Origins of postsynaptic potentials evoked in identified rat neostriatal neurons by stimulation in substantia nigra

SummaryResponses of striatal neurons to stimulation in substantia nigra were recorded intracellularly in intact rats and after acute or chronic unilateral lesions of cerebral cortex or after combined cortical lesions and unilateral thalamic transections. Spiny striatal efferent neurons were identified by intracellular injection of horseradish peroxidase. In intact animals substantia nigra stimulation evoked a complex response with both excitatory and inhibitory phases. Acute unilateral decortication abolished the inhibitory phase of the response and reduced the amplitude of the initial EPSP. Thus, part of the excitatory phase and most or all of the inhibitory phase of the response result from polysynaptic routes to striatum involving cerebral cortex. The remaining EPSP observed in acute decorticate animals exhibited two components distinguished on the basis of their time courses. The latter of these was abolished by thalamic transections. The earlier component was shown to be a monosynaptic EPSP evoked by axon collaterals of cortical efferent neurons projecting to brainstem and was not observed in animals subjected to chronic decortication. After removal of all of these non-nigral response components a small long latency EPSP could be evoked by nigral stimulation. This EPSP is probably due to activation of dopaminergic nigro-striatal axons.

[1]  J. Deniau,et al.  Electrophysiological properties of identified output neurons of the rat substantia nigra (pars compacta and pars reticulata): Evidences for the existence of branched neurons , 1978, Experimental Brain Research.

[2]  K. Endo,et al.  Short latency EPSPs of pyramidal tract cells evoked by stimulation of the centrum medianum-parafascicular complex and the nucleus ventralis anterior of the thalamus , 1976, Brain Research.

[3]  M. Sugimori,et al.  Convergence of excitatory synaptic inputs to caudate spiny neurons , 1977, Brain Research.

[4]  G. Aghajanian,et al.  Antidromic identification of dopaminergic and other output neurons of the rat substantia nigra , 1978, Brain Research.

[5]  S. L. Liles Single-unit responses of caudate neurons to stimulation of frontal cortex, substantia nigra and entopeduncular nucleus in cats. , 1974, Journal of neurophysiology.

[6]  C. Fox,et al.  The spiny neurons in the primate striatum: a Golgi and electron microscopic study. , 1972, Journal fur Hirnforschung.

[7]  K. Jinnai,et al.  Neurons of the motor cortex projecting commonly on the caudate nucleus and the lower brain stem in the cat , 1979, Neuroscience Letters.

[8]  H. T. Chang,et al.  Anatomy and physiology of substantia nigra and retrorubral neurons studied by extra- and intracellular recording and by horseradish peroxidase labeling , 1981, Neuroscience.

[9]  J. Hedreen Corticostriatal cells identified by the peroxidase method , 1977, Neuroscience Letters.

[10]  P. Groves,et al.  Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular inject of horseradish peroxidase. , 1980, The Journal of comparative neurology.

[11]  G. Bernardi,et al.  Intracellular responses of caudate neurons to temporally and spatially combined stimuli. , 1973, Experimental neurology.

[12]  Charles J. Wilson,et al.  A simple and rapid section embedding technique for sequential light and electron microscopic examination of individually stained central neurons , 1979, Journal of Neuroscience Methods.

[13]  C. P. Vandermaelen,et al.  Excitation of caudate-putamen neurons following stimulation of the dorsal raphe nucleus in the rat , 1979, Brain Research.

[14]  E. Cherubini,et al.  Caudate neuronal responses evoked by cortical stimulation: contribution of an indirect corticothalamic pathway , 1979, Brain Research.

[15]  W. Vogel,et al.  Phenylethanolamine-N-methyltransferase activity in various areas of human brain, tissues and fluids , 1976, Brain Research.

[16]  R. Hassler,et al.  Locally evoked potentials in slices of rat neostriatum: A tool for the investigation of intrinsic excitatory processes , 1979, Experimental Brain Research.

[17]  R. Porter,et al.  Cells of origin and terminal distrubution of corticostriatal fibers arising in the sensory‐motor cortex of monkeys , 1977, The Journal of comparative neurology.

[18]  Charles J. Wilson,et al.  Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: A study employing intracellular injection of horseradish peroxidase , 1980 .

[19]  Webster Ke Cortico-striate interrelations in the albino rat. , 1961 .

