Multiple single-unit recordings in the striatum of freely moving animals: effects of apomorphine and d-amphetamine in normal and unilateral 6-hydroxydopamine-lesioned rats

Ensembles of striatal neurons were recorded in freely moving normal and unilateral 6-hydroxydopamine (6-OHDA)-lesioned rats using chronically implanted electrode arrays. Animals received bilateral striatal implants of two 16-microwire arrays 1 week before recordings. Identified striatal neurons were categorized as medium spiny-like and large aspiny-like based on a combination of their activity autocorrelations and firing rates. Baseline firing rates of medium spiny-like neurons in the 6-OHDA-lesioned striata were significantly faster than were firing rates of the same neurons in the intact hemispheres of 6-OHDA-lesioned rats or normal animals. However, firing rates of large aspiny-like neurons were faster in both hemispheres of the 6-OHDA-lesioned rats as compared to normal animals. Interestingly, firing rates of neurons in all groups decreased by fivefold or greater under urethane anesthesia, although the relative firing rates between hemispheres were unchanged. d-Amphetamine (5.0 mg/kg, s.c.) increased the firing rates of both types of striatal neurons by twofold or greater in normal rats and in the intact hemispheres of 6-OHDA-lesioned animals. By contrast, this treatment did not alter neuron firing in the 6-OHDA-lesioned striata. Apomorphine (0.05 mg/kg, s.c.) did not affect neuronal firing rates either in normal rat striatum or in the unlesioned hemispheres of 6-OHDA-lesioned animals. However, it did significantly increase the firing rate of the medium spiny-like neurons in 6-OHDA-lesioned striata. These results demonstrate that the dopaminergic innervation of the striatum differentially influences two electrophysiologically distinct sets of striatal neurons in freely moving rats.

[1]  M. Palmer,et al.  Effects of dopamine on spontaneous and evoked activity of caudate neurons , 1983, Neuropharmacology.

[2]  R. Christopher Pierce,et al.  A simple micromanipulator for multiple uses in freely moving rats: electrophysiology, voltammetry, and simultaneous intracerebral infusions , 1993, Journal of Neuroscience Methods.

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

[4]  G. Gerhardt,et al.  Increased dopamine clearance in the non-lesioned striatum of rhesus monkeys with unilateral 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) striatal lesions , 1995, Neuroscience Letters.

[5]  Asif A Ghazanfar,et al.  Hebb's Dream: The Resurgence of Cell Assemblies , 1997, Neuron.

[6]  E. Garcia-Rill,et al.  Long-term decreases in spontaneous firing of caudate neurons induced by amphetamine in cats , 1980, Brain Research.

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

[8]  W. Schultz,et al.  Striatal cell supersensitivity to apomorphine in dopamine-lesioned rats correlated to behaviour , 1978, Neuropharmacology.

[9]  U. Ungerstedt,et al.  6-Hydroxy-dopamine induced degeneration of central monoamine neurons. , 1968, European journal of pharmacology.

[10]  B J Hoffer,et al.  Cytochemical and electrophysiological studies of dopamine in the caudate nucleus. , 1976, Research publications - Association for Research in Nervous and Mental Disease.

[11]  U. Ungerstedt.  Striatal dopamine release after amphetamine or nerve degeneration revealed by rotational behaviour. , 1971, Acta physiologica Scandinavica. Supplementum.

[12]  P. Bickford,et al.  Reduced ageing effects of striatal neuronal discharge rate by aged ventral mesencephalic grafts , 1996, Neuroreport.

[13]  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.

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

[15]  Greg A. Gerhardt,et al.  Correlation of apomorphine- and amphetamine-induced turning with nigrostriatal dopamine content in unilateral 6-hydroxydopamine lesioned rats , 1993, Brain Research.

[16]  G. Rebec,et al.  Amphetamine-induced excitations predominate in single neostriatal neurons showing motor-related activity , 1989, Brain Research.

[17]  Charles J. Wilson,et al.  The generation of natural firing patterns in neostriatal neurons. , 1993, Progress in brain research.

[18]  G. Graveland,et al.  The frequency and distribution of medium-sized neurons with indented nuclei in the primate and rodent neostriatum , 1985, Brain Research.

[19]  W. B. Orr,et al.  Evidence for two functionally distinct subpopulations of neurons within the rat striatum , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  G. Rebec,et al.  Heterogenous responses of neostriatal neurons to amphetamine in freely moving rats , 1988, Brain Research.

