The Concept of the Ventral Striatum in Nonhuman Primates
Abstract
ABSTRACT: The concept of the ventral striatum was first put forth by Heimer and Wilson to describe the extension of basal ganglia elements into the olfactory tubercle. The ventral striatum includes the conventional nucleus accumbens, which has been closely associated with reward and motivation. This paper uses the afferent connections to the ventral striatum to define this region in monkeys. Furthermore the shell and core subterritories are discussed with respect to their histochemistry and specific connections.
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The NAc, along with the extended amygdala, mediates reward-based drive and motivation.
“The NAc, along with the extended amygdala, mediates reward-based drive and motivation [61,62]”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [61]
Cites
Functional architecture of basal ganglia circuits: neural substrates of parallel processing
Alexander, G. E., & Crutcher, M. D. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90107-l · Cited by 4,131 · see citing works
Specificity in the projection patterns of accumbal core and shell in the rat
Heimer, L., Zahm, D. S., Churchill, L., Kalivas, P. W., & Wohltmann, C. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90202-y · Cited by 1,219 · see citing works
Alheid, G. F., & Heimer, L. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90217-5 · Cited by 1,217 · see citing works
Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys
Carmichael, S. T., & Price, J. L. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903630408 · Cited by 1,197 · see citing works
The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning
LeDoux, J., Cicchetti, P., Xagoraris, A., & Romanski, L. (1990) · The Journal of Neuroscience · doi:10.1523/jneurosci.10-04-01062.1990 · Cited by 1,167 · see citing works
Amygdalo‐cortical projections in the monkey ( <i>Macaca fascicularis</i> )
Amaral, D. G., & Price, J. L. (1984) · Journal of Comparative Neurology · doi:10.1002/cne.902300402 · Cited by 1,162 · see citing works
Brog, J. S., Salyapongse, A., Deutch, A. Y., & Zahm, D. S. (1993) · Journal of Comparative Neurology · doi:10.1002/cne.903380209 · Cited by 1,102 · see citing works
On the significance of subterritories in the “accumbens” part of the rat ventral striatum
Zahm, D. S., & Brog, J. S. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90202-d · Cited by 1,040 · see citing works
The Frontal Lobes and Voluntary Action
Passingham, R. (1993) · doi:10.1093/oso/9780198521853.001.0001 · Cited by 970 · see citing works
Pennartz, C. M. A., Groenewegen, H. J., & LOPESDASILVA, F. (1994) · Progress in Neurobiology · doi:10.1016/0301-0082(94)90025-6 · Cited by 802 · see citing works
Neurobiology of Cingulate Cortex and Limbic Thalamus
Vogt, B. A., & Gabriel, M. (1993) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4899-6704-6 · Cited by 772 · see citing works
Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey
Carmichael, S. T., & Price, J. L. (1994) · Journal of Comparative Neurology · doi:10.1002/cne.903460305 · Cited by 656 · see citing works
The orbital and medial prefrontal circuit through the primate basal ganglia
Haber, S., Kunishio, K., Mizobuchi, M., & Lynd-Balta, E. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-07-04851.1995 · Cited by 605 · see citing works
Self-citationGustatory, olfactory, and visual convergence within the primate orbitofrontal cortex
Rolls, E., & Baylis, L. (1994) · The Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05437.1994 · Cited by 587 · see citing works
The neurobiology of drug addiction
Koob, G. F., & Nestler, E. J. (1997) · Journal of Neuropsychiatry · doi:10.1176/jnp.9.3.482 · Cited by 572 · see citing works
Direct and indirect pathways from the amygdala to the frontal-lobe in rhesus-monkeys
