Abstract
Nigrostriatal dopaminergic neurons are usually considered to interface the ventral limbic and dorsal sensorimotor striatum, since the shell of the nucleus accumbens (Acb shell) projects to the ventral tegmental area/substantia nigra pars compacta (VTA/SNC) complex. However, both the organization of Acb shell projections to the nigrostriatal neurons innervating the sensorimotor striatum and the synaptic influence exerted by the Acb shell on these neurons remain to be determined. These questions were addressed in the rat using neuroanatomical and electrophysiological approaches.
Combined anterograde tracing from the Acb shell with retrograde tracing from the sensorimotor region of the dorsal striatum revealed that labeled fibers from the Acb shell overlap retrogradely labeled nigrostriatal neurons located in the medial SNC and the lateral VTA but avoid the nigrostriatal neurons located laterally. In addition, stimulation of the Acb-shell induced an inhibition of dopaminergic nigrostriatal neurons projecting to the sensorimotor striatal territory. In agreement with the anatomical observations, these responses were observed in nigrostriatal neurons located in the medial SNC and the lateral VTA but not in nigrostriatal neurons located laterally.
These data further establish the existence of a functional link between the Acb shell and the sensorimotor striatum via dopaminergic nigrostriatal neurons. The present study also reveals that among the dopaminergic nigrostriatal neurons innervating the sensorimotor striatal territory, only the subpopulation located in the medial SNC and lateral VTA receives an inhibitory input from the Acb shell. This indicates a functional heterogeneity within the population of dopaminergic neurons innervating a given striatal territory.
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Alexander GE and Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13: 266–271.
Belin D and Everitt BJ (2008) Cocaine seeking habits depend upon dopamine-dependent connectivity linking the ventral with the dorsal striatum. Neuron 57: 432–441.
Deniau JM and Thierry AM (1997) Anatomical segregation of information processing in the rat substantia nigra pars reticulata. Adv Neurol 74: 83–96.
Deniau JM, Hammond C, Riszk A and Feger J (1978) Electrophysiological properties of identified output neurons of the rat substantia nigra (pars compacta and pars reticulata): evidences for the existence of branched neurons. Exp Brain Res 32: 409–422.
Deniau JM, Menetrey A and Charpier S (1996) The lamellar organization of the rat substantia nigra pars reticulata: Segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections. Neuroscience 73: 761–781.
Ferraguti F, Zoli M, Aronsson M, Agnati LF, Goldstein M, Filer D and Fuxe K (1990) Distribution of glutamic acid decarboxylase messenger RNA-containing nerve cell populations in the male rat brain. J Chem Neuroanat 3: 377–396.
Groenewegen HJ, Berendse HW and Wouterlood FG (1994) Organization of the projections from the ventral striatopallidal system to ventral mesencephalic dopaminergic neurons. In: Percheron G and McKenzie JS (eds) The Basal Ganglia IV. Plenum, New York, NY, pp. 81–93.
Groenewegen HJ, Wright CI, Beijer AV and Voorn P (1999) Convergence and segregation of ventral striatal inputs and outputs. Ann NY Acad Sci 877: 49–63.
Guyenet PG and Aghajanian GK (1978) Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra. Brain Res 150: 69–84.
Haber SN, Fudge JL and McFarland NR (2000) Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20: 2369–2382.
Heimer L, Zahm DS, Churchill L, Kalivas PW and Wohltmann C (1991) Specificity in the projection patterns of the accumbal core and shell in the rat. Neuroscience 41: 89–125.
Heimer L, Alheid GF, de Olmos JS, Groenewegen HJ, Haber SN, Harlan RE and Zahm DS (1997) The accumbens: Beyond the Core-Shell dichotomy. J Neuropsychiatry Clin Neurosci 9: 354–381.
Ikemoto S (2007) Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56: 27–78.
Mailly P, Charpier S, Mahon S, Menetrey A, Thierry AM, Glowinski J and Deniau JM (2001) Dendritic arborizations of the rat substantia nigra pars reticulata neurons: Spatial organization and relation to the lamellar compartmentation of striato-nigral projections. J Neurosci 21: 6874–6888.
Maurice N, Deniau JM, Menetrey A, Glowinski J and Thierry AM (1997) Position of the ventral pallidum in the rat prefrontal cortex-basal ganglia circuit. Neuroscience 80: 523–534.
Maurice N, Deniau JM, Menetrey A, Glowinski J and Thierry AM (1998) Prefrontal cortex-basal ganglia circuits in the rat: Involvement of ventral pallidum and subthalamic nucleus. Synapse 29: 363–370.
Maurin Y, Banrezes B, Menetrey A, Mailly P and Deniau JM (1999) Three-dimensional distribution of nigrostriatal neurons in the rat: Relation to the topography of striatonigral projections. Neuroscience 91: 891–909.
Montaron MF, Deniau JM, Menetrey A, Glowinski J and Thierry AM (1996) Prefrontal cortex inputs of the nucleus accumbens-nigro-thalamic circuit. Neuroscience 71: 371–382.
Nauta WJ, Smith GP, Faull RL and Domesick VB (1978) Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience 3: 385–401.
Otake K and Nakamura Y (2000) Possible pathways through which neurons of the shell of the nucleus accumbens influence the outflow of the core of the nucleus accumbens. Brain Dev 22: S17–26.
Paxinos G and Watson C (1996) The Rat Brain in Stereotaxic Coordinates. Academic, New York, NY.
Somogyi P, Bolam JP, Totterdell S and Smith AD (1981) Monosynaptic input from the nucleus accumbens-ventral striatum region to retrogradely labelled nigrostriatal neurons. Brain Res 217: 245–263.
West AR, Floresco SB, Charara A, Rosenkranz JA and Grace AA (2003) Electrophysiological interactions between striatal glutamatergic and dopaminergic systems. Ann NY Acad Sci 1003: 53–57.
Wright CI, Beijer AV and Groenewegen HJ (1996) Basal amygdaloid complex afferents to the rat nucleus accumbens are compartmentally organized. J Neurosci 16: 1877–1893.
Acknowledgments
Supported by a Dutch Medical Research Council program grant (NWO-ZonMW 903-42-092) and a NWO-ZonMW/INSERM travel grant (910-48-029).
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van Dongen, Y.C., Kolomiets, B.P., Groenewegen, H.J., Thierry, AM., Deniau, JM. (2009). A Subpopulation of Mesencephalic Dopamine Neurons Interfaces the Shell of Nucleus Accumbens and the Dorsolateral Striatum in Rats. In: Groenewegen, H., Voorn, P., Berendse, H., Mulder, A., Cools, A. (eds) The Basal Ganglia IX. Advances in Behavioral Biology, vol 58. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0340-2_10
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DOI: https://doi.org/10.1007/978-1-4419-0340-2_10
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