Abstract
A major approach of our laboratory has been the use of electrophysiological recording techniques to investigate the effects on the electrical activity of neurons of the basal forebrain of electrical stimulation of the amygdala and hippocampus. As shown in Fig. 1, highly reliable electrophysiological responses to inputs from these two prominent limbic structures are excitation of accumbens neurons and inhibition of subpallidal neurons. Since the ventral striatum receives strong mesolimbic dopamine projections we have also investigated the effects on these electrophysiological responses of dopamine, either applied exogenously to accumbens neurons by micro-iontophoresis, or released endogenously from electrical stimulation of the ventral tegmental area of the midbrain. Dopamine has been shown to modulate the excitatory responses of accumbens neurons to stimulation of the amygdala and hippocampus and, in turn, to influence the electrophysiological responses of subpallidal neurons. The functional implications for limbic-motor integration of the interaction of dopamine inputs to the accumbens with inputs from amygdala and hippocampus have been investigated in complementary behavioral experiments. Before considering the results of our research in more detail some background is needed.
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References
Alheid, G.F. and Heimer, L., 1988, New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid and corticopetal components of substantia innominata. Neurosci., 27: 1–39.
Austin, M.C. and Kalivas, P.W., 1987, Modulation of GABAergic function on the substantia innominata by the mesolimbic dopamine system. Proc. Soc. Neurosci., 13: 958, Abstr. 264.16.
Austin, M.C. and Kalivas, P.W., 1990, Enkephalinergic and GABAergic modulation of motor activity in the ventral pallidum. J. Pharmacol. Exp. Therap. 252: 1370–1377.
Beckstead, R.M., Domesick, V. B. and Nauta, W.J.H., 1979, Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res., 175: 191–217.
Bjursten, L.-M., Norrsell, K., and Norrsell, U., 1976, Behavioral repertory of cats without cerebral cortex from infancy. Exp. Brain Res. 25: 115–130.
Blaker, W.D., 1985, GABAergic control of the cholinergic projections to the frontal cortex is not tonic. Brain Res., 325: 389–390.
Boldry, R.C. and Uretsky, N.J., 1988, The importance of dopaminergic neurotransmission in the hypermotility response produced by the administration of N-methyl-D-aspartic acid into the nucleus accumbens. Neuropharmacol., 27: 569–577.
Brashear, H.R., Zaborszky, L. and Heimer, L., 1986, Distribution of GABAergic and cholinergic neurons in the rat diagonal band. Neurosci., 17: 439–451.
Brudzynski, S.M. and Mogenson, G.J. 1985, Assocation of the mesencephalic locomotor region with locomotor region with locomotor activity induced by injections of amphetamine into the nucleus accumbens. Brain Res., 334: 77–84.
Brudzynski, S.M. and Mogenson, G.J. 1986, Inhibition of amphetamine-induced locomotor activity by injection of carbachol into the anterior hypothalamic/preoptic area: pharmacological and electrophysiological studies in the rat. Brain Res. 376: 47–56.
Cador, M., Robbins, T.W. and Everitt, B.J. 1989, Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum. Neurosci., 30: 77–86.
Christie, M.J., James, L.B. and Beart, P.M., 1985, An excitatory amino acid projection from the medial prefrontal cortex to the anterior part of nucleus accumbens in the rat. J. Neurochem., 45: 477–482.
Christie, M.J., Summers, R.J., Stephenson, J.A., Cook, C.J. and Beart, P.M., 1987, Excitatory amino acid projections to the nucleus accumbens septi in the rat: a retrograde transport study utilizing D-[3H] aspartate and [3H]GABA. Neurosci., 22: 425–439.
Coyle, J.T., Price, D.L. and DeLong, M.R., 1983, Alzheimer’s disease: a disorder of cortical cholinergic innervation. Science, 219: 1184–1190.
Dahlstrom, A. and Fuxe, K., 1964, Evidence for the existence of monoamines in the central nervous system. I. Determination of monoamines in the cell bodies of brainstem neurones. Acta Physiol. Scand. Suppl., 232: 1–25.
Divac, I., 1975, Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Res., 93:385–398.
Fuster, J.M., 1989, “The Frontal Cortex”, 2nd Edition, Raven Press, New York.
Garcia-Rill, E., Skinner, R.D. and Fitzgerald, J.A., 1983, Activity in the mesencephalic locomotor region during locomotion. Exp. Neurol. 82: 609–622.