Porrino, L. J., Crane, A. M., & Goldman‐Rakic, P. S. (1981) · Journal of Comparative Neurology · doi:10.1002/cne.901980111 · Cited by 491 · see citing works
Cholecystokinin innervation of the ventral striatum: A morphological and radioimmunological study
Záborszky, L., Alheid, G. F., Beinfeld, M. C., Eiden, L. E., Heimer, L., & Palkovits, M. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90302-1 · Cited by 489 · see citing works
The contribution of the amygdala to normal and abnormal emotional states
Aggleton, J. P. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90110-8 · Cited by 423 · see citing works
The accumbens: beyond the core-shell dichotomy
Heimer, L., Alheid, G. F., de Olmos, J. S., Groenewegen, H. J., Haber, S. N., Harlan, R. E., & Zahm, D. S. (1997) · Journal of Neuropsychiatry · doi:10.1176/jnp.9.3.354 · Cited by 418 · see citing works
Self-citationThe amygdalostriatal projections in the monkey. An anterograde tracing study
Russchen, F. T., Bakst, I., Amaral, D. G., & Price, J. L. (1985) · Brain Research · doi:10.1016/0006-8993(85)90530-x · Cited by 395 · see citing works
Anatomic and Behavioral Aspects of Frontal‐Subcortical Circuitsa
CUMMINGS, J. L. (1995) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1995.tb38127.x · Cited by 362 · see citing works
Parthasarathy, H. B., Schall, J. D., & Graybiel, A. M. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04468.1992 · Cited by 353 · see citing works
Chapter 29 The nucleus accumbens: gateway for limbic structures to reach the motor system?
Groenewegen, H. J., Wright, C. I., & Beijer, A. V. J. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61883-x · Cited by 344 · see citing works
Chikama, M., McFarland, N. R., Amaral, D. G., & Haber, S. N. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-24-09686.1997 · Cited by 341 · see citing works
Self-citationPrimate cingulostriatal projection: Limbic striatal versus sensorimotor striatal input
Kunishio, K., & Haber, S. N. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903500302 · Cited by 290 · see citing works
Self-citationLynd-Balta, E., & Haber, S. N. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90182-1 · Cited by 233 · see citing works
Self-citationHaber, S. N., & Elde, R. (1982) · Neuroscience · doi:10.1016/0306-4522(82)91118-6 · Cited by 232 · see citing works
Self-citationAfferent connections of the caudolateral orbitofrontal cortex taste area of the primate
Baylis, L. L., Rolls, E. T., & Baylis, G. C. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00449-f · Cited by 217 · see citing works
Neurophysiological analysis of brain-stimulation reward in the monkey
Rolls, E. T., Burton, M. J., & Mora, F. (1980) · Brain Research · doi:10.1016/0006-8993(80)91216-0 · Cited by 193 · see citing works
Haber, S. N., Ryoo, H., Cox, C., & Lu, W. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903620308 · Cited by 188 · see citing works
Self-citationThe 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 · see citing works
Self-citationBaylis, L. L., & Gaffan, D. (1991) · Experimental Brain Research · doi:10.1007/bf00230535 · Cited by 166 · see citing works
O’Donnell, P., & Grace, A. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-08-03456.1993 · Cited by 151 · see citing works
Benjamin, R. M., & Burton, H. (1968) · Brain Research · doi:10.1016/0006-8993(68)90100-5 · Cited by 148 · see citing works
Organization of thalamic projections to the ventral striatum in the primate
Giménez‐Amaya, J. M., McFarland, N. R., Heras, S. D. L., & Haber, S. N. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903540109 · Cited by 143 · see citing works
Self-citationFornix system efferent projections in the squirrel monkey: An experimental degeneration study
Poletti, C. E., & Creswell, G. F. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901750107 · Cited by 128 · see citing works
Goldman‐Rakic, P. S., & Selemon, L. D. (1986) · Cerebral cortex · doi:10.1007/978-1-4613-2149-1_12 · Cited by 109 · see citing works
