On the significance of subterritories in the “accumbens” part of the rat ventral striatum

Zahm, D.S.; Brog, J.S.

doi:10.1016/0306-4522(92)90202-d

Cited by 1,040Neurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology ResearchNeurological disorders and treatments

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

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Abstract

Although many workers have appreciated the striking cytologic and neurochemical similarities of neostriatum, accumbens and olfactory tubercle, a compelling case for regarding these areas as territories in a striatal complex awaited the arguments made by Heimer and his colleagues based on their investigations of connections. A number of recent papers support this viewpoint and extend it with the characterization of three accumbal subterritories: core, shell and rostral pole. The case for separate classifications of systems traversing the accumbens has become more compelling with each study that demonstrates connectional, cytoarchitectural and neurochemical specificity conforming to the boundaries separating the core and its downstream targets from the shell and its projection fields. Furthermore, its apparent composite of core-like and shell-like characteristics distinguishes the rostral pole as yet another unique subterritory. Differences in compartmental organization distinguish the accumbens and neostriatum. The available data are consistent with the periventricular and rostrolateral enkephalin-rich zones being ventralmost parts of the neostriatal patch and matrix compartments, respectively. The accumbal cell cluster compartment, on the other hand, appears to be a separate entity, with connectional and neurochemical features that are dissimilar to both patch and matrix of neostriatum. Boundaries between the accumbens and caudate-putamen remain elusive, and the point of view that such boundaries do not exist but, rather, are represented by "transition zones" must to a large degree reflect the reality. Likewise, it is important to acknowledge that the boundaries between accumbal subterritories are not necessarily distinct or observed faithfully by all of the afferent systems. "Transition zones" appear to be particularly significant organizational features in rostral and lateral parts of the accumbens. Interestingly, histochemically distinct cell clusters tend to be numerous in boundary regions between adjacent territories and subterritories. The predominant organizational pattern appears to be one in which the core, shell and rostral pole engage different forebrain systems that possibly subserve entirely different functions mediated by distantly related mechanisms. In this regard, it is of paramount interest that the processing of information conveyed to the accumbens by diverse cortical and subcortical inputs occurs within distinct and perhaps very different dopaminergic environments in the core, shell and rostral pole (e.g., see Refs 24, 34, 90, 110).

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Functional differences exist between the two accumbens compartments, shell and core.
“These results confirm functional differences between the two accumbens compartments inferred from anatomical observations that the afferents to and efferents from the accumbens differ significantly between the shell and core”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Zahm and Brog, 1992
Anatomical and functional differences between the anterior and posterior ventral striatum have been reported for the nucleus accumbens in particular.
“In fact, anatomical and functional differences between the anterior and posterior ventral striatum have been reported by many researchers for the nucleus accumbens in particular (e.g., Fallon and Moore, 1978; Voorn and Docter, 1992; Zahm and Brog, 1992; Reynolds and Berridge, 2002; Zangen et al., 2006).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Zahm and Brog, 1992

