAMINE-CONTAINING NEURONS IN THE CENTRAL NERVOUS SYSTEM. I. DEMONSTRATION OF MONOAMINES IN THE CELL BODIES OF BRAIN STEM NEURONS.
Dahlstroem, A., & Fuxé, K. (1964) · PubMed · Cited by 5,133
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,514
Neurotransmitters and neuromodulators in the basal ganglia
Graybiel, A. M. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90104-i · Cited by 1,576
The neostriatal mosaic: multiple levels of compartmental organization
Gerfen, C. R. (1992) · Trends in Neurosciences · doi:10.1016/0166-2236(92)90355-c · Cited by 1,471
The control of firing pattern in nigral dopamine neurons: burst firing
Grace, A., & Bunney, B. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-11-02877.1984 · Cited by 1,346
Catecholamine innervation of the basal forebrain IV. Topography of the dopamine projection to the basal forebrain and neostriatum
Fallon, J. H., & Moore, R. Y. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901800310 · Cited by 1,190
The control of firing pattern in nigral dopamine neurons: single spike firing
Grace, A., & Bunney, B. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-11-02866.1984 · Cited by 862
The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems
Gerfen, C. R. (1984) · Nature · doi:10.1038/311461a0 · Cited by 842
The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems
Gerfen, C. R., Herkenham, M. A., & Thibault, J. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-12-03915.1987 · Cited by 804
Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining
Graybiel, A. M., & Ragsdale, C. W. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.11.5723 · Cited by 784
A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin
Pinault, D. (1996) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(95)00144-1 · Cited by 720
The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey.
Gerfen, C. R., Baimbridge, K. G., & Miller, J. J. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.24.8780 · Cited by 645
The neostriatal mosaic. I. compartmental organization of projections from the striatum to the substantia nigra in the rat
Gerfen, C. R. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902360404 · Cited by 563
Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum
Herkenham, M. A., & Pert, C. B. (1981) · Nature · doi:10.1038/291415a0 · Cited by 544
Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat
Donoghue, J. P., & Herkenham, M. A. (1986) · Brain Research · doi:10.1016/0006-8993(86)91658-6 · Cited by 418
Heterogeneity of striatal and limbic dopamine innervation: Highly fluorescent islands in developing and adult rats
Olson, L., Seiger, Å., & Fuxé, K. (1972) · Brain Research · doi:10.1016/0006-8993(72)90385-x · Cited by 405
The neostriatal mosaic: III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems
Gerfen, C. R., Baimbridge, K. G., & Thibault, J. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-12-03935.1987 · Cited by 340
The dopaminergic innervation of the ventral striatum in the rat: A light‐ and electron‐microscopical study with antibodies against dopamine
Voorn, P., Jorritsma‐Byham, B., Dijk, C. V., & Buijs, R. M. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902510106 · Cited by 318
Histochemical confirmation for dopaminergic innervation of the rat cerebral cortex after destruction of the noradrenergic ascending pathways
Berger, B., Tassin, J., Blanc, G., Doyennette‐Moyne, M., & Thierry, A. M. (1974) · Brain Research · doi:10.1016/0006-8993(74)90948-2 · Cited by 278
Subdivisions of the dopamine-containing A8-A9-A10 complex identified by their differential mesostriatal innervation of striosomes and extrastriosomal matrix
Jiménez-Castellanos, J., & Graybiel, A. M. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90285-5 · Cited by 272
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Juraska, J. M., Wilson, C. J., & Groves, P. M. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901720403 · Cited by 258
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Lindvall, O., & Björklund, A. (1979) · Brain Research · doi:10.1016/0006-8993(79)90907-7 · Cited by 235
The fronto-striatal projection in the cat and monkey and its relationship to inhomogeneities established by acetylcholinesterase histochemistry
Ragsdale, C. W., & Graybiel, A. M. (1981) · Brain Research · doi:10.1016/0006-8993(81)90556-4 · Cited by 233
