Summary
Excitatory postsynaptic potentials evoked in rat neostriatal spiny projections neurons were followed by a long (100–300 ms) period of membrane hyperpolarization, followed in turn by a late depolarization. Concomitant with these changes in membrane potential were inhibition and subsequent excitation of spontaneous firing and excitatory activity evoked from substantia nigra and cerebral peduncle, but not from cortical stimulating sites. Thalamic-evoked excitatory activity was sometimes sensitive and sometimes insensitive to this inhibition, which has previously been believed to result from intrinsic inhibitory synaptic activity among neostriatal neurons. In intracellular recordings from neostriatal neurons in urethane anesthetized rats this longlasting inhibitory response (1) exhibited alterations with intracellularly applied steady currents comparable to those of the EPSP, (2) failed to respond to intracellular injection of chloride ions, (3) was associated with either a decrease or no detectable change in the input conductance of the neurons, and (4) was abolished after lesions that interrupted polysynaptic pathways to neostriatum through intracortical and intrathalamic synaptic circuits. These findings indicate that the long lasting inhibitory portion of the responses of neostriatal neurons arises from a phasic inhibition of tonically active corticostriatal and thalamostriatal neurons and a concurrent decrease in the excitability of polysynaptic pathways converging on neostriatal neurons.
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References
Albé-Fessard D, Oswaldo-Cruz E, Rocha-Miranda CD (1960) Activités évoquées dans le noyau caude du chat en réponse à des types divers d'afferences. I. Étude microphysiologique. Electroenceph Clin Neurophysiol 12: 405–420
Andersen P, Eccles JC, Sears TA (1964) The ventro-basal complex of the thalamus: Types of cells, their responses and their functional organization. J Physiol (Lond) 174: 370–399
Bernardi G, Marciani MG, Morocutti C, Giacomini P (1975) The action of GABA on rat caudate neurones recorded intracellularly. Brain Res 92: 511–515
Bernardi G, Marciani MG, Morocutti C, Giacomini P (1976) The action of picrotoxin and bicuculline on rat caudate neurons inhibited by GABA. Brain Res 102: 379–384
Buchwald NA, Price DD, Vernon L, Hull CD (1973) Caudate intracellular response to thalamic and cortical inputs. Exp Neurol 38: 311–323
Conner JD (1970) Caudate nucleus neurons: Correlation of the effects of substantia nigra stimulation with iontophoretic dopamine. J Physiol (Lond) 208: 691–703
Creutzfeldt OD, Lux HD, Watanabe S (1966) Electrophysiology of cortical nerve cells. In: Purpura DP, Yahr MD (eds) The thalamus. Columbia Univ. Press, New York, pp 210–235
Feltz P, Albé-Fessard D (1972) A study of an ascending nigrocaudate pathway. Electroenceph Clin Neurophysiol 33: 179–193
Fuller DRG, Hull CD, Buchwald NA (1975) Intracellular responses of caudate output neurons to orthodromic stimulation. Brain Res 96: 337–341
Gonzales-Vegas JA (1974) Antagonism of dopamine-mediated inhibition in the nigro-striatal pathway: A mode of action of some catatonia-inducing drugs. Brain Res 80: 219–228
Hull CD, Bernardi G, Buchwald NA (1970) Intracellular responses of caudate neurons to brain stem stimulation. Brain Res 22: 163–179
Hull CD, Bernardi G, Price DD, Buchwald NA (1973) Intracellular responses of caudate neurons to temporally and spatially combined stimuli. Exp Neurol 38: 324–336
Katayama Y, Miyazaki S, Tsubokawa T (1981) Electrophysiological evidence favoring intracaudate axon collaterals of GABAergic caudate output neurons in the cat. Brain Res 216: 180–186
Katayama Y, Tsubokawa T, Moriyasu N (1980) Slow rhythmic activity of caudate neurons in the cat: Statistical analysis of caudate neuronal spike trains. Exp Neurol 68: 310–321