[21]  G. Di Chiara,et al.  Dopamine-acetylcholine-glutamate interactions in the striatum. A working hypothesis. , 1993, Advances in neurology.

[22]  J. Bolam,et al.  Cholinergic synaptic input to different parts of spiny striatonigral neurons in the rat , 1988, The Journal of comparative neurology.

[23]  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.

[24]  J. Wayne Aldridge,et al.  The temporal structure of spike trains in the primate basal ganglia: afferent regulation of bursting demonstrated with precentral cerebral cortical ablation , 1991, Brain Research.

[25]  George V. Rebec,et al.  Neuronal and behavioral correlates of intrastriatal infusions of amphetamine in freely moving rats , 1993, Brain Research.

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

[27]  T. Ljungberg,et al.  A direct comparison of amphetamine-induced behaviours and regional brain dopamine release in the rat using intracerebral dialysis , 1987, Brain Research.

[28]  G. Rebec,et al.  Responses of neurons in dorsal striatum during amphetamine-induced focused stereotypy , 1997, Psychopharmacology.

[29]  P. Groves,et al.  Differential effects of the optical isomers of amphetamine on neuronal activity in the reticular formation and caudate nucleus of the rat , 1975, Brain Research.

[30]  M. Kimura.  Behaviorally contingent property of movement-related activity of the primate putamen. , 1990, Journal of neurophysiology.

[31]  G Bernardi,et al.  Electrophysiology of dopamine-denervated striatal neurons. Implications for Parkinson's disease. , 1993, Brain : a journal of neurology.

[32]  P. Groves,et al.  Enhancement of effects of dopaminergic agonists on neuronal activity in the caudate-putamen of the rat following long-term d-amphetamine administration , 1976, Pharmacology Biochemistry and Behavior.

[33]  G. Rebec,et al.  Iontophoresis of amphetamine in the neostriatum and nucleus accumbens of awake, unrestrained rats , 1997, Brain Research.

[34]  M. West,et al.  Low-dose amphetamine elevates movement-related firing of rat striatal neurons , 1997, Brain Research.

[35]  Kitai St,et al.  Cholinergic and dopaminergic modulation of potassium conductances in neostriatal neurons. , 1993 .

[36]  F. Delcomyn,et al.  Identification of bursts in spike trains , 1992, Journal of Neuroscience Methods.

[37]  George V. Rebec,et al.  Striatal single-unit responses to amphetamine and neuroleptics in freely moving rats , 1993, Neuroscience & Biobehavioral Reviews.

[38]  G. Rebec,et al.  Apomorphine-induced inhibition of neostriatal activity is enhanced by lesions induced by 6-hydroxydopamine but not by long-term administration of amphetamine , 1984, Neuropharmacology.

[39]  P. Groves,et al.  Antidromically identified striatonigral projection neurons in the chronically implanted behaving rat: relations of cell firing to amphetamine-induced behaviors. , 1989, Behavioral neuroscience.

[40]  J. P. Huston,et al.  The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments , 1996, Progress in Neurobiology.

[41]  G. E. Alexander,et al.  Microstimulation of the primate neostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties. , 1985, Journal of neurophysiology.

[42]  A. D. Smith,et al.  The section-Golgi-impregnation procedure—3. Combination of Golgi-impregnation with enzyme histochemistry and electron microscopy to characterize acetylcholinesterase-containing neurons in the rat neostriatum , 1984, Neuroscience.

[43]  G. E. Alexander,et al.  Microstimulation of the primate neostriatum. I. Physiological properties of striatal microexcitable zones. , 1985, Journal of neurophysiology.

[44]  G. Rebec,et al.  Bilateral cortical ablations attenuate amphetamine-induced excitations of neostriatal motor-related neurons in freely moving rats , 1991, Neuroscience Letters.

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

[46]  J. P. Huston,et al.  UNILATERAL 6-HYDROXYDOPAMINE LESIONS OF MESO-STRIATAL DOPAMINE NEURONS AND THEIR PHYSIOLOGICAL SEQUELAE , 1996, Progress in Neurobiology.

[47]  U. Ungerstedt.  Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. , 1971, Acta physiologica Scandinavica. Supplementum.

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

[49]  S. Iversen,et al.  Blockage of amphetamine induced motor stimulation and stereotypy in the adult rat following neonatal treatment with 6-hydroxydopamine. , 1973, Brain research.

[50]  Charles J. Wilson,et al.  Synaptic Regulation of Action Potential Timing in Neostriatal Cholinergic Interneurons , 1998, The Journal of Neuroscience.