Augmentation of prefrontal cortical monoaminergic activity inhibits dopamine release in the caudate nucleus: Anin vivo neurochemical assessment in the rhesus monkey

Prefrontal cortical modulation of caudate nucleus dopamine release was investigated in the rhesus monkey using the in vivo microdialysis technique. Reliable and stable basal caudate nucleus dopamine levels were quickly attained within hours following insertion of the dialysis probes. High-potassium (60 mM) or tetrodotoxin (10 microM) infusions significantly altered caudate nucleus dopamine levels in the dialysate indicating that measured dopamine levels reflected impulse-dependent release from the presynaptic pool. Pharmacological augmentation of monoaminergic transmission in the sulcus principalis region of the prefrontal cortex resulted in significant alterations in caudate nucleus dopamine levels. Increase of monoaminergic activity by infusion of either D-amphetamine (100 microM) or cocaine hydrochloride (100 microM) resulted in a gradual and prolonged decrease in caudate nucleus dopamine levels. Similar decreases were noticed in caudate nucleus dopamine metabolite levels. The present results indicate that in non-human primates modulation of dorsolateral prefrontal cortical monoaminergic transmission results in alterations in dopamine levels in subcortical structures. This observation may have clinical implications for therapeutic management of certain neuropsychiatric disorders, particularly schizophrenia.

[1]  Koh Hh,et al.  Effects of ketamine on brain monoamine levels in rats. , 1978 .

[2]  Ariel Y. Deutch,et al.  Prefrontal cortical dopamine depletion enhances the responsiveness of mesolimbic dopamine neurons to stress , 1990, Brain Research.

[3]  W. Nauta,et al.  An intricately patterned prefronto‐caudate projection in the rhesus monkey , 1977, The Journal of comparative neurology.

[4]  G. Aghajanian,et al.  Effects of Amphetamine on Single Cell Activity in a Catecholamine Nucleus, the Locus Coeruleus , 1971, Nature.

[5]  R. Roth,et al.  Effects of 6-hydroxydopamine lesions of the prefrontal cortex on tyrosine hydroxylase activity in mesolimbic and nigrostriatal dopamine systems , 1992, Neuroscience.

[6]  P. Goldman-Rakic,et al.  In vivo assessment of basal and drug‐induced dopamine release in cortical and subcortical regions of the anesthetized primate , 1993, Synapse.

[7]  N. Koshikawa,et al.  Ketamine anaesthesia has no effect on striatal dopamine metabolism in rats , 1988, Brain Research.

[8]  C. Carter,et al.  Effect of lesion of cortical dopamine terminals on subcortical dopamine receptors in rats , 1980, Nature.

[9]  M. Le Moal,et al.  Presynaptic control of dopamine metabolism in the nucleus accumbens. Lack of effect of buspirone as demonstrated using in vivo voltammetry. , 1987, Life sciences.

[10]  J. Glowinski,et al.  AN ADAPTATION OF THE PUSH‐PULL CANNULA METHOD TO STUDY THE IN VIVO RELEASE OF [3H]DOPAMINE SYNTHESIZED FROM [3H]TYROSINE IN THE CAT CAUDATE NUCLEUS: EFFECTS OF VARIOUS PHYSICAL AND PHARMACOLOGICAL TREATMENTS , 1977, Journal of neurochemistry.

[11]  P. Goldman-Rakic,et al.  Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[12]  A. D. Smith,et al.  Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium‐size spiny neurons in the rat neostriatum , 1988, The Journal of comparative neurology.

[13]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain IV. Topography of the dopamine projection to the basal forebrain and neostriatum , 1978, The Journal of comparative neurology.

[14]  P F Morrison,et al.  Effects of Different Semipermeable Membranes on In Vitro and In Vivo Performance of Microdialysis Probes , 1990, Journal of neurochemistry.

[15]  R. Hassler,et al.  Effect of frontal cortex ablation on striatal glutamic acid level in rat , 1977, Brain Research.

[16]  P. Goldman-Rakic,et al.  The anatomy of dopamine in monkey and human prefrontal cortex. , 1992, Journal of neural transmission. Supplementum.

[17]  A. Young,et al.  Excitatory Amino Acid Neurotransmitters in the Corticostriate Pathway: Studies Using Intracerebral Microdialysis In Vivo , 1986, Journal of neurochemistry.

[18]  R. Saunders,et al.  An improved methodology for routine in vivo microdialysis in non-human primates , 1994, Journal of Neuroscience Methods.

[19]  G. Aghajanian,et al.  Reserpine suppression of dorsal raphe neuronal firing: mediation by adrenergic system. , 1978, European journal of pharmacology.

[20]  P. Goldman-Rakic,et al.  Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique. , 1993, Cerebral cortex.

