Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study
Abstract
In situ hybridization histochemistry using cDNA oligonucleotide probes for the neuropeptides dynorphin, enkephalin and substance P was used to map the distribution of peptidergic neurons in the striatal patch and matrix compartments in the rat. Striatal neurons containing message for each of these peptides were distributed in both striatal compartments in the following proportions: dynorphin, in 52% of patch neurons and 45% of matrix neurons; enkephalin, in 65% of patch neurons and 58% of matrix neurons and substance P, in 61% of patch neurons of 54% matrix neurons. Fluorescent retrograde axonal tracing combined with in situ hybridization histochemistry demonstrated that the majority of neurons expressing enkephalin project to the globus pallidus and few project to the substantia nigra, whereas the reverse obtains for neurons expressing dynorphin and substance P.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the striatum, DA D2R is expressed in neurons containing enkephalin, the endogenous MOR ligand; both receptors are involved in pair bond formation but not maintenance.
“In the striatum, DA D2R is expressed in striatal neurons containing enkephalin, the endogenous ligand for MOR (Gerfen and Young 1988); both of which receptors are involved in pair bond formation but do not have a clear role in maintenance.”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Gerfen and Young 1988
Cites
Ljungdahl, Å., Hökfelt, T. G. M., & Nilsson, G. (1978) · Neuroscience · doi:10.1016/0306-4522(78)90116-1 · Cited by 1,434 · see citing works
Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties
Schmued, L. C., & Fallon, J. H. (1986) · Brain Research · doi:10.1016/0006-8993(86)91199-6 · Cited by 887 · see citing works
Gerfen, C. R. (1984) · Nature · doi:10.1038/311461a0 · Cited by 837 · see citing works
Self-citationImmunohistochemical localization of enkephalin in rat brain and spinal cord
Sar, M., Stumpf, W. E., Miller, R. J., Chang, K., & Cuatrecasas, P. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901820103 · Cited by 822 · see citing works
Elde, R., Hökfelt, T. G. M., Johansson, O., & Terenius, L. Y. (1976) · Neuroscience · doi:10.1016/0306-4522(76)90063-4 · Cited by 774 · see citing works
Mesencephalic dopamine neurons regulate the expression of neuropeptide mRNAs in the rat forebrain.
Young, W. S., Bonner, T. I., & Brann, M. R. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.24.9827 · Cited by 745 · see citing works
The distribution of substance P immunoreactive fibers in the rat central nervous system
Cuello, A. C., & Kanazawa, I. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901780108 · Cited by 728 · see citing works
The distribution of enkephalin-immunoreactive cell bodies in the rat central nervous system
Hökfelt, T. G. M., Elde, R. P., Johansson, O., Terenius, L. Y., & Stein, L. (1977) · Neuroscience Letters · doi:10.1016/0304-3940(77)90160-4 · Cited by 693 · see citing works
The structure of the caudate nucleus of the cat: light and electron microscopy
Kemp, J. M., & Powell, T. P. S. (1971) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1971.0102 · Cited by 672 · see citing works
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 636 · see citing works
Self-citationGerfen, C. R. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902360404 · Cited by 563 · see citing works
Self-citationThe immunocytochemical localization of enkephalin in the central nervous system of the rat
Finley, J. C. W., Maderdrut, J. L., & Petrusz, P. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901980402 · Cited by 555 · see citing works
Wilson, C. J., & Groves, P. M. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901940308 · Cited by 527 · see citing works
Herkenham, M. A., & Pert, C. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-08-01129.1982 · Cited by 466 · see citing works
Ribak, C. E., Vaughn, J. E., & Roberts, E. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870203 · Cited by 410 · see citing works
Graybiel, A. M., Ragsdale, C. W., Yoneoka, E. S., & Elde, R. P. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90131-7 · Cited by 396 · see citing works
Kanazawa, I., Emson, P. C., & Cuello, A. C. (1977) · Brain Research · doi:10.1016/0006-8993(77)90323-7 · Cited by 340 · see citing works
Medium spiny neuron projection from the rat striatum: An intracellular horseradish peroxidase study
Preston, R. J., Bishop, G. A., & Kitai, S. T. (1980) · Brain Research · doi:10.1016/0006-8993(80)90462-x · Cited by 321 · see citing works
The identification of striatal and pallidal neurons projecting to substantia nigra
Grofová, I. (1975) · Brain Research · doi:10.1016/0006-8993(75)90550-8 · Cited by 315 · see citing works
On the origin of substance P and glutamic acid decarboxylase (GAD) in the substantia nigra
Brownstein, M., Mroz, E. A., Tappaz, M., & Leeman, S. E. (1977) · Brain Research · doi:10.1016/0006-8993(77)91034-4 · Cited by 314 · see citing works