[20]  G. Bernardi,et al.  Intracellular responses of caudate neurons to brain stem stimulation. , 1970, Brain research.

[21]  T. Pasik,et al.  A Golgi study of neuronal types in the neostriatum of monkeys , 1976, Brain Research.

[22]  D. Albe-Fessard,et al.  A study of an ascending nigro-caudate pathway. , 1972, Electroencephalography and clinical neurophysiology.

[23]  P. Somogyi,et al.  Projection of neostriatal spiny neurons to the substantia nigra. Application of a combined golgi-staining and horse-radish peroxidase transport procedure at both light and electron microscopic levels , 1979, Brain Research.

[24]  Y. Katayama,et al.  Slow rhythmic activity of caudate neurons in the cat: Statistical analysis of caudate neuronal spike trains , 1980, Experimental Neurology.

[25]  J. Donoghue,et al.  A collateral pathway to the neostriatum from corticofugal neurons of the rat sensory‐motor cortex: An intracellular HRP study , 1981, The Journal of comparative neurology.

[26]  J. A. González-Vegas Antagonism of dopamine-mediated inhibition in the nigro-striatal pathway: a mode of action of some catatonia-inducing drugs. , 1974, Brain research.

[27]  W. Precht,et al.  Nigro-caudate and caudato-nigral relationship: an electrophysiological study , 1975, Brain Research.

[28]  A. Dray,et al.  Caudate stimulation and substantia nigra activity in the rat. , 1976, The Journal of physiology.

[29]  I. Kanazawa,et al.  Electrophysiological evidence for the existence of excitatory fibres in the caudato-nigral pathway in the cat , 1980, Neuroscience Letters.

[30]  Robert Miller,et al.  Distribution and properties of commissural and other neurons in cat sensorimotor cortex , 1975, The Journal of comparative neurology.

[31]  T. Powell,et al.  The structure of the caudate nucleus of the cat: light and electron microscopy. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[32]  H. Burton,et al.  Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates , 1976, The Journal of comparative neurology.

[33]  G. Somjen,et al.  Interactions of nigrostriate synaptic transmission, iontophoretic O-methylated phenethylamines, dopamine, apomorphine and acetylcholine , 1976, Brain Research.

[34]  A. Malliani,et al.  I. Synaptic potentials and discharge characteristics of caudate neurons activated by thalamic stimulation. , 1967, Brain research.

[35]  J. D. Kocsis,et al.  Dual excitatory inputs to caudate spiny neurons from substantia nigra stimulation , 1977, Brain Research.

[36]  C. G. Phillips,et al.  Corticospinal neurones. Their role in movement. , 1977, Monographs of the Physiological Society.

[37]  S. T. Kitai,et al.  Single neostriatal efferent axons in the globus pallidus: a light and electron microscopic study. , 1981, Science.

[38]  H. Mclennan,et al.  Mechanisms of excitation and inhibition in the nigrostriatal system , 1977, Brain Research.

[39]  C. P. Vandermaelen,et al.  Intracellular analysis of synaptic potentials in rat neostriatum following stimulation of the cerebral cortex, thalamus, and substantia nigra , 1980, Brain Research Bulletin.

[40]  K. Endo,et al.  The distribution and pattern of axon branching of pyramidal tract cells. , 1973, Brain research.

[41]  N. A. Buchwald,et al.  Intracellular responses of caudate output neurons to orthodromic stimulation , 1975, Brain Research.

[42]  J. Féger,et al.  The unitary activity of the substantia nigra following stimulation of the striatum in the awake monkey , 1975, Brain Research.

[43]  J D Connor,et al.  Caudate nucleus neurones: correlation of the effects of substantia nigra stimulation with iontophoretic dopamine , 1970, The Journal of physiology.

[44]  D. Purpura,et al.  Electrophysiological analysis of reciprocal caudato-nigral relations. , 1967, Brain research.

[45]  Mnh,et al.  Histologie du Système Nerveux de Lʼhomme et des Vertébrés , 1998 .

[46]  J. W. Lighthall,et al.  Inhibition in slices of rat neostriatum , 1981, Brain Research.

[47]  S. T. Kitai,et al.  Medium spiny neuron projection from the rat striatum: An intracellular horseradish peroxidase study , 1980, Brain Research.

[48]  K. Jinnai,et al.  Common projection of the motor cortex to the caudate nucleus and the cerebellum , 1978, Experimental Brain Research.