[21]  G. Cohen,et al.  Studies on the distinction between uptake inhibition and release of (3H)dopamine in rat brain tissue slices. , 1975, Biochemical pharmacology.

[22]  A. Deutch The regulation of subcortical dopamine systems by the prefrontal cortex: interactions of central dopamine systems and the pathogenesis of schizophrenia. , 1992, Journal of neural transmission. Supplementum.

[23]  T. Goldberg,et al.  Learning and memory in monozygotic twins discordant for schizophrenia , 1993, Psychological Medicine.

[24]  B. Westerink,et al.  Scope and limitations of in vivo brain dialysis: a comparison of its application to various neurotransmitter systems. , 1987, Life sciences.

[25]  D. Rosene,et al.  A cryoprotection method that facilitates cutting frozen sections of whole monkey brains for histological and histochemical processing without freezing artifact. , 1986, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[26]  T. Robinson,et al.  Microdialysis in the neurosciences , 1991 .

[27]  J. Glowinski,et al.  The mesocortico-prefrontal dopaminergic neurons , 1984, Trends in Neurosciences.

[28]  U. Ungerstedt,et al.  An in vivo microdialysis characterization of extracellular dopamine and GABA in dorsolateral striatum of awake freely moving and halothane anaesthetised rats , 1990, Journal of Neuroscience Methods.

[29]  H. Herdon,et al.  Differences between the release of radiolabelled and endogenous dopamine from superfused rat brain slices: Effects of depolarizing stimuli, amphetamine and synthesis inhibition , 1985, Brain Research.

[30]  T. Thompson American Psychiatric Press Review of Psychiatry, vol. 12 , 1994 .

[31]  S. Sesack,et al.  In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other , 1990, Brain Research.

[32]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[33]  D. Weinberger Implications of normal brain development for the pathogenesis of schizophrenia. , 1987, Archives of general psychiatry.

[34]  Hugh J. Spencer Antagonism of cortical excitation of striatal neurons by glutamic acid diethyl ester: Evidence for glutamic acid as an excitatory transmitter in the rat striatum , 1976, Brain Research.

[35]  J. Scheel-Krüger,et al.  Comparative studies of various amphetamine analogues demonstrating different interactions with the metabolism of the catecholamines in the brain. , 1971, European journal of pharmacology.

[36]  H. Fibiger,et al.  Electrical Stimulation of the Medial Prefrontal Cortex Increases Dopamine Release in the Striatum , 1993, Neuropsychopharmacology.

[37]  K. E. Moore,et al.  D-amphetamine-induced release of "newly synthesized" and "stored" dopamine from the caudate nucleus in vivo. , 1975, The Journal of pharmacology and experimental therapeutics.

[38]  C. A. Marsden,et al.  Measurement of neurotransmitter release in vivo , 1984 .

[39]  U. Ungerstedt,et al.  An In Vivo Study of Dopamine Release and Metabolism in Rat Brain Regions Using Intracerebral Dialysis , 1986, Journal of neurochemistry.

[40]  R. Roth,et al.  Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with Phaseolus vulgaris leucoagglutinin , 1989, The Journal of comparative neurology.

[41]  J. Desce,et al.  l-Glutamate-evoked release of dopamine from synaptosomes of the rat striatum: Involvement of AMPA and N-methyl-d-aspartate receptors , 1992, Neuroscience.

[42]  A. Grace Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: A hypothesis for the etiology of schizophrenia , 1991, Neuroscience.

[43]  R. M. Beckstead,et al.  Striatal preprotachykinin and preproenkephalin mRNA levels and the levels of nigral substance P and pallidal Met5-enkephalin depend on corticostriatal axons that use the excitatory amino acid neurotransmitters aspartate and glutamate: quantitative radioimmunocytochemical and in situ hybridization ev , 1990, Brain research. Molecular brain research.

[44]  R. E. Study,et al.  Isoflurane Inhibits Multiple Voltage‐gated Calcium Currents in Hippocampal Pyramidal Neurons , 1994, Anesthesiology.

[45]  S. D. Glick,et al.  Similar effects ofd-amphetamine and cocaine on extracellular dopamine levels in medial prefrontal cortex of rats , 1990, Brain Research.

[46]  D. Weinberger,et al.  Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia. III. A new cohort and evidence for a monoaminergic mechanism. , 1988, Archives of general psychiatry.

[47]  M. Reilly,et al.  Intraneuronal dopaminergic action of cocaine and some of its metabolites and analogs , 1983, Neuropharmacology.

[48]  E. Rubinstein,et al.  Comparison of ketamine, physical restraint, halothane and pentobarbital: Lack of influence on serotonergic measures in monkeys and rats , 1987, Neuropharmacology.