The organization of midbrain projections to the striatum in the primate: sensorimotor-related striatum versus ventral striatum
Lynd-Balta, E., & Haber, S. N. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90182-1 · Cited by 233
The neostriatal mosaic: multiple levels of compartmental organization
Gerfen, C. R. (1992) · Springer eBooks · doi:10.1007/978-3-7091-9211-5_4 · Cited by 232
The Primate Substantia Nigra and VTA: Integrative Circuitry and Function
Haber, S. N., & Fudge, J. L. (1997) · Critical Reviews in Neurobiology · doi:10.1615/critrevneurobiol.v11.i4.40 · Cited by 228
Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys
Stefanacci, L., SUZUKI, W. A., & Amaral, D. G. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961125)375:4 · Cited by 192
Cytoarchitectonic heterogeneity of the primate neostriatum: Subdivision into island and matrix cellular compartments
Goldman‐Rakic, P. S. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902050408 · Cited by 188
Topography and functional role of dopaminergic projections from the ventral mesencephalic tegmentum to the ventral pallidum
Klitenick, M. A., Deutch, A. Y., Churchill, L., & Kalivas, P. W. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90430-a · Cited by 182
Localization of nicotinic receptor subunit mRNAs in monkey brain by in situ hybridization
Quik, M., Polonskaya, Y., Gillespie, A. J., Jakowec, M. W., Lloyd, G. K., & Langston, J. W. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20000911)425:1 · Cited by 172
The organization of midbrain projections to the ventral striatum in the primate
Lynd‐Balta, E., & Haber, S. N. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90181-3 · Cited by 169
Monoamine Innervation of Cerebral Cortex and a Theory of the Role of Monoamines in Cerebral Cortex and Basal Ganglia
Fallon, J. H., & Loughlin, S. E. (1932) · Cerebral cortex · doi:10.1007/978-1-4615-6616-8_2 · Cited by 166
Evidence for a dopaminergic innervation of the subthalamic nucleus in the rat
Hassani, O.-K., François, C., Yelnik, J., & Féger, J. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01167-5 · Cited by 166
Primate striatonigral projections: A comparison of the sensorimotor‐related striatum and the ventral striatum
Lynd‐Balta, E., & Haber, S. N. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903450407 · Cited by 164
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Song, D. D., & Haber, S. N. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-13-05102.2000 · Cited by 163
Midbrain dopamine system electrophysiological functioning: A review and new hypothesis
Bunney, B. S., Chiodo, L. A., & Grace, A. A. (1991) · Synapse · doi:10.1002/syn.890090202 · Cited by 159
Substantia nigra dopamine neurons: separate populations project to neostriatum and allocortex
Fallon, J. H., Riley, J. N., & Moore, R. Y. (1978) · Neuroscience Letters · doi:10.1016/0304-3940(78)90160-x · Cited by 150
The organization of the thalamic, nigral and raphe cells projecting to the medial vs lateral caudate-putamen in rat. A fluorescent retrograde double labeling study
van der Kooy, D. (1979) · Brain Research · doi:10.1016/0006-8993(79)91038-2 · Cited by 143
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Tepper, J. M., Sawyer, S. F., & Groves, P. M. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-09-02794.1987 · Cited by 138
Distinct nigrostriatal projection systems innervate striosomes and matrix in the primate striatum
Langer, L. F., & Graybiel, A. M. (1989) · Brain Research · doi:10.1016/0006-8993(89)91114-1 · Cited by 133
The axonal arborization of single nigrostriatal neurons in rats
Gauthier, J., Parent, M., Lévesque, M., & Parent, A. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01573-5 · Cited by 127
Ovarian hormones differentially influence immunoreactivity for dopamine ?- hydroxylase, choline acetyltransferase, and serotonin in the dorsolateral prefrontal cortex of adult rhesus monkeys
Kritzer, M. F., & Kohama, S. G. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990705)409:3 · Cited by 126
Extrastriatal dopaminergic innervation of human basal ganglia
Cossette, M., Lévesque, M., & Parent, A. (1999) · Neuroscience Research · doi:10.1016/s0168-0102(99)00029-2 · Cited by 121
Dopaminergic innervation of human basal ganglia
Prensa, L., Cossette, M., & Parent, A. (2000) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(00)00099-5 · Cited by 119
Dendro-dendritic synapses in substantia nigra: Descriptions based on analysis of serial sections