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The ventral striatopallidothalamic projection: II. The ventral pallidothalamic link
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Immunocytochemical localization of choline acetyltransferase in rat ventral striatum: a light and electron microscopic study
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The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes
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Neurobiology of addiction
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Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents
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The organization of the basal ganglia-thalamocortical circuits: Open interconnected rather than closed segregated
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Functional–anatomical implications of the nucleus accumbens core and shell subterritories
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Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour
Hall, J., Parkinson, J. A., Connor, T. M., Dickinson, A., & Everitt, B. J. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01577.x · Cited by 355 · see citing works
A proposed hypothalamic–thalamic–striatal axis for the integration of energy balance, arousal, and food reward
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The role of the striatum in aversive learning and aversive prediction errors
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Rewarding Actions of Phencyclidine and Related Drugs in Nucleus Accumbens Shell and Frontal Cortex
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Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep–wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats
Léna, I., Parrot, S., Deschaux, O., Muffat‐Joly, S., Sauvinet, V., Renaud, B., Suaud‐Chagny, M. ‐., & Gottesmann, C. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20602 · Cited by 322 · see citing works
Contributions of the striatum to learning, motivation, and performance: an associative account
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Fear and Feeding in the Nucleus Accumbens Shell: Rostrocaudal Segregation of GABA-Elicited Defensive Behavior Versus Eating Behavior
Reynolds, S. M., & Berridge, K. C. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-09-03261.2001 · Cited by 281 · see citing works
The persistence of maladaptive memory: Addiction, drug memories and anti-relapse treatments
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The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia
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IκB Kinase Regulates Social Defeat Stress-Induced Synaptic and Behavioral Plasticity
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Nucleus accumbens dopamine depletions make rats more sensitive to high ratio requirements but do not impair primary food reinforcement
Aberman, J. E., & Salamone, J. D. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00004-4 · Cited by 263 · see citing works
Nucleus Accumbens μ-Opioid Receptors Mediate Social Reward
Trezza, V., Damsteegt, R., Achterberg, E. J. M., & Vanderschuren, L. J. M. J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5492-10.2011 · Cited by 263 · see citing works
The Concept of the Ventral Striatum in Nonhuman Primates
HABER, S. N., & McFARLAND, N. R. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09259.x · Cited by 253 · see citing works
Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical–ventral striatopallidal systems
Parkinson, J. A., Willoughby, P. J., Robbins, T. W., & Everitt, B. J. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.1.42 · Cited by 314 · see citing works
α6-Containing nicotinic acetylcholine receptors dominate the nicotine control of dopamine neurotransmission in nucleus accumbens
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Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study
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Specificity in the Projections of Prefrontal and Insular Cortex to Ventral Striatopallidum and the Extended Amygdala
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The putative role of extra-synaptic mesolimbic dopamine in the neurobiology of nicotine dependence
Balfour, D. J. K., Wright, A. E., Benwell, M. E. M., & Birrell, C. E. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00202-3 · Cited by 231 · see citing works
Dopamine or opioid stimulation of nucleus accumbens similarly amplify cue‐triggered ‘wanting’ for reward: entire core and medial shell mapped as substrates for <scp>PIT</scp> enhancement
Peciña, S., & Berridge, K. C. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12174 · Cited by 216 · see citing works
The dopaminergic hyper-responsiveness of the shell of the nucleus accumbens is hormone-dependent
Barrot, M., Marinelli, M., Abrous, D. N., Rougé‐Pont, F., Le Moal, M., & Piazza, P. V. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00996.x · Cited by 210 · see citing works
Functional Specificity of Ventral Striatal Compartments in Appetitive Behaviors
KELLEY, A. E. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09262.x · Cited by 198 · see citing works
Preferential Reactivation of Motivationally Relevant Information in the Ventral Striatum
Lansink, C. S., Goltstein, P. M., Lankelma, J. V., Joosten, R. N. J. M. A., McNaughton, B. L., & Pennartz, C. M. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1054-08.2008 · Cited by 168 · see citing works
Differential behavioral responses to dopaminergic stimulation of nucleus accumbens subregions in the rat
Swanson, C. J., Heath, S., Stratford, T. R., & Kelley, A. E. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(97)00043-9 · Cited by 176 · see citing works
Habit-forming actions of nomifensine in nucleus accumbens
Carlezon, W. A., Devine, D. P., & Wise, R. A. (1995) · Psychopharmacology · doi:10.1007/bf02246095 · Cited by 170 · see citing works
