In vivo voltammetric monitoring of norepinephrine release in the rat ventral bed nucleus of the stria terminalis and anteroventral thalamic nucleus

The role and contribution of the dense noradrenergic innervