Subpallidal outputs to the nucleus accumbens and the ventral tegmental area: anatomical and electrophysiological studies

The goal of this study was to investigate the functional organization of the subpallidal-->accumbens direct and indirect feedback loops by both anatomical and electrophysiological methods. The results of the dextran-conjugated rhodamine injections into the subpallidal area has shown three distinct projections: (1) a substantial pathway from the subpallidal area to the ventral tegmental area, (2) a more diffuse rostral projection from the subpallidal area to the core area of the nucleus accumbens, and (3) a sparse pathway projecting rostrodorsally from the subpallidal area toward the thalamic regions. Electrical or chemical stimulation of the subpallidal region, which was studied by the axonal tracer, evoked inhibitory responses in the majority (60 and 80%, respectively) of the accumbens and ventral tegmental area neurons in a standard extracellular recording study. Less than 1/3 of the accumbens or ventral tegmental area cells showed an increase in the mean firing rate. The majority (77.5%) of all responded neurons had a latency of less than 10 ms. Furthermore, injection of glutamate into the subpallidal area not only altered the firing pattern of the accumbens neurons, but also attenuated their excitatory responses elicited by the electrical stimulation of the ventral subiculum. Our results indicate that the subpallidal area plays a predominantly inhibitory role in the ventral tegmental area-accumbens-subpallidal circuitry, presumably by its GABAergic projections, and may also modulate subicular input into the nucleus accumbens.

[1]  D. Nance,et al.  Fluorescent dextrans as sensitive anterograde neuroanatomical tracers: Applications and pitfalls , 1990, Brain Research Bulletin.

[2]  P. Voorn,et al.  The dopaminergic innervation of the ventral striatum in the rat: A light‐ and electron‐microscopical study with antibodies against dopamine , 1986, The Journal of comparative neurology.

[3]  G. Mogenson,et al.  Effect of picrotoxin and nipecotic acid on inhibitory response of dopaminergic neurons in the ventral tegmental area to stimulation of the nucleus accumbens , 1980, Brain Research.

[4]  P. Willner,et al.  The Mesolimbic Dopamine System: From Motivation to Action An International Workshop Malta September 25–29, 1989 , 1989, Psychobiology.

[5]  D. S. Zahm,et al.  Specificity in the projection patterns of accumbal core and shell in the rat , 1991, Neuroscience.

[6]  L. Swanson,et al.  Anatomical and electrophysiological evidence for a projection from the medial preoptic area to the ‘mesencephalic and subthalamic locomotor regions’ in the rat , 1987, Brain Research.

[7]  P. Kalivas,et al.  Dopaminergic involvement in locomotion elicited from the ventral pallidum/substantia innominata , 1991, Brain Research.

[8]  Mitsuo Yoshida,et al.  Activation of mesencephalic dopamine neurons by chemical stimulation of the nucleus tegmenti pedunculopontinus pars compacta , 1988, Brain Research.

[9]  G. Mogenson,et al.  Decrease of locomotor activity by injections of carbachol into the anterior hypothalamic/preoptic area of the rat , 1986, Brain Research.

[10]  L. W. Swanson,et al.  Neural mechanisms for the functional coupling of autonomic, endocrine and somatomotor responses in adaptive behavior , 1981, Brain Research Reviews.

[11]  A comparison of the effects of electrical stimulation of the amygdala and hippocampus on subpallidal output neurons to the pedunculopontine nucleus , 1989, Brain Research.

[12]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[13]  S. Henriksen,et al.  Electrophysiological evidence for reciprocal connectivity between the nucleus accumbens septi and ventral pallidal region , 1992, Brain Research.

[14]  P. Kalivas,et al.  A topographically organized gamma‐aminobutyric acid projection from the ventral pallidum to the nucleus accumbens in the rat , 1994, The Journal of comparative neurology.

[15]  N. Swerdlow,et al.  The neural substrates of apomorphine-stimulated locomotor activity following denervation of the nucleus accumbens. , 1984, Life sciences.

[16]  L. Heimer,et al.  In vivo anterograde and retrograde axonal trnasport of the fluoresecent rhodamine-dextran-amine, Fluor-Ruby, within the CNS , 1990, Brain Research.

[17]  A M Graybiel,et al.  Fiber connections of the basal ganglia. , 1979, Progress in brain research.

[18]  G. Mogenson,et al.  Nucleus accumbens to globus pallidus GABA projection subserving ambulatory activity. , 1980, The American journal of physiology.

[19]  D. S. Zahm,et al.  Two transpallidal pathways originating in the rat nucleus accumbens , 1990, The Journal of comparative neurology.

