Electrophysiological characterization of rat striatal neurons in vitro following a unilateral lesion of dopamine cells

The effects of a unilateral 6 to 19‐week lesion of dopamine cells on the excitability of rat striatal neurons were investigated in vitro using the intracellularly recorded membrane properties of neurons obtained ipsilateral and contralateral to 6‐hydroxydopamine (6‐OHDA) injection sites. Neurons ipsilateral to the lesion site and in striatal tissue depleted of dopamine exhibited resting membrane potentials and membrane resistances similar to those recorded in contralateral striatal neurons. Denervation appeared to have no appreciable effect on the proportion of neurons exhibiting various patterns of neuronal spiking (repetitive, bursting, or single spike) evoked by depolarizing current pulses. Current‐voltage determinations revealed nominal rectification in the majority of neurons and marked nonlinearty consistent with inward rectification at potentials hyperpolarized and depolarized to rest in a large proportion of the remaining neurons. Neurons ipsilateral to 6‐OHDA lesion sites exhibited these relationships in the same proportion as contralateral control cells. However, ipsilateral neurons with nominal rectification exhibited an average rate constant for the early onset of small hyperpolarizing membrane transients which was significantly smaller than that of controls. This finding suggests that intrinsic membrane parameters regulating the excitability of certain striatal neurons may be under the influence of dopamine or other factors closely associated with nigrostriatal nerve terminals. Published 1993 Wiley‐Liss, Inc.

[1]  C. Gerfen,et al.  D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. , 1990, Science.

[2]  T. F. Freund,et al.  Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines , 1984, Neuroscience.

[3]  P. Calabresi,et al.  Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: Evidence for D1 receptor involvement , 1987, Neuroscience.

[4]  C. Gerfen,et al.  Levodopa replacement therapy alters enzyme activities in striatum and neuropeptide content in striatal output regions of 6-hydroxydopamine lesioned rats , 1991, Brain Research.

[5]  J. Walsh,et al.  Dye‐Coupling in the neostriatum of the rat: I. Modulation by dopamine‐depleting lesions , 1989, Synapse.

[6]  H. Dodt,et al.  Muscarinic slow excitation and muscarinic inhibition of synaptic transmission in the rat neostriatum. , 1986, The Journal of physiology.

[7]  S. W. Jaslove The integrative properties of spiny distal dendrites , 1992, Neuroscience.

[8]  W. Rall Time constants and electrotonic length of membrane cylinders and neurons. , 1969, Biophysical journal.

[9]  C. Wilson,et al.  Cellular mechanisms controlling the strength of synapses. , 1988, Journal of electron microscopy technique.

[10]  Theodore W. Berger,et al.  Short-term effects of dopamine-depleting brain lesions on spontaneous activity of striatal neurons: Relation to local dopamine concentration and behavior , 1986, Brain Research.

[11]  I. Strömberg,et al.  Effects of locally applied D1 and D2 agonists on striatal neurons with 6-OHDA and pertussis toxin lesions , 1991, Brain Research.

[12]  Stéphane Huot,et al.  Simultaneous Determination of 3,4‐Dihydroxyphenylalanine, 5‐Hydroxytryptophan, Dopamine, 4‐Hydroxy‐3‐Methoxyphenylalanine, Norepinephrine, 3,4‐Dihydroxyphenylacetic Acid, Homovanillic Acid, Serotonin, and 5‐Hydroxyindoleacetic Acid in Rat Cerebrospinal Fluid and Brain by High‐Performance Liquid Chro , 1982, Journal of neurochemistry.

[13]  G. Arbuthnott,et al.  Spine density on neostriatal neurones changes with 6-hydroxydopamine lesions and with age , 1989, Brain Research.

[14]  A. D. Smith,et al.  The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones , 1990, Trends in Neurosciences.

[15]  John F. Marshall,et al.  Plasticity of [14C]2-deoxy-d-glucose incorporation into neostriatum and related structures in response to dopamine neuron damage and apomorphine replacement , 1980, Brain Research.