Groves, P. M., & Linder, J. C. (1983) · Experimental Brain Research · doi:10.1007/bf00238581 · Cited by 115
Dopaminergic mechanisms in subthalamic nucleus of rat: analysis using horseradish peroxidase and microiontophoresis
Campbell, G. A., Eckardt, M. J., & Weight, F. F. (1985) · Brain Research · doi:10.1016/0006-8993(85)91580-x · Cited by 113
Dopaminergic innervation of the pallidum in the normal state, in MPTP-treated monkeys and in parkinsonian patients
Jan, C., François, C., Tandé, D., Yelnik, J., Tremblay, L., Agid, Y., & Hirsch, É. C. (2000) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2000.01351.x · Cited by 102
The striatal mosaic in primates: Patterns of neuropeptide immunoreactivity differentiate the ventral striatum from the dorsal striatum
Martin, L. J., Hadfield, M. G., Dellovade, T., & Price, D. L. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90303-6 · Cited by 101
Golgi study of the primate substantia nigra. I. Quantitative morphology and typology of nigral neurons
Yelnik, J., François, C., Percheron, G., & Heyner, S. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902650402 · Cited by 98
Evidence that dopaminergic axons provide a dense innervation of specific neuronal subpopulations in the rat basolateral amygdala
Brinley-Reed, M., & McDonald, A. J. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02112-5 · Cited by 84
Monoaminergic presynaptic axons and dendrites in rat locus coeruleus seen in reconstructions of serial sections
Groves, P. M., & Wilson, C. J. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901930403 · Cited by 83
Non-dopaminergic nigrostriatal pathway
Guyenet, P. G., & Crane, J. K. (1981) · Brain Research · doi:10.1016/0006-8993(81)90235-3 · Cited by 75
Anatomy and physiology of substantia nigra and retrorubral neurons studied by extra- and intracellular recording and by horseradish peroxidase labeling
Preston, R. J., McCREA, R. A., Chang, H. T., & Kitai, S. T. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90127-5 · Cited by 72
Catecholaminergic innervation of the subthalamic nucleus: evidence for a rostral continuation of the A9 (substantia nigra) dopaminergic cell group
Meibach, R. C., & Katzman, R. (1979) · Brain Research · doi:10.1016/0006-8993(79)90639-5 · Cited by 70
Anatomical evidence for collateral branching of substantia nigra neurons: a combined horseradish peroxidase and [3H]wheat germ agglutinin axonal transport study in the rat
Steindler, D. A., & Deniau, J. (1980) · Brain Research · doi:10.1016/0006-8993(80)90729-5 · Cited by 65
Organization of mesencephalic dopamine neurons projecting to neocortex and septum.
Lindvall, O., Björklund, A., & Divac, I. (1977) · PubMed · Cited by 55
The effect of long-term amphetamine administration on the activity of dopaminergic neurons of the substantia nigra
Staunton, D. A., Young, S. J., & Groves, P. M. (1980) · Brain Research · doi:10.1016/0006-8993(80)90560-0 · Cited by 26
A new approach to quantitate the density and antigen contents of high densities of transmitter-identified terminals. Immunocytochemical studies on different types of tyrosine hydroxylaxe immunoreactive nerve terminals in nucleus caudatus putamen of the rat
Agnati, L. F., Fuxé, K., Zini, I., Calzà, L., Benfenati, F., Zoli, M., Hökfelt, T. G. M., & Goldstein, M. (1982) · Neuroscience Letters · doi:10.1016/0304-3940(82)90302-0 · Cited by 23
Evidence for a morphologically distinct subpopulation of striatipetal axons following injections of WGA-HRP into the ventral tegmental area in the rat
Zahm, D. S. (1989) · Brain Research · doi:10.1016/0006-8993(89)90552-0 · Cited by 11

Research works printed but not linked: 2

Bjo ¨rklund A, Lindvall O (1984) Dopamine systems in the CNS. In: Hand- book of chemical neuroanatomy, Classical transmitters in the CNS, Part I (Bjo ¨rklund A, Ho ¨kfelt T, eds), pp 55-112. Amsterdam: Elsevier.
Gerfen CR, Wilson CJ (1996) The basal ganglia. In: Handbook of chem- ical anatomy, integrated systems in the CNS, Part III (Swanson LW, Bjo ¨rkulnd A, Ho ¨kfelt T, eds), pp 371-468. Amsterdam: Elsevier.

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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
DOI: 10.1523/jneurosci.21-18-07247.2001
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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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

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