Garcia-Rill, E., 1986, The basal ganglia and the locomotor regions. Brain Res. Rev. 11:47–63.
Grillner, S., 1985, Neurobiological bases of rhythmic acts in vertebrates. Science, 228: 143–149.
Groenewegen, H.J., 1988, Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neurosci., 24: 379–431.
Groenewegen, H.J., Vermeulen-Van der Zee, E., te Kortschot, A. and Witter, M.P., 1987, Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoglutinin. Neurosci., 23: 103–120.
Grove, E.A., 1988a, Neural associations of the substantia innominata in the rat: afferent connections. J.Comp.Neurol . 277: 315–346.
Grove , E.A., 1988b, Efferent connections of the substantia innominata in the rat. J.Comp.Neurol. 277: 347–164.
Haber, S.N., 1987, Anatomical relationship between the basal ganglia and the basal nucleus of Meynert in human and monkey forebrain. Proc. Natl. Acad. Sei. USA, 84: 1408–1412.
Haber, S.N. and Nauta, W.J.H., 1983, Ramifications of the globus pallidus in the rat as indicated by patterns of immunohistochemistry. Neurosci., 9: 245–260.
Haber, S.N., Groenewegen, H.J., Grove, E.A. and Nauta, W.J.H., 1985, Efferent connections of the ventral pallidum: evidence of a dual striato pallidofugal pathway. J.Comp.Neurol., 235: 322–335.
Heimer, L. and Wilson, R.D., 1975, The subsortical projections of the allocortex: similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. In: “Golgi Centennial Symposium”, M. Santini, ed.. Raven Press, N. Y., pp.177–193.
Heimer, L., Switzer, R.D. and Van Hoesen, G.W., 1982, Ventral striatum and ventral pallidum: Components of the motor system? Trends in Neurosci., 5: 83–87.
Hess, W.R., 1954, “Das Zwischenhirn” 2nd Ed. Schwabe, Basel.
Hill, J.M., 1985, Iron concentration reduced in ventral pallidum, globus pallidus, and substantia nigra by GABA-transaminase inhibitor, Gamma-vinyl GABA. BrainRes., 342: 18–25.
Hill, J.M. and Switzer, R.C., 1984, The regional distribution and cellular localization of iron in the rat brain. Neurosci., 11: 595–603.
Isaacson, R.L., 1982, “Limbic System” 2nd Ed., Plenum, New York.
Jones, D.L. and Mogenson, G.J., 1980a, Nucleus accumbens to globus GABA projection: electrophysiological and iontophoretic investigations. Brain Res., 188: 93–105.
Jones, D.L. and Mogenson, G.J., 1980b, Nucleus accumbens to globus pallidus GABA projection subserving ambulatory activity. Am. J. Physiol., 238: 65–69.
Jones, D.L., Mogenson, G.J. and Wu, M., 1981, Injections of dopaminergic, cholinergic, serotoninergic and GABAergic drugs into the nucleus accumbens: effects on locomotor activity in the rat. Neuropharmacol., 20: 29–37.
Kalivas, P.W., 1990, This book.
Kelley, A.E. and Domesick, V.B., 1982, The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde and retrograde horseradish peroxidase study. Neurosci., 7: 2321–2335.
Kelley, A.E., Domesick, V.B. and Nauta, W.J.H., 1982, The amygdalostriatal projection in the rat— an anatomical study by anterograde and retrograde tracing methods. Neurosci., 7: 615–630.
Kelley, A.E., and Stinus, L., 1985, Disappearance of hoarding behaviour after 6-hydroxydopamine lesions of the mesolimbic dopamine neurones and its reinstatement with L-dopa. Behav. Neurosci., 99: 531–545.
Kolb, B., 1974, Prefrontal lesions alter eating and hoarding behaviour in rats. Physiol. Behav., 12: 507–511.
Koob, G.F., 1990, This book.
Krettek, J.E. and Price, J.L., 1978, Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J.Comp.Neurol., 178: 225–254.
Lehmann, J., Nagy, J.I., Atmadja, S. and Fibiger, H.C., 1980, The nucleus basalis magnocellularis: the origin of a cholinergic projection to the neocortex of the rat. Neurosci., 5: 1161–1174.
Markowitsch, J.J., 1982, Thalamic mediodorsal nucleus and memory: a critical evaluation of studies in animals and man. Neurosci. Biobehav. Rev., 6: 351–381.