[16]  P. Calabresi,et al.  Intrinsic membrane properties of neostriatal neurons can account for their low level of spontaneous activity , 1987, Neuroscience.

[17]  R P Lesser,et al.  Analysis of the clinical problems in parkinsonism and the complications of long‐term levodopa therapy , 1979, Neurology.

[18]  M. Levine Neurophysiological and Morphological Alterations in Caudate Neurons in Aged Cats a , 1988, Annals of the New York Academy of Sciences.

[19]  T. Kita,et al.  Passive electrical membrane properties of rat neostriatal neurons in an in vitro slice preparation , 1984, Brain Research.

[20]  A. Prince,et al.  HEPANOSTICON IN SCREENING FOR HBsAg , 1975, The Lancet.

[21]  Y. Kawaguchi,et al.  Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents. , 1992, Journal of neurophysiology.

[22]  C. Wilson,et al.  Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. , 1989, Journal of neurophysiology.

[23]  F. Pongrácz,et al.  The function of dendritic spines: A theoretical study , 1985, Neuroscience.

[24]  S. T. Kitai,et al.  Morphological and physiological properties of neostriatal neurons: An intracellular horseradish peroxidase study in the rat , 1982, Neuroscience.

[25]  T. Berger,et al.  Spontaneous activity of Type II but not Type I striatal neurons is correlated with recovery of behavioral function after dopamine-depleting brain lesions , 1988, Brain Research.

[26]  K. Jellinger,et al.  Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. , 1973, Journal of the neurological sciences.

[27]  S. T. Kitai,et al.  Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  T. Powell,et al.  The termination of fibres from the cerebral cortex and thalamus upon dendritic spines in the caudate nucleus: a study with the Golgi method. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  Charles J. Wilson,et al.  Spontaneous firing patterns of identified spiny neurons in the rat neostriatum , 1981, Brain Research.

[30]  H. Fibiger,et al.  On the use of lesions of afferents to localize neurotransmitter receptor sites in the striatum , 1982, Brain Research.

[31]  P. Calabresi,et al.  Endogenous dopamine and dopaminergic agonists modulate synaptic excitation in neostriatum: Intracellular studies from naive and catecholamine-depleted rats , 1988, Neuroscience.

[32]  C. Marsden,et al.  SUCCESS AND PROBLEMS OF LONG-TERM LEVODOPA THERAPY IN PARKINSON'S DISEASE , 1977, The Lancet.

[33]  U. Ungerstedt,et al.  Short-term dopaminergic regulation of GABA release in dopamine deafferented caudate-putamen is not directly associated with glutamic acid decarboxylase gene expression , 1991, Neuroscience Letters.

[34]  R. C. Collins,et al.  Effects of dopaminergic stimulation on functional brain metabolism in rats with unilateral substantia nigra lesions , 1983, Brain Research.

[35]  P. Calabresi,et al.  Depletion of catecholamines reveals inhibitory effects of bromocryptine and lysuride on neostriatal neurones recorded intracellularly in vitro , 1988, Neuropharmacology.

[36]  D. Hillman,et al.  Robust synaptic plasticity of striatal cells following partial deafferentation , 1990, Brain Research.

[37]  T. Berger,et al.  Long-term effects of dopamine-depleting brain lesions on spontaneous activity of type II striatal neurons: Relation to behavioral recovery , 1986, Brain Research.

[38]  N. A. Buchwald,et al.  Quantitative morphology of medium-sized caudate spiny neurons in aged cats , 1986, Neurobiology of Aging.

[39]  R. North,et al.  Membrane properties and synaptic responses of rat striatal neurones in vitro. , 1991, The Journal of physiology.

[40]  M. Sugimori,et al.  Response properties and electrical constants of caudate nucleus neurons in the cat. , 1978, Journal of neurophysiology.

[41]  J. P. Walsh,et al.  Intracellular neurophysiological analysis reveals alterations in excitation in striatal neurons in aged rats , 1989, Brain Research.

[42]  G. Shepherd The Synaptic Organization of the Brain , 1979 .