Evoked Extracellular Dopamine In Vivo in the Medial Prefrontal Cortex

Abstract: The measurement of evoked extracellular dopamine in the medial prefrontal cortex by using fast‐scan cyclic voltammetry with carbon‐fiber microelectrodes was established and release characteristics of mesoprefrontal dopamine neurons were examined in vivo in anesthetized rats. Despite the sparse dopaminergic innervation and the presence of more dense noradrenergic and serotonergic innervations overall in the medial prefrontal cortex, the measurement of extracellular dopamine was achieved by selective recording in dopamine‐rich terminal fields and selective activation of ascending dopamine neurons. This was confirmed by electrochemical, pharmacological, and anatomical evidence. An increased release capacity for mesoprefrontal dopamine neurons was also demonstrated by the slower decay of the evoked dopamine response after inhibition of catecholamine synthesis and the maintenance of the evoked dopamine response at higher levels in the medial prefrontal cortex compared with the striatum during supraphysiological stimulation.

[1]  J. B. Justice,et al.  In vivo voltammetric determination of the kinetics of dopamine metabolism in the rat , 1985, Neuroscience Letters.

[2]  Jonathan A. Stamford,et al.  Diffusion and uptake of dopamine in rat caudate and nucleus accumbens compared using fast cyclic voltammetry , 1988, Brain Research.

[3]  J. Glowinski,et al.  Differential effects of ascending neurons containing dopamine and noradrenaline in the control of spontaneous activity and of evoked responses in the rat prefrontal cortex , 1988, Neuroscience.

[4]  L. Descarries,et al.  Regional and laminar density of the dopamine innervation in adult rat cerebral cortex , 1987, Neuroscience.

[5]  R. Roth,et al.  Extracellular dopamine and neurotensin in rat prefrontal cortex in vivo: effects of median forebrain bundle stimulation frequency, stimulation pattern, and dopamine autoreceptors , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  C. Kilts,et al.  Mesoamygdaloid dopamine neurons: differential rates of dopamine turnover in discrete amygdaloid nuclei of the rat brain , 1987, Brain Research.

[7]  L. Cubeddu,et al.  Sustained high release at rapid stimulation rates and reduced functional autoreceptors characterize prefrontal cortex dopamine terminals. , 1988, The Journal of pharmacology and experimental therapeutics.

[8]  R. Wightman,et al.  Monitoring the Stimulated Release of Dopamine with In Vivo Voltammetry. II: Clearance of Released Dopamine from Extracellular Fluid , 1984, Journal of neurochemistry.

[9]  G. Koob,et al.  The origin and distribution of dopamine-containing afferents to the rat frontal cortex , 1978, Brain Research.

[10]  L. Descarries,et al.  Quantified regional and laminar distribution of the noradrenaline innervation in the anterior half of the adult rat cerebral cortex , 1988, The Journal of comparative neurology.

[11]  R. Wightman,et al.  Effects of D‐2 Antagonists on Frequency‐Dependent Stimulated Dopamine Overflow in Nucleus Accumbens and Caudate‐Putamen , 1989, Journal of neurochemistry.

[12]  R. Moore,et al.  Serotonin neurons of the midbrain raphe: Ascending projections , 1978, The Journal of comparative neurology.

[13]  B. Bunney,et al.  Acute Effects of Typical and Atypical Antipsychotic Drugs on the Release of Dopamine from Prefrontal Cortex, Nucleus Accumbens, and Striatum of the Rat: An In Vivo Microdialysis Study , 1990, Journal of neurochemistry.

[14]  R. Wightman,et al.  Electrochemical, pharmacological and electrophysiological evidence of rapid dopamine release and removal in the rat caudate nucleus following electrical stimulation of the median forebrain bundle. , 1985, European journal of pharmacology.

[15]  J. Glowinski,et al.  Selective activation of the mesocortical DA system by stress , 1976, Nature.

[16]  K Fuxe,et al.  Distribution of noradrenaline nerve terminals in cortical areas of the rat. , 1968, Brain research.

[17]  E. Abercrombie,et al.  Differential Effect of Stress on In Vivo Dopamine Release in Striatum, Nucleus Accumbens, and Medial Frontal Cortex , 1989, Journal of neurochemistry.

[18]  L. Descarries,et al.  Quantification of the dopamine innervation in adult rat neostriatum , 1986, Neuroscience.