[49]  H. Benveniste,et al.  Determination of Brain Interstitial Concentrations by Microdialysis , 1989, Journal of neurochemistry.

[50]  B. Moghaddam,et al.  Differential effect of cocaine on extracellular dopamine levels in rat medial prefrontal cortex and nucleus accumbens: Comparison to amphetamine , 1989, Synapse.

[51]  J. Lehmann,et al.  The striatal cholinergic interneuron: Synaptic target of dopaminergic terminals? , 1983, Neuroscience.

[52]  U. Ungerstedt,et al.  Anaesthesia effects on in vivo acetylcholine transmission; comparisons of radioenzymatic and HPLC assays. , 1990, European journal of pharmacology.

[53]  A C Roberts,et al.  6-Hydroxydopamine lesions of the prefrontal cortex in monkeys enhance performance on an analog of the Wisconsin Card Sort Test: possible interactions with subcortical dopamine , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  Douglas W. Jones,et al.  The effect of amphetamine on regional cerebral blood flow during cognitive activation in schizophrenia , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  P. Goldman-Rakic,et al.  Overlap of dopaminergic, adrenergic, and serotoninergic receptors and complementarity of their subtypes in primate prefrontal cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  P. Goldman-Rakic,et al.  Topography of Corticostriatal Projections in Nonhuman Primates and Implications for Functional Parcellation of the Neostriatum , 1986 .

[57]  B. Westerink,et al.  Chronic Use of Intracerebral Dialysis for the In Vivo Measurement of 3,4‐Dihydroxyphenylethylamine and Its Metabolite 3,4‐Dihydroxyphenylacetic Acid , 1986, Journal of Neurochemistry.

[58]  J. Hsiao,et al.  In vivo changes of catecholamines in hemiparkinsonian monkeys measured by microdialysis , 1990, Experimental Neurology.

[59]  L. Saarnivaara,et al.  Effect of Ketamine Anaesthesia on the Content of Monoamines and their Metabolites in the Rat Brain , 1976, Acta anaesthesiologica Scandinavica.

[60]  L. Cubeddu,et al.  Effects of d-amphetamine and dopamine synthesis inhibitors on dopamine and acetylcholine neurotransmission in the striatum. I. Release in the absence of vesicular transmitter stores. , 1986, The Journal of pharmacology and experimental therapeutics.

[61]  P. Herrling Pharmacology of the corticocaudate excitatory postsynaptic potential in the cat: Evidence for its mediation by quisqualateor kainate-receptors , 1985, Neuroscience.

[62]  T. Svensson,et al.  Local cooling of pre-frontal cortex induces pacemaker-like firing of dopamine neurons in rat ventral tegmental area in vivo. , 1989, Acta physiologica Scandinavica.

[63]  S. Iversen,et al.  Effect of injections of 6-OHDA into either nucleus accumbens septi or frontal cortex on spontaneous and drug-induced activity , 1983, Neuropharmacology.

[64]  D. Weinberger,et al.  Dopamine and schizophrenia—a cortically corrective perspective , 1992 .

[65]  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.

[66]  U. Ungerstedt,et al.  In vivo measurement of extracellular dopamine and DOPAC in rat striatum after various dopamine-releasing drugs; implications for the origin of extracellular DOPAC. , 1988, European journal of pharmacology.

[67]  Tadaharu Tsumoto,et al.  Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral neocortex , 1990, Neuroscience Research.

[68]  K. Davis,et al.  Dopamine in schizophrenia: a review and reconceptualization. , 1991, The American journal of psychiatry.

[69]  D. Weinberger,et al.  Microinjection of apomorphine into the prefrontal cortex of the rat reduces dopamine metabolite concentrations in microdialysate from the caudate nucleus , 1991, Biological Psychiatry.

[70]  G. Gessa,et al.  (—)-Sulpiride activates the firing rate and tyrosine hydroxylase activity of dopaminergic neurons in unanesthetized rats , 1983, Brain Research.

[71]  D. Weinberger,et al.  Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia. IV. Further evidence for regional and behavioral specificity. , 1988, Archives of general psychiatry.

[72]  M. Le Moal,et al.  Opposite influences of dopaminergic pathways to the prefrontal cortex or the septum on the dopaminergic transmission in the nucleus accumbens. An in vivo voltammetric study , 1989, Neuroscience.

[73]  F. Gonon,et al.  Prefrontal cortex regulates burst firing and transmitter release in rat mesolimbic dopamine neurons studied in vivo , 1993, Neuroscience Letters.

[74]  Philip Seeman,et al.  Cloning of the gene for a human dopamine D4 receptor with high affinity for the antipsychotic clozapine , 1991, Nature.

[75]  R. Roth,et al.  Pharmacology of mesocortical dopamine neurons. , 1983, Pharmacological reviews.