Mesulam, M.M., Mufson, E.J., Wainer, B.H. and Levey, A.I., 1983, Central cholinergic pathways in the rat, an overview based on an alternative nomenclature (Chl-Ch6). Neuroscience, 10: 1185–1201.
Mogenson, G.J., 1987, Limbic-motor integration. Prog. Psychobiol. Physiol. Psychol., 12: 117–170.
Mogenson, G.J. and Nielsen, M., 1983, Evidence that an accumbens to subpallidal GABAergic projection contributes to locomotor activity. Brain Res. Bull., 11: 309–314.
Mogenson, G.J. and Nielsen, M., 1984a, A study of the contribution of hippocampal-accumbens-subpallidal projections to locomotor activity. Behav. Neural. Biol., 42: 38–51.
Mogenson, G.J. and Nielsen, M., 1984b, Neurochemical evidence to suggest that the nucleus accumbens and subpallidal regions contribute to exploratory locomotion. Behav. Neural Biol., 42: 52–60.
Mogenson, G.J. and Wu, M., 1986, Subpallidal projections to the mesencephalic locomotor region investigated with a combination of behavioral and electrophysiological recording techniques. Brain Res. Bull., 16: 383–390.
Mogenson, G.J. and Wu, M., 1988a, Differential effects on locomotor activity of injections of procaine into mediodorsal thalamus and pedun-culopontine nucleus. Brain Res. Bull., 20: 241–246.
Mogenson, G.J. and Wu, M., 1988, Disruption of food hoarding by injections of procaine into mediodorsal thalamus, GABA into subpallidal region and haloperidol into the accumbens. Brain Res. Bull., 20: 247–251.
Mogenson, G.J. and Yim, C.Y., 1981, Electrophysiological and neurophar-macological-behavioral studies of the nucleus accumbens: implications for its role as a limbic-motor interface. In “The Neurobiology of the Nucleus Accumbens”, R. B. Chronister and J. F. DeFrance, eds., Haer Institute, New Brunswick, pp. 210–229.
Mogenson, G.J., Jones, D.L. and Yim, C.Y., 1980, From motivation to action: Functional interface between the limbic system and the motor system. Prog. Neurobiol., 14: 69–97.
Mogenson, G.J., Swanson, L.W. and Wu, M., 1983, Neural projections from nucleus accumbens to globus pallidus, substantia innominata, and lateral preoptic-lateral hypothalamic area: an anatomical and electrophysiological investigation in the rat. J. Neurosci., 3: 189–202.
Mogenson, G.J., Wu, M. and Manchanda, S.K., 1979, Locomotor activity initiated by microinfusions of Picrotoxin into the ventral tegmental area. Brain Res., 161: 311–319.
Mogenson, G.J., Yang, C.R. and Yim, C.Y., 1988, Influence of dopamine on limbic inputs to the nucleus accumbens. Ann. N. Y. Acad.Sci., 537: 86–100.
Mogenson, G.J., Ciriello, J., Garland, J. and Wu, M., 1987, Ventral pallidum projections to mediodorsal nucleus of the thalamus: an anatomical and electrophysiological investigation in the rat. Brain Res., 404: 221–230.
Moon-Edley, S. and Graybiel, A.M., 1983, The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus pars compacta. J.Comp.Neurol., 217: 187–215.
Nauta, W.J.H., Smith, G.P., Faull, R.L.M. and Domesick, V.B., 1978, Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neurosci., 3: 385–401.
O’Keefe, J. and Nadel, L., 1978, “The Hippocampus as a Cognitive Map” Clarendon Press, Oxford.
Onteniente, B., Simon, H., Taghzouti, K., Geffard, M., Le Moal, M. and Galas, A., 1987, Dopamine-GABA interactions in the nucleus accumbens and lateral septum of the rat. Brain Res., 421: 391–396.
Patel, S. and Slater, P., 1988, Effects of GABA compounds injected into the subpallidal regions of rat brain on nucleus accumbens evoked hyperactivity. Behav. Neurosci., 102: 596–600.
Paxinos, G. and Watson, C., 1986, “The Rat Brain in Stereotaxic Coordinates”, 2nd edition, Academic Press, N. Y.
