Hostname: page-component-848d4c4894-75dct Total loading time: 0 Render date: 2024-06-05T14:25:16.429Z Has data issue: false hasContentIssue false

The Ventral Striatum as an Interface Between the Limbic and Motor Systems

Published online by Cambridge University Press:  07 November 2014

Extract

Over the next 2 years, CNS Spectrums will be publishing a series of articles on neuroanatomy. The purpose of these articles is to broaden knowledge and interest in neuroanatomy, with a special reference to some key brain structures that are important for neuropsychiatry. Interest in nuclear structures and hodology, in connectivity and circuitry between brain regions, and in neurochemical associations has increased in the last 3 decades due to new neuroanatomical staining methods, brain imaging, and new treatments, such as deep brain stimulation.These columns will enliven an understanding of the clinical neuroscience interface but also provide a solid framework of contemporary neuroanatomy for psychiatrists and neurologists.

The first in the series reviews the ventral striatum. Henk J. Groenewegen, MD, PhD, in a column dedicated to the late Lennart Heimer, MD, reveals the importance of this structure and its connectivity for a contemporary understanding of brain-behavior relationships. In earlier conceptions, the basal ganglia were solely related to motor function, uninvolved with emotion or cognition. This conception arose from a misunderstanding of basic neuroanatomy, which has been unravelled by careful neuroanatomical studies in the last 30 years with new tissue staining and tracing techniques.The basal ganglia are the main target structures of the limbic system, hence the motion in emotion.