Kitai ST, Wagner A, Precht W, Ohno T (1975) Nigro-caudate and caudato-nigral relationship: An electrophysiological study. Brain Res 85: 44–48
Kocsis JD, Kitai ST (1977) Dual excitatory inputs to caudate spiny neurons from substantia nigra stimulation. Brain Res 138: 271–283
Kocsis JD, Sugimori M, Kitai ST (1976) Convergence of excitatory synaptic inputs to caudate spiny neurons. Brain Res 124: 403–413
Lighthall JW, Kitai ST (1981) GABA-ergic recurrent inhibition in neostriatal slice preparation. Neurosci Abst 7: 849
Lighthall JW, Park MR, Kitai ST (1981) Inhibition in slices of rat striatum. Brain Res 212: 182–187
Liles SL (1974) Single-unit responses of caudate neurons to stimulation of frontal cortex, substantia nigra and entopeduncular nucleus in cats. J Neurophysiol 37: 254–265
Llinás R (1964) Mechanisms of supraspinal actions upon spinal cord activities. Differences between reticular and cerebellar inhibitory actions upon alpha extensor motoneurons. J Neurophysiol 27: 1117–1126
Misgeld U, Wagner A, Ohno T (1982) Depolarizing IPSPs and depolarization by GABA of rat neostriatum cells in vitro. Exp Brain Res 45: 108–114
Park MR, Gonzales-Vegas JA, Kitai ST (1982) Serotonergic excitation from dorsal raphe stimulation recorded intracellularly from rat caudate-putamen. Brain Res 243: 49–58
Park MR, Lighthall JW, Kitai ST (1980) Recurrent inhibition in the rat neostriatum. Brain Res 194: 359–369
Phillips CG, Porter R (1977) Corticospinal neurones. Academic Press, New York
Purpura DP (1972) Synaptic mechanisms in coordination of activity in thalamic internuncial common paths. In: Frigyesi TL, Rinvik E, Yahr MD (eds) Corticothalamic projections and sensorimotor activities. Raven Press, New York, pp 21–56
Purpura DP, Malliani A (1967) Intracellular studies of the corpus striatum. I. Synaptic potentials and discharge characteristics of caudate neurons activated by thalamic stimulation. Brain Res 6: 325–340
Richardson TL, Miller JJ, McLennan H (1977) Mechanisms of excitation and inhibition in the nigrostriatal system. Brain Res 127: 219–234
Rocha-Miranda CE (1965) Single unit analysis of cortex-caudate connections. Electroenceph Clin Neurophysiol 19: 237–247
Sedgwick EM, Williams TD (1967) The response of single units in the caudate nucleus to peripheral stimulation. J Physiol (Lond) 189: 281–298
Stefanis C, Jasper HH (1964) Intracellular microelectrode studies of antidromic responses in cortical pyramidal tract neurons. J Neurophysiol 27: 828–854
Terzuolo CA (1959) Cerebellar inhibitory and excitatory actions upon spinal extensor motoneurons. Arch Ital Biol 97: 316–339
Toyama K, Tsukahara N, Udo M (1968) Nature of the cerebellar influences upon the red nucleus neurons. Exp Brain Res 4: 292–309
VanderMaelen CP, Bonduki AC, Kitai ST (1979) Excitation of caudate-putamen neurons following stimulation of the dorsal raphe nucleus in the rat. Brain Res 175: 356–361
VanderMaelen CP, Kitai ST (1981) Intracellular analysis of synaptic potentials in rat neostriatum following stimulation of the cerebral cortex, thalamus and substantia nigra. Brain Res Bull 5: 725–733
Wilson CJ, Chang HT, Kitai ST (1982) Origins of postsynaptic potentials evoked in identified rat neostriatal neurons by stimulation in substantia nigra. Exp Brain Res 45: 157–167
Wilson CJ, Chang HT, Kitai ST (1983) Origins of postsynaptic potentials evoked in spiny neostriatal projection neurons by thalamic stimulation in the rat. Exp Brain Res 51: 217–226
Wilson CJ, Groves PM (1981) Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res 220: 67–80
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Wilson, C.J., Chang, H.T. & Kitai, S.T. Disfacilitation and long-lasting inhibition of neostriatal neurons in the rat. Exp Brain Res 51, 227–235 (1983). https://doi.org/10.1007/BF00237198
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DOI: https://doi.org/10.1007/BF00237198