Pickel, V.M., Towle, A.C., Joh, T.H., and Chan, J., 1988, GABA in the medial rat nucleus accumbens: ultrastruetural localization in neurones receiving monosynaptic input from catecholaminergic afferents. J.Comp.Neurol., 272: 1–14.
Pijnenberg, A.J.J, and van Rossum, J., 1973, Stimulation of locomotor activity following injection of dopamine into the nucleus accumbens. J.Pharm.Pharmacol., 25: 1003–1005.
Richardson, R.T. and DeLong, M.R., 1988, A reappraisal of the functions of the nucleus basalis of Meynert. Trends in Neurosci., 11: 265–267.
Schacter, G.B., Yang, C.R., Innis, N.K. and Mogenson, G.J., 1989, The role of the hippocampal-nucleus accumbens pathway in radial-arm maze performance. Brain Res., 494: 339–349.
Scheel-Kruger, J., 1986, Dopamine-GABA interactions: evidence that GABA transmits, modulates and mediates dopaminergic functions in the basal ganglia and the limbic system. Acta Neurol. Scanda Suppl., 107: 1–54.
Semba, K. and Fibiger, H.C., 1988, Time of origin of cholinergic neurons in the rat basal forebrain. J.Comp.Neurol., 269: 87–95.
Shefchyk, D.J., Jell, R.M. and Jordan, L.M., 1984, Reversible cooling of the brainstem reveals areas required for mesencephalic locomotor region evoked treadmill locomotion. Exp. Brain Res., 56: 257–262.
Shik, M.L., Severin, F.V. and Orlovsky, G.N., 1966, Control of walking and running by means of electrical stimulation of the mid-brain. Biophysics 11: 756–765.
Skinner, R.D. and Garcia-Rill E., 1984, The mesencephalic locomotor region (MLR) in the rat. Brain Res. 323: 385–389.
Sugimoto, T. and Mizuno, N., 1987, Neurotensin in projection neurons of the striatum and nucleus accumbens, with reference to co-existence with enkephalin and GABA: immunohistochemical study in the cat. J.Comp.Neurol., 257: 383–395.
Swanson, L.W., Mogenson, G.J., Gerfen, C.R. and Robinson, P., 1984, Evidence for a projection from the lateral preoptic area and substantia innominata to the “mesencephalic locomotor region” in the rat. Brain Res., 295: 161–178.
Swerdlow, N.R. and Koob, G.F., 1987a, Dopamine, schizophrenia, mania, and depression: toward a unified hypothesis of cortical-striato-pallido-thalamic function. Brain Behav.Sci., 10: 197–245.
Swerdlow, N.R. and Koob, G.F., 1987b, Lesions of the dorsomedial nucleus of the thalamus, medial prefrontal cortex and pedunculopontine nucleus: effects on locomotor activity mediated by nucleus accumbens-ventral pallidal circuitry. Brain Res., 412: 233–243.
Swerdlow, N.R., Swanson, L.W. and Koob, G.F., 1984, Electrolytic lesions of the substantia innominata and lateral preoptic area attenuate the ‘supersensitive’ locomotor response to apomorphine resulting from denervation of the nucleus accumbens. Brain Res. 306: 141–148.
Switzer, R.C., Hill, J. and Heimer, L., 1982, The globus pallidus and its rostroventral extension into the olfactory tubercle of the rat: a cyto- and chemoarchitectural study. Neurosci., 7: 1891–1904.
Totterdell, S. and Smith, A.D., 1989, Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J. Chem. Neuroanat., 2: 285–298.
Uchimura, N. and North, R.A., 1990, Muscarine reduces inwardly rectifying potassium conductance in rat nucleus accumbens neurones. J. Physiol. (London) 422: 369–380.
Vanderwolf, C.H., 1971, Limbic-diencephalic mechanisms of voluntary movement. Psychol. Rev., 78: 83–113.
Victor, M., Adams, R.D. and Collins, G.H., 1971, The Wernicke-Korsakoff Syndrome. Oxford, Blackwell, 1971.
Vives, F. and Mogenson, G.J., 1985, Electrophysiological evidence that mediodorsal nucleus of the thalamus is a relay of the pathway between the ventral pallidum and the medial prefrontal cortex in the rat. Brain Res., 344: 329–337.
Vives, F. and Mogenson, G.J., 1986, Electrophysiological study of the effects of Di and D2 dopamine antagonists on the interaction of converging inputs from the sensory-motor cortex and substantia nigra neurons in the rat. Neurosci., 17: 349–359.