Role of nucleus accumbens in neuropathic pain: Linked multi-scale evidence in the rat transitioning to neuropathic pain
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Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (<i>Microtus ochrogaster</i>)
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Nucleus Accumbens Modulation in Reward and Aversion
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Limbic cortical-ventral striatal systems underlying appetitive conditioning
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Cortical Cholinergic Transmission and Cortical Information Processing in Schizophrenia
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Patterns of overlap and segregation between insular cortical, intermediodorsal thalamic and basal amygdaloid afferents in the nucleus accumbens of the rat
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Differential involvement of the shell and core subterritories of the nucleus accumbens in latent inhibition and amphetamine-induced activity
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A Role for Phasic Dopamine Release within the Nucleus Accumbens in Encoding Aversion: A Review of the Neurochemical Literature
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The nucleus accumbens and reward: neurophysiological investigations in behaving animals
Carelli, R. M. (2002) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582302238338 · Cited by 131 · see citing works
Neural encoding of cocaine‐seeking behavior is coincident with phasic dopamine release in the accumbens core and shell
Owesson‐White, C. A., Ariansen, J., Stuber, G. D., Cleaveland, N. A., Cheer, J. F., Mark Wightman, R., & Carelli, R. M. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06916.x · Cited by 126 · see citing works
The human basal forebrain. Part II
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Kicking the habit: The neural basis of ingrained behaviors in cocaine addiction
Pierce, R. C., & Vanderschuren, L. J. M. J. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.01.007 · Cited by 115 · see citing works
Dynamics of rapid dopamine release in the nucleus accumbens during goal-directed behaviors for cocaine versus natural rewards
Cameron, C. M., Wightman, R. M., & Carelli, R. M. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.08.006 · Cited by 109 · see citing works
The Neuronal Pathways Mediating the Behavioral and Addictive Properties of Nicotine
Balfour, D. J. K. (2009) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-540-69248-5_8 · Cited by 99 · see citing works
Nucleus Accumbens Core Mammalian Target of Rapamycin Signaling Pathway Is Critical for Cue-Induced Reinstatement of Cocaine Seeking in Rats
Wang, X., Luo, Y.-X., He, Y.-Y., Li, F.-Q., Shi, H.-S., Xue, L.-F., Xue, Y.-X., & Lu, L. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1264-10.2010 · Cited by 88 · see citing works
The conditions that promote fear learning: Prediction error and Pavlovian fear conditioning
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A framework for understanding the emerging role of corticolimbic-ventral striatal networks in OCD-associated repetitive behaviors
Wood, J., & Ahmari, S. E. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00171 · Cited by 85 · see citing works
“…pathway contains medium spiny neurons expressing D2 receptors, and projects to the ventral pallidum and subthalamic nucleus (Albin et al., 1989; Zahm and Brog, 1992; Graybiel, 2000; Zhou et al., 2003; Humphries and Prescott, 2010; Kravitz et al., 2010; Sesack and Grace, 2010; Freeze et al.,…”
Background
Disruption of dopaminergic neurotransmission in nucleus accumbens core inhibits the locomotor stimulant effects of nicotine and d-amphetamine in rats
Boye, S. M., Grant, R. J., & Clarke, P. B. S. (2001) · Neuropharmacology · doi:10.1016/s0028-3908(01)00003-x · Cited by 87 · see citing works
Role of glutamatergic system and mesocorticolimbic circuits in alcohol dependence
Alasmari, F., Goodwani, S., McCullumsmith, R. E., & Sari, Y. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.10.001 · Cited by 85 · see citing works
High-frequency stimulation of the nucleus accumbens core and shell reduces quinpirole-induced compulsive checking in rats
Mundt, A., Klein, J., Joel, D., Heinz, A., Djodari‐Irani, A., Harnack, D., Kupsch, A., Orawa, H., Juckel, G., Morgenstern, R., et al. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06777.x · Cited by 80 · see citing works
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Authors: Zahm, D. S., & Brog, J. S.
Affiliations: Saint Louis University (US)
Corresponding author: Zahm, D.S.
ORCID: Zahm, D.S.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 1992-10
Volume: 50
Issue: 4
Pages: 751-767
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/0306-4522(92)90202-d
OpenAlex: W2014415095
Cited by: 1,040
References: 106
Citations by year: 2026: 5 · 2025: 11 · 2024: 10 · 2023: 14 · 2022: 16 · 2021: 18 · 2020: 16 · 2019: 27 · 2018: 23 · 2017: 24 · 2016: 23 · 2015: 29 · 2014: 33 · 2013: 18 · 2012: 32
FWCI: 3.99
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: American Parkinson Disease Association
Parkinson Vereniging
National Institutes of Health
U.S. Public Health Service
Parkinsonfonden
National Institute of Neurological Disorders and Stroke (NS23805, R01NS023805)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Health Sciences › Medicine › Neurology › Neurological disorders and treatments
Keywords: ventral striatum, accumbens, neostriatum, olfactory tubercle, caudate-putamen, transition zone, afferent connections
MeSH terms: Animals, Corpus Striatum, Humans, Nucleus Accumbens, Rats

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On the significance of subterritories in the “accumbens” part of the rat ventral striatum

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