Oertel, W. H., & Mugnaini, E. (1984) · Neuroscience Letters · doi:10.1016/0304-3940(84)90519-6 · Cited by 282 · see citing works
Penny, G. R., Afsharpour, S., & Kitai, S. T. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90076-x · Cited by 276 · see citing works
Single Neostriatal Efferent Axons in the Globus Pallidus: A Light and Electron Microscopic Study
Chang, H. T., Wilson, C. J., & Kitai, S. T. (1981) · Science · doi:10.1126/science.7256286 · Cited by 271 · see citing works
Projections of substance P containing neurons from neostriatum to substantia nigra
Hong, J., Yang, H., Racagni, G., & Costa, E. (1977) · Brain Research · doi:10.1016/0006-8993(77)90464-4 · Cited by 254 · see citing works
Pickel, V. M., Sumal, K. K., Beckley, S. C., Miller, R. J., & Reis, D. J. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901890408 · Cited by 238 · see citing works
Dynorphin-immunoreactive neurons in the central nervous system of the rat
Vincent, S. R., Hökfelt, T. G. M., Christensson, I., & Terenius, L. Y. (1982) · Neuroscience Letters · doi:10.1016/0304-3940(82)90249-x · Cited by 231 · see citing works
Immunohistochemical evidence for a dynorphin immunoreactive striato-nigral pathway
Vincent, S. R., Hökfelt, T. G. M., Christensson, I., & Terenius, L. Y. (1982) · European Journal of Pharmacology · doi:10.1016/0014-2999(82)90477-0 · Cited by 223 · see citing works
Somogyi, P., & Smith, A. D. (1979) · Brain Research · doi:10.1016/0006-8993(79)90084-2 · Cited by 203 · see citing works
Bolam, J. P., Somogyi, P., Takagi, H., Fodor, I., & Smith, A. D. (1983) · Journal of Neurocytology · doi:10.1007/bf01148468 · Cited by 185 · see citing works
Beckstead, R. M., & Kersey, K. S. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902320406 · Cited by 185 · see citing works
Localization of immunoreactive enkephalins in GABA synthesizing neurons of the rat neostriatum
D, N. A. M., DiFiglia, M., Graveland, G. A., Schwartz, W. J., & Wu, J. (1984) · Brain Research · doi:10.1016/0006-8993(84)90850-3 · Cited by 167 · see citing works
DiFiglia, M., Aronin, N., & Jb, M. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-03-00303.1982 · Cited by 159 · see citing works
Compartmental distribution of striatal cell bodies expressing [Met]enkephalin-like immunoreactivity.
Graybiel, A. M., & Chesselet, M. ‐. (1984) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.81.24.7980 · Cited by 144 · see citing works
Somogyi, P., Priestley, J. V., Cuello, A. C., et al. (1982) · Journal of Neurocytology · doi:10.1007/bf01153519 · Cited by 119 · see citing works
Organization of the striatum: Collateralization of its Efferent Axons
Loopuijt, L. D., & van der Kooy, D. (1985) · Brain Research · doi:10.1016/0006-8993(85)90363-4 · Cited by 115 · see citing works
Oertel, W., Riethmüller, G., Mugnaini, E., Schmechel, D. E., Weindl, A., Gramsch, C., & Herz, A. (1983) · Life Sciences · doi:10.1016/0024-3205(83)90447-2 · Cited by 105 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The functional anatomy of basal ganglia disorders
Albin, R. L., Young, A. B., & Penney, J. B. (1989) · Trends in Neurosciences · doi:10.1016/0166-2236(89)90074-x · Cited by 5,353 · see citing works
Gerfen, C. R., Engber, T. M., Mahan, L. C., Susel, Z., Chase, T. N., Monsma, F. J., & Sibley, D. R. (1990) · Science · doi:10.1126/science.2147780 · Cited by 2,967 · see citing works
Self-citationA gene expression atlas of the central nervous system based on bacterial artificial chromosomes
Gong, S., Zheng, C., Doughty, M. L., Losos, K., Didkovsky, N., Schambra, U. B., Nowak, N. J., Joyner, A., Leblanc, G., Hatten, M. E., et al. (2003) · Nature · doi:10.1038/nature02033 · Cited by 2,108 · see citing works
The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia
Gerfen, C. R. (1992) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.15.030192.001441 · Cited by 1,004 · see citing works
Self-citationPhysiology and pharmacology of striatal neurons
Kreitzer, A. C. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135422 · Cited by 530 · see citing works
Taverna, S., Ilijic, E., & Surmeier, D. J. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5493-07.2008 · Cited by 399 · see citing works
Basal ganglia dysfunction in Tourette’s syndrome: a new hypothesis
Mink, J. W. (2001) · Pediatric Neurology · doi:10.1016/s0887-8994(01)00262-4 · Cited by 357 · see citing works
Newton, S. S., Thome, J., Wallace, T. L., Shirayama, Y., Schlesinger, L., Sakai, N., Chen, J., Neve, R., Nestler, E. J., & Duman, R. S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10883.2002 · Cited by 313 · see citing works
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
“In the striatum , DA D2R is expressed in striatal neurons containing enkephalin , the endogenous ligand for MOR ( Gerfen and Young 1988 ) ; both of which receptors are involved in pair bond formation but do not have a clear role in maintenance .”