Martin, L. J., Hadfield, M. G., Dellovade, T., & Price, D. L. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90303-6 · Cited by 101 · see citing works
François, C., Percheron, G., Parent, A., et al. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903050104 · Cited by 85 · see citing works
Martin, L., Blackstone, C. D., Huganir, R. L., & Price, D. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-02-00782.1993 · Cited by 80 · see citing works
Akert, K., & Monakow, K. H.-V. (1980) · Springer eBooks · doi:10.1007/978-94-009-8225-3_45 · Cited by 75 · see citing works
Mogenson, G. J., Brudzyński, S. M., Wu, M., Yang, C. R., & Yim, C. Y. (2019) · CRC Press eBooks · doi:10.1201/9780429274411-7 · Cited by 69 · see citing works
Hurd, Y. L., & Herkenham, M. A. (1995) · Neuroscience · doi:10.1016/0306-4522(94)00417-4 · Cited by 58 · see citing works
Neurochemical heterogeneity of the primate nucleus accumbens
Ikemoto, K., Satoh, K., Maeda, T., & Fibiger, H. C. (1995) · Experimental Brain Research · doi:10.1007/bf00242004 · Cited by 49 · see citing works
The Circuitry Mediating the Translation of Motivational Stimuli Into Adaptive Motor Responses
Kalivas, P. W., Churchill, L., & Klitenick, M. A. (2019) · CRC Press eBooks · doi:10.1201/9780429274411-8 · Cited by 47 · see citing works
Integrative Aspects of Basal Ganglia Circuitry
Haber, S. N., Lynd‐Balta, E., & Spooren, W. P. J. M. (1994) · Advances in behavioral biology · doi:10.1007/978-1-4613-0485-2_7 · Cited by 44 · see citing works
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Haber, S. N. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2003.10.003 · Cited by 1,479 · see citing works
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Kegeles, L. S., Abi-Dargham, A., Frankle, W. G., Gil, R., Cooper, T. B., Slifstein, M., Hwang, D.-R., Huang, Y., Haber, S. N., & Laruelle, M. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.10 · Cited by 565 · see citing works
Self-citationLeyton, M. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00366-4 · Cited by 476 · see citing works
Heinz, A., Siessmeier, T., Wrase, J., Hermann, D., Klein, S., Grüsser-Sinopoli, S. M., Flor, H., Braus, D. F., Buchholz, H. G., Gründer, G., et al. (2004) · American Journal of Psychiatry · doi:10.1176/ajp.161.10.1783 · Cited by 408 · see citing works
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Dichter, G. S., Damiano, C. A., & Allen, J. A. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-19 · Cited by 299 · see citing works
Porrino, L. J., Lyons, D., Smith, H. R., Daunais, J. B., & Nader, M. A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5578-03.2004 · Cited by 276 · see citing works
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- Authors
- HABER, S. N., & McFARLAND, N. R.
- Affiliations
- University of Rochester Medicine (US)
- Corresponding author
- HABER, SUZANNE N.
- Venue
- Annals of the New York Academy of Sciences
- Publisher
- Wiley
- Published
- 1999-06
- Volume
- 877
- Issue
- 1
- Pages
- 33-48
- ISSN
- 0077-8923 (ISSN-L)
- 1749-6632
- OpenAlex
- W2012187737
- Cited by
- 253
- References
- 47
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 6 · 2023: 7 · 2022: 4 · 2021: 9 · 2020: 3 · 2019: 8 · 2018: 9 · 2017: 6 · 2016: 10 · 2015: 9 · 2014: 7 · 2013: 13 · 2012: 17
- FWCI
- 0.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of the New York Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH11661, F31MH011661, MH45573)
- National Institute of Neurological Disorders and Stroke (NS22511, R01NS022511)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- ventral striatum, non-human primates, monkeys, nucleus accumbens, olfactory tubercle, basal ganglia, afferent connections, reward, motivation, histochemistry
- MeSH terms
- Animals, Basal Ganglia, Corpus Striatum, Motivation, Olfactory Pathways, Primates, Reward
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