Walaas, I. and Fonnum, F., 1979, The distribution and origin of glutamate decarboxylase and choline acetyltransferase in ventral pallidum and other basal forebrain regions. Brain Res., 177: 325–336.
Wenk, G.J., 1984, Pharmacological manipulations of the substantia innominata — cortico cholinergic pathway. Neurosci. Lett., 51: 99–103.
White, F.J. and Wang, R.X., 1985, Electrophysiological evidence for the existence of both D1 and D2 dopamine receptors in the rat nucleus accumbens. J. Neurosci., 6: 274–280.
Wood, P.L., 1986, Pharmacological evaluation of GABAergic and glutamatergic inputs to the nucleus basalis — cortico and the septal — hippocampal cholinergic projections. Canadn. J. Physiol. Pharmacol., 64: 325–328.
Wood, P.L. and Richard, J., 1982, GABAergic regulation of the substantia innominata — cortico cholinergic pathway. Neuropharmacol., 21: 969–972.
Yang, C.R. and Mogenson, G.J., 1984, Electrophysiological responses of neurones in the nucleus accumbens to hippocampal stimulation and the attenuation of the excitatory responses by mesolimbic dopaminergic system. Brain Res., 324: 69–84.
Yang, C.R. and Mogenson, G.J., 1985, An electrophysiological study of the neural projections from the hippocampus to the ventral pallidum and the subpallidal areas by way of the nucleus accumbens. Neurosci., 15: 1015–1024.
Yang, C.R. and Mogenson, G.J., 1986, Dopamine enhances terminal excitability of hippocampal-accumbens neurones via D2 receptor: role of dopamine in presynaptic inhibition. J. Neurosci., 6: 2470–2478.
Yang, C.R. and Mogenson, G.J., 1987, Hippocampal signal transmission to the pedunculopontine nucleus and its regulation by dopamine D2 receptors in the nucleus accumbens: an electrophysiological and behavioral study. Neurosci., 23: 1041–1055.
Yang, C.R. and Mogenson, G.J., 1989, Ventral pallidal responses to dopamine receptor stimulation in the nucleus accumbens. Brain Res., 489: 237–246.
Yang, C.R. and Mogenson, G.J., 1990, Dopaminergic modulation of cholinergic responses in rat medial prefrontal cortex. Brain Res., (in press).
Yim, C.Y., 1990, This book.
Yim, C.Y. and Mogenson, G.J., 1982, Responses of nucleus accumbens neurones to amygdala stimulation and its modification by dopamine. Brain Res., 239: 401–415.
Yim, C.Y. and Mogenson, G.J., 1989, Low doses of accumbens dopamine modulate amygdala suppression of spontaneous exploratory activity in rats. Brain Res., 477: 202–210.
Young, W.S., Alheid, G.F. and Heimer, L., 1984, The ventral pallidal projection to the mediodorsal thalamus: a study with fluorescent retrograde tracers and immunohistofluorescence. J. Neurosci. 4:1626–1638.
Zaborszky, L., Leranth, C. and Heimer, L., 1984, Ultrastruetural evidenceof amygdalofugal axons terminating on cholinergic cells of the rostral forebrain. Neurosci. Lett., 52: 219–225.
Zaborszky, L., Heimer, L., Eckenstein, F. and Leranth, C., 1986, GABAergic input to cholinergic basal forebrain neurones: an untrastructural study using retrograde tracing of HRP and double Immunolabelling. J.Comp.Neurol., 250: 282–295.
Zahm, D.S. and Heimer, L., 1988, The ventral striatopallidal parts of the basal ganglia in the rat: I. Neurochemical compartmentation as reflected by the distributions of neurotensin and substance P immunoreactivity. J.Comp.Neurol., 272: 516–535.
Zahm, D.S., Zaborsky, L., Alones, V.E. and Heimer, L., 1985, Evidence for the coexistence of glutamate decarboxylase and met-enkephalin immunoreactivities in axon terminals of rat ventral pallidum. Brain Res., 325: 317–321.
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Mogenson, G.J., Yang, C.R. (1991). The Contribution of Basal Forebrain to Limbic — Motor Integration and the Mediation of Motivation to Action. In: Napier, T.C., Kalivas, P.W., Hanin, I. (eds) The Basal Forebrain. Advances in Experimental Medicine and Biology, vol 295. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-0145-6_14
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