[20]  T. Joh,et al.  Gamma‐aminobutyric acid in the medial rat nucleus accumbens: Ultrastructural localization in neurons receiving monosynaptic input from catecholaminergic afferents , 1988, The Journal of comparative neurology.

[21]  P. Kalivas,et al.  GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area , 1993, Neuroscience.

[22]  H. Groenewegen,et al.  Organization of the efferent projections of the nucleus accumbens to pallidal, hypothalamic, and mesencephalic structures: A tracing and immunohistochemical study in the cat , 1984, The Journal of comparative neurology.

[23]  P. Kalivas,et al.  Amphetamine lowers extracellular GABA concentration in the ventral pallidum , 1990, Brain Research.

[24]  R. Oades,et al.  Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity , 1987, Brain Research Reviews.

[25]  G. P. Smith,et al.  Efferent connections and nigral afferents of the nucleus accumbens septi in the rat , 1978, Neuroscience.

[26]  S. Haber,et al.  Organization of the output of the ventral striatopallidal system in the rat: Ventral pallidal efferents , 1993, Neuroscience.

[27]  D. S. Zahm,et al.  Evidence for the coexistence of glutamate decar☐ylase and Met-enkephalin immunoreactivities in axon terminals of rat ventral pallidum , 1985, Brain Research.

[28]  G. Mogenson,et al.  Limbic-motor integration , 1987 .

[29]  D. S. Zahm,et al.  The patterns of afferent innervation of the core and shell in the “Accumbens” part of the rat ventral striatum: Immunohistochemical detection of retrogradely transported fluoro‐gold , 1993, The Journal of comparative neurology.

[30]  W. Nauta,et al.  Efferent connections of the ventral pallidum: Evidence of a dual striato pallidofugal pathway , 1985, The Journal of comparative neurology.

[31]  L. W. Swanson,et al.  Evidence for a projection from the lateral preoptic area and substantia innominata to the ‘mesencephalic locomotor region’ in the rat , 1984, Brain Research.

[32]  G. Mogenson,et al.  Subpallidal projections to the mesencephalic locomotor region investigated with a combination of behavioral and electrophysiological recording techniques , 1986, Brain Research Bulletin.

[33]  P. Kalivas,et al.  The role of mesoaccumbens-pallidal circuitry in novelty-induced behavioral activation , 1995, Neuroscience.

[34]  G. Mogenson,et al.  Ventral pallidum projections to mediodorsal nucleus of the thalamus: an anatomical and electrophysiological investigation in the rat , 1987, Brain Research.

[35]  W. Nauta,et al.  THE ANATOMY OF THE EXTRAPYRAMIDAL SYSTEM , 1979 .

[36]  D. Munoz,et al.  Chromogranin A applied to the nucleus accumbens decreases locomotor activity induced by activation of the mesolimbic dopaminergic system in the rat , 1994, Brain Research Bulletin.

[37]  P. Strange Dopaminergic Ergot derivatives and motor functions: Edited by K. Fuxe and D. B. Calne. Pp. 447. Pergamon Press, Oxford. 1979. £27.50 , 1980 .

[38]  P. Bailey The neurobiology of the nucleus accumbens R. B. Chronister and J. F. de France (Eds). Haer Institute for Electrophysiological Research (1981). 388 pp , 1982, Neuroscience.

[39]  G. Mogenson,et al.  An electrophysiological study of the neural projections from the hippocampus to the ventral pallidum and the subpallidal areas by way of the nucleus accumbens , 1985, Neuroscience.

[40]  G. Mogenson,et al.  Hippocampal signal transmission to the pedunculopontine nucleus and its regulation by dopamine D2 receptors in the nucleus accumbens: An electrophysiological and behavioural study , 1987, Neuroscience.

[41]  G. Mogenson,et al.  Evidence that an accumbens to subpallidal GABAergic projection contributes to locomotor activity , 1983, Brain Research Bulletin.

[42]  G. Mogenson,et al.  Decreases in rat locomotor activity as a result of changes in synaptic transmission to neurons within the mesencephalic locomotor region. , 1993, Canadian journal of physiology and pharmacology.

[43]  O. Phillipson,et al.  The topographic order of inputs to nucleus accumbens in the rat , 1985, Neuroscience.

[44]  G. Mogenson,et al.  Nucleus accumbens to globus pallidus GABA projection: Electrophysiological and iontophoretic investigations , 1980, Brain Research.

[45]  G. Mogenson,et al.  An electrophysiological study of inputs to neurons of the ventral tegmental area from the nucleus accumbens and medial preoptic-anterior hypothalamic areas , 1980, Brain Research.

[46]  V. Reggie Edgerton,et al.  Neurobiological basis of human locomotion , 1991 .