Type
Brain Regions of Interest
Copyright
Copyright © Cambridge University Press 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1.Heimer, L, Wilson, RD. The subcortical projections of the allocortex: similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. In: Santini, M, ed. Perspectives in Neurobiology. Golgi Centennial Symposium, New York, NY: Raven Press; 1975:177193.Google Scholar
2.Alexander, GE, Crutcher, MD, DeLong, M. Basal ganglia-thalamocortlcal circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions. Prog Brain Res. 1990;85:119146.CrossRefGoogle ScholarPubMed
3.Everitt, BJ, Parkinson, JA, Olmstead, M, Arroyo, M, Robledo, P, Robbins, TW. Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann N Y Acad Sci. 1999;877:412438.CrossRefGoogle ScholarPubMed
4.Robbins, TW, Everitt, BJ. Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem. 2002;78:625636.CrossRefGoogle ScholarPubMed
5.Van den Heuvel, OA, Veltman, DJ, Groenewegen, HJ, et al.Disorder-specific neuroanatomical correlates of attentional bias in obsessive-compulsive disorder, panic disorder and hypochondriasis. Arch Gen Psychiatry. 2005;62:922933.CrossRefGoogle ScholarPubMed
6.Grace, AA. Gating of information flow within the limbic system and the pathophysiology of schizophrenia. Brain Res Rev. 2000;31:330341.CrossRefGoogle ScholarPubMed
7.Heimer, L. Basal forebrain in the context of schizophrenia. Brain Res Rev. 2000;31:205235.CrossRefGoogle ScholarPubMed
8.Voorn, P, Vanderschuren, LJ, Groenewegen, H, Robbins, T, Pennartz, C. Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 2004;27:468474.CrossRefGoogle ScholarPubMed
9.Fudge, JL, Haber, SN. Defining the caudal ventral striatum in primates: cellular and histochemical features. J Neurosci. 2002;22:10781082.CrossRefGoogle ScholarPubMed
10.Meredith, GE. The synaptic framework for chemical signaling in nucleus accumbens. Ann N Y Acad Sci. 1999;877:140156.CrossRefGoogle ScholarPubMed
11.Zaborszky, L, Alheid, GR, Beinfeld, MC, Eiden, LE, Heimer, L, Palkovits, M. Cholecystokinin innervation of the ventral striatum: a morphological and radioimmunological study. Neuroscience. 1985;4:427453.CrossRefGoogle Scholar
12.Groenewegen, HJ, Wright, CI, Beijer, A. The nucleus accumbens: gateway for limbic structures to reach the motor system? Prog Brain Res. 1996;107:485511.CrossRefGoogle ScholarPubMed
13.Zahm, DS, Brag, JS. On the significance of subterritories in the “accumbens”part of the rat ventral striatum. Neuroscience. 1992;50:751767.CrossRefGoogle ScholarPubMed
14.Meredith, GE, Pattiselanno, A, Groenewegen, HJ, Haber, SN. Shell and core in monkey and human nucleus accumbens identified with antibodies to calbindin-D28k. J Comp Neurol. 1996;365:628639.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
15.Graybiel, AM. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci. 1990;13:244254.CrossRefGoogle ScholarPubMed
16.Heimer, L. de Olmos, JS, Alheid, GF, et al.The human basal forebrain. Part II. In: Bloom, FE, Björklund, A, Hökfelt, T, eds. The Primate Nervous System, Part III (Handbook of Chemical Neuroanatomy, Vol 15). Amsterdam, the Netherlands: Elsevier; 1999:57226.CrossRefGoogle Scholar
17.Voorn, R, Brady, LS, Berendse, HW, Richfield, EK. Densitometrical analysis of opioid receptor ligand binding in the human striatum—I. Distribution of mu opioid receptor defines shell and core of the ventral striatum. Neuroscience. 1996;75:777792.CrossRefGoogle ScholarPubMed
18.Berendse, HW, Richfield, EK. Heterogeneous distribution of dopamine D1 and D2 receptors in the human ventral striatum. Neurosci Lett. 1993;150:7579.CrossRefGoogle ScholarPubMed
19.Joyce, JN, Gurevich, EV. D3 receptors and the actions of neuroleptics in the ventral striatopallidal system of schizophrenics. Ann N Y Acad Sci. 1999;877:595613.CrossRefGoogle ScholarPubMed
20.Schwartz, JC, Diaz, J, Pilon, C, Sokoloff, P. Possible implications of the dopamine D(3) receptor in schizophrenia and in antipsychotic drug actions. Brain Res Rev. 2000;31:277287.CrossRefGoogle ScholarPubMed
21.Ferry, AT, Ongur, D, An, X, Price, JL. Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J Comp Neurol. 2000;425:447470.3.0.CO;2-V>CrossRefGoogle Scholar
22.Kunishio, K, Haber, SN. Primate cingulostriatal projection: limbic striatal versus sensorimotor striatal input. J Comp Neurol. 1994;350:337356.CrossRefGoogle ScholarPubMed
23.Groenewegen, HJ, Berendse, HW, Haber, S. Organization of the output of the-ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience. 1993;57:113142.CrossRefGoogle ScholarPubMed
24.Bolam, JP, Hanley, JJ, Booth, P, Bevan, M. Synaptic organisation of the basal ganglia. J Anat. 2000;196:527542.CrossRefGoogle ScholarPubMed
25.Haber, SN, Wolfe, DP, Groenewegen, H. The relationship between ventral striatal efferent fibers and the distribution of peptide-positive woolly fibers in the forebrain of the rhesus monkey. Neuroscience. 1990;39:323338.CrossRefGoogle ScholarPubMed
26.Deniau, JM, Menetrey, A, Thierry, AM. Indirect nucleus accumbens input to the prefrontal cortex via the substantia nigra pars reticulata: a combined anatomical and electrophysiological study in the rat. Neuroscience. 1994;61:533545.CrossRefGoogle Scholar
27.Groenewegen, HJ, Berendse, HW. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol. 1990;294:607622.CrossRefGoogle ScholarPubMed