[19]  C. Altar,et al.  Dopamine release in vivo from nigrostriatal, mesolimbic, and mesocortical neurons: utility of 3-methoxytyramine measurements. , 1988, Pharmacological reviews.

[20]  B. Scatton,et al.  In vivo voltammetric measurement of extracellular DOPAC levels in the anteromedial prefrontal cortex of the rat , 1986, Brain Research.

[21]  B. Berger,et al.  Histochemical confirmation for dopaminergic innervation of the rat cerebral cortex after destruction of the noradrenergic ascending pathways. , 1974, Brain research.

[22]  R. Roth,et al.  Selective increase in dopamine metabolism in the prefrontal cortex by the anxiogenic beta-carboline FG 7142. , 1985, Biochemical pharmacology.

[23]  R. Wightman,et al.  Fast-scan voltammetry of biogenic amines. , 1988, Analytical chemistry.

[24]  H. Kim,et al.  Dynamics of the striatal 3-MT pool in rat and mouse: species differences as assessed by steady-state measurements and intracerebral dialysis. , 1988, Life sciences.

[25]  R. Roth,et al.  Regulation of dopamine synthesis in the medial prefrontal cortex is mediated by release modulating autoreceptors: studies in vivo. , 1986, The Journal of pharmacology and experimental therapeutics.

[26]  R. Wightman,et al.  Strategies for low detection limit measurements with cyclic voltammetry. , 1991, Analytical chemistry.

[27]  B. Scatton,et al.  An in Vivo Voltammetric Study of the Response of Mesocortical and Mesoaccumbens Dopaminergic Neurons to Environmental Stimuli in Strains of Rats with Differing Levels of Emotionality , 1988, Annals of the New York Academy of Sciences.

[28]  B. Berger,et al.  Dopaminergic innervation of the rat prefrontal cortex: A fluorescence histochemical study , 1976, Brain Research.

[29]  J. Glowinski,et al.  Topographical distribution of dopaminergic innervation and dopaminergic receptors of the anterior cerebral cortex of the rat , 1978, Brain Research.

[30]  J. B. Justice,et al.  Mechanisms contributing to the recovery of striatal releasable dopamine following MFB stimulation , 1987, Brain Research.

[31]  R. Roth,et al.  Characterization of dopamine release in the rat medial prefrontal cortex as assessed by in vivo microdialysis: Comparison to the striatum , 1990, Neuroscience.

[32]  R. Roth,et al.  Modulation of mesoprefrontal dopamine neurons by central benzodiazepine receptors. I. Pharmacological characterization. , 1990, The Journal of pharmacology and experimental therapeutics.

[33]  P. Voorn,et al.  Development of Dopamine - Containing Systems in the CNS , 1992 .

[34]  R. Roth,et al.  Mesocortical dopamine neurons: rapid transmitter turnover compared to other brain catecholamine systems. , 1981, Brain research.

[35]  C. Woolsey,et al.  The orbitofrontal cortex and its connections with the mediodorsal nucleus in rabbit, sheep and cat. , 1948, Research publications - Association for Research in Nervous and Mental Disease.

[36]  K Fuxe,et al.  Pharmaco-histochemical evidence of the existence of dopamine nerve terminals in the limbic cortex. , 1974, European journal of pharmacology.

[37]  Miklós Palkovits,et al.  Distribution of norepinephrine and dopamine in cerebral cortical areas of the rat , 1979, Brain Research Bulletin.

[38]  F. Gonon,et al.  Presynaptic autoinhibition of the electrically evoked dopamine release studied in the rat olfactory tubercle byin vivo electrochemistry , 1991, Neuroscience.

[39]  Anders Björklund,et al.  Regional differences in the regulation of dopamine and noradrenaline release in medial frontal cortex, nucleus accumbens and caudate-putamen: a microdialysis study in the rat , 1992, Brain Research.

[40]  G. Gerhardt,et al.  In vivo electrochemical studies of monoamine release in the medial prefrontal cortex of the rat , 1989, Neuroscience.

[41]  B. Bunney,et al.  Dopamine and norepinephrine innervated cells in the rat prefrontal cortex: pharmacological differentiation using microiontophoretic techniques. , 1976, Life sciences.

[42]  H. E. Rosvold,et al.  Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. , 1979, Science.