Hohmann, A. G., & Herkenham, M. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00524-7 · Cited by 301 · see citing works
Gerfen, C., Keefe, K., & Gauda, E. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-12-08167.1995 · Cited by 283 · see citing works
Self-citationκ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance
Resendez, S. L., Kuhnmuench, M., Krzywosinski, T., & Aragona, B. J. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5779-11.2012 · Cited by 110 · see citing works
“D2-like receptors are expressed on neurons that contain enkephalin, an endogenous ligand for -opioid receptors that mediate motivation and positive hedonics (Bozarth and Wise, 1981; Gerfen and Young, 1988; Pecina and Berridge, 2005).”
BackgroundStillman, A. A., Krsnik, Ž., Sun, J., Rašin, M., State, M. W., šestan, N., & Louvi, A. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21919 · Cited by 95 · see citing works
Adenylyl Cyclase Type 5 Contributes to Corticostriatal Plasticity and Striatum-Dependent Learning
Kheirbek, M. A., Britt, J. P., Beeler, J. A., Ishikawa, Y., McGehee, D. S., & Zhuang, X. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3343-09.2009 · Cited by 93 · see citing works
Dopamine and opioid systems interact within the nucleus accumbens to maintain monogamous pair bonds
Resendez, S. L., Keyes, P. C., Day, J. J., Hambro, C., Austin, C. J., Maina, F. K., Eidson, L. N., Porter-Stransky, K. A., Nevárez, N., McLean, J. W., et al. (2016) · eLife · doi:10.7554/elife.15325 · Cited by 88 · see citing works
Gerfen, C. R. (2004) · The Rat Nervous System · doi:10.1016/b978-012547638-6/50019-5 · Cited by 85 · see citing works
Self-citationRegulation of striatal cells and goal-directed behavior by cerebellar outputs
Xiao, L., Bornmann, C., Hatstatt-Burklé, L., & Scheiffele, P. (2018) · Nature Communications · doi:10.1038/s41467-018-05565-y · Cited by 82 · see citing works
Nicotine and endogenous opioids: neurochemical and pharmacological evidence
Hadjiconstantinou, M., & Neff, N. H. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.11.010 · Cited by 81 · see citing works
Ehrman, L. A., Mu, X., Waclaw, R. R., Yoshida, Y., Vorhees, C. V., Klein, W. H., & Campbell, K. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1308275110 · Cited by 79 · see citing works
Kelly, S. M., Raudales, R., He, M., Lee, J. H., Kim, Y., Gibb, L. G., Wu, P., Matho, K., Osten, P., Graybiel, A. M., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.06.021 · Cited by 68 · see citing works
Reduced Slc6a15 in Nucleus Accumbens D2-Neurons Underlies Stress Susceptibility
Chandra, R., Francis, T. C., Nam, H., Riggs, L. M., Engeln, M., Rudzinskas, S., Konkalmatt, P., Russo, S. J., Turecki, G., Iniguez, S. D., et al. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.3250-16.2017 · Cited by 49 · see citing works
Choi, K. H., Zarandi, B., Todd, K. G., Biondo, A. M., & Greenshaw, A. J. (2000) · Psychopharmacology · doi:10.1007/s002130000391 · Cited by 23 · see citing works
Tanimoto, Y., Kakinuma, H., Aoki, R., Shiraki, T., Higashijima, S.-I., & Okamoto, H. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113916 · Cited by 16 · see citing works
- Authors
- Gerfen, C. R., & Scott Young, W.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Gerfen, Charles R.
- ORCID
- Gerfen, Charles R.
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 1988-09
- Volume
- 460
- Issue
- 1
- Pages
- 161-167
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W1975814998
- Cited by
- 658
- References
- 36
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 3 · 2023: 7 · 2022: 8 · 2021: 6 · 2020: 10 · 2019: 19 · 2018: 12 · 2017: 10 · 2016: 21 · 2015: 14 · 2014: 19 · 2013: 12 · 2012: 11
- FWCI
- 5.92
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- striatonigral neurons, striatopallidal neurons, peptidergic neurons, dynorphin, enkephalin, substance P, globus pallidus, substantia nigra, neuropeptide expression
- MeSH terms
- Animals, Axonal Transport, Corpus Striatum, DNA, Dynorphins, Enkephalins, Globus Pallidus, Histocytochemistry, Male, Neurons, Neuropeptides, Nucleic Acid Hybridization, Rats, Inbred Strains, Receptors, Opioid, RNA, Messenger, Substance P, Substantia Nigra, Transcription, Genetic, Oligonucleotide Probes, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