28.Berridge, CW, Stratford, TL, Foote, S, Kelley, A. Distribution of dopamine beta-hydroxylase-like immunoreactive fibers within the shell subregion of the nucleus accumbens. Synapse. 1997;27:2302413.0.CO;2-E>CrossRefGoogle ScholarPubMed
29.Nauta, WJ, Smith, GP, Fauli, RL, Domesick, VB. Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience. 1978;3:385401.CrossRefGoogle ScholarPubMed
30.Groenewegen, HJ, Van den Heuvel, OA, Cath, DC, Voorn, P. Veltman, DJ. Does an imbalance between the dorsal and ventral striatopallidal systems play a role in Tourette's Syndrome? A neuronal circuit approach. Brain Dev. 2003;25:S3S14.CrossRefGoogle ScholarPubMed
31.Haber, SN, Fudge, JL, McFarland, N. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci. 2000;20:23692382.CrossRefGoogle ScholarPubMed
32.Mogenson, GJ, Jones, DL, Yim, C. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol. 1980;14:6997.CrossRefGoogle ScholarPubMed
33.Maldonado-lrizarry, CS, Kelley, AE. Excitotoxic lesions of the core and shell subregions of the nucleus accumbens differentially disrupt body weight regulation and motor activity in rat. Brain Res Bull. 1995;38:551559.CrossRefGoogle Scholar
34.Kelley, AE. Neural integrative activities of nucleus accumbens subregions in relation to learning and motivation. Psychobiol. 1999;27:198213.CrossRefGoogle Scholar
35.Kelley, AE. Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobeh Rev. 2004;27:765776.CrossRefGoogle ScholarPubMed
36.Reynolds, SM, Berridge, KC. Fear and feeding in the nucleus accumbens shell: rostrocaudal segregation of GABA-elicited defensive behavior versus eating behavior. J Neurosci. 2001;21:32613270.CrossRefGoogle ScholarPubMed
37.Reynolds, SM, Berridge, KC. Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste “liking”/”disliking” reactions, place preference/avoidance, and fear. J Neurosci. 2002;22:73087320.CrossRefGoogle Scholar
38.Reynolds, SM, Berridge, KC. Glutamate motivational ensembles in nucleus accumbens: rostrocaudal shell gradients of fear and feeding. Eur J Neurosci. 2003:17:21872200.CrossRefGoogle ScholarPubMed
39.Cardinal, RN. Parkinson, JA, Hall, J, Everitt, BJ. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobeh Rev. 2002;26:321352.CrossRefGoogle ScholarPubMed
40.Parkinson, JA, Olmstead, MC, Bums, L, Robbins, T, Everitt, B. Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J Neurosci. 1999;19:24012411.CrossRefGoogle ScholarPubMed
41.Bell, K, Duffy, P, Kalivas, PW. Context-specific enhancement of glutamate transmission by cocaine. Neumpsycopharmacology. 2000;23:335344.CrossRefGoogle ScholarPubMed
42.Corbit, LH, Muir, JL, Balleine, B. The role of the nucleus accumbens in instrumental conditioning: evidence of a functional dissociation between accumbens core and shell. J Neurosci. 2001;21:32513260.CrossRefGoogle ScholarPubMed
43.Fenu, S, Acquas, E, Di Chiara, G. Role of striatal acetylcholine on dopamine D1 receptor agonist-induced turning behavior in 6-hydroxydopamine lesioned rats: a microdialysis-behavioral study. Neurol Sci. 2001;22:6364.CrossRefGoogle ScholarPubMed
44.Hotsenpiller, G, Giorgetti, M, Wolf, ME. Alterations n behaviour and glutamate transmission following presentation of stimuli previously associated with cocaine exposure. Eur J Neurosci. 2001;14:18431855.CrossRefGoogle Scholar
45.Di Chiara, G. Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res. 2002;137:75114.CrossRefGoogle ScholarPubMed
46.Phillips, GD, Setzu, E, Vugler, A, Hitchcott, PK. Immunohistochemical assessment of mesotelencephalic dopamine activity during the acquisition and expression of pavlovian versus instrumental behaviors. Neuroscience. 2003;117:755767.CrossRefGoogle Scholar
47.Ito, R, Robbins, TW, Everitt, B. Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat Neurosci. 2004;7:389397.CrossRefGoogle ScholarPubMed
48.Sellings, LH, McQuade, LE, Clarke, P. Evidence for multiple sites within rat ventral striatum mediating cocaine-conditioned place preference and locomotor activation. J Pharmacol Exp Ther. 2006:317:11781187.CrossRefGoogle ScholarPubMed
49.Van Kuyck, K, Gabriels, L, Cosyns, P, et alBehavioural and physiological effects of electrical stimulation in the nucleus accumbens: a review. Acta Neurochir Suppl. 2007;97(pt 2):375391.CrossRefGoogle ScholarPubMed
50.Pakkenberg, B. Pronounced reduction of total neuron number in mediodorsal thalamic nucleus and nucleus accumbens in schizophrenics. Arch Gen Psychiatry. 1990;47:10231028.CrossRefGoogle ScholarPubMed
51.Baumann, B, Bogerts, B. The pathomorphology of schizophrenia and mood disorders: similarities and differences. Schizophr Res. 1999;39:141148.CrossRefGoogle ScholarPubMed
52.Chambers, RA, Krystal, JH, Self, D. A neurobiological basis for substance abuse comorbidity in schizophrenia. Biol Psychiatry. 2001;50:7183.CrossRefGoogle ScholarPubMed
53.Brody, AL. Functional brain imaging of tobacco use and dependence. J Psychiatr Res. 2006;40:404418.CrossRefGoogle ScholarPubMed
54.Kalivas, PW, Volkow, N, Seamans, J. Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron. 2005;45:647650.CrossRefGoogle ScholarPubMed
55.Sturm, V, Lenartz, D, Koulousakis, A, et al.The nucleus accumbens: a target for deep brain stimulation in obsessive-compulsive- and anxiety-disorders. J Chem Neuroanat. 2003;26:293299.CrossRefGoogle ScholarPubMed