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

[44]  R. Wightman,et al.  Molecular Specificity of In Vivo Electrochemical Measurements , 1987 .

[45]  C. Leonard,et al.  The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. , 1969, Brain research.

[46]  R. M. Beckstead,et al.  Convergent thalamic and mesencephalic projections to the anterior medial cortex in the rat , 1976, The Journal of comparative neurology.

[47]  G. Jonsson,et al.  Neurochemical studies on central dopamine neurons--regional characterization of dopamine turnover. , 1984, Medical biology.

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

[49]  Ralph N. Adams,et al.  In vivo electrochemical measurements in the CNS , 1990, Progress in Neurobiology.

[50]  F. Mora,et al.  Brain self-stimulation: direct evidence for the involvement of dopamine in the prefrontal cortex. , 1977, Science.

[51]  R. Wightman,et al.  In vivo comparison of the regulation of releasable dopamine in the caudate nucleus and the nucleus accumbens of the rat brain , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  J. Glowinski,et al.  Dopaminergic Terminals in the Rat Cortex , 1973, Science.

[53]  R. Roth,et al.  Evidence for the absence of impulse-regulating somatodendritic and synthesis-modulating nerve terminal autoreceptors on subpopulations of mesocortical dopamine neurons , 1984, Neuroscience.

[54]  B. Brodie,et al.  Application of steady state kinetics to the estimation of synthesis rate and turnover time of tissue catecholamines. , 1966, The Journal of pharmacology and experimental therapeutics.

[55]  I. Hoffmann,et al.  Dopamine Autoreceptors Modulate Dopamine Release from the Prefrontal Cortex , 1986, Journal of neurochemistry.

[56]  R. Wightman,et al.  Direct in vivo monitoring of dopamine released from two striatal compartments in the rat. , 1983, Science.

[57]  J. Millar,et al.  Stimulated limbic and striatal dopamine release measured by fast cyclic voltammetry: anatomical, electrochemical and pharmacological characterisation , 1988, Brain Research.

[58]  M. Brazell,et al.  DIFFERENTIAL PULSE VOLTAMMETRY IN THE ANAESTHETIZED RAT: IDENTIFICATION OF ASCORBIC ACID, CATECHOL AND INDOLEAMINE OXIDATION PEAKS IN THE STRIATUM AND FRONTAL CORTEX , 1982, British journal of pharmacology.

[59]  C. Altar,et al.  Dopamine autoreceptors modulate the in vivo release of dopamine in the frontal, cingulate and entorhinal cortices. , 1987, The Journal of pharmacology and experimental therapeutics.

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

[61]  S. O'dell,et al.  Dopamine high-affinity transport site topography in rat brain: Major differences between dorsal and ventral striatum , 1990, Neuroscience.

[62]  R. Wightman,et al.  Heterogeneity of stimulated dopamine overflow within rat striatum as observed with in vivo voltammetry , 1989, Brain Research.

[63]  J. Fallon Topographic Organization of Ascending Dopaminergic Projections a , 1988, Annals of the New York Academy of Sciences.

[64]  R. M. Wightman,et al.  Real-time characterization of dopamine overflow and uptake in the rat striatum , 1988, Neuroscience.

[65]  M. Fillenz,et al.  Simultaneous monitoring of dopamine release in rat frontal cortex, nucleus accumbens and striatum: Effect of drugs, circadian changes and correlations with motor activity , 1985, Neuroscience.

[66]  U. Ungerstedt Stereotaxic mapping of the monoamine pathways in the rat brain. , 1971, Acta physiologica Scandinavica. Supplementum.

[67]  P. Garris,et al.  Regulation of transient dopamine concentration gradients in the microenvironment surrounding nerve terminals in the rat striatum , 1992, Neuroscience.

[68]  J. B. Justice,et al.  Dynamics of the recovery of releasable dopamine following electrical stimulation of the medial forebrain bundle , 1987, Neuroscience Letters.

[69]  G. Rose,et al.  Release of Monoamines from Striatum of Rat and Mouse Evoked by Local Application of Potassium: Evaluation of a New In Vivo Electrochemical Technique , 1986, Journal of neurochemistry.

[70]  R. Roth,et al.  Mesocortical dopamine neurons. Lack of autoreceptors modulating dopamine synthesis. , 1981, Molecular pharmacology.

[71]  E. Richfield,et al.  Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system , 1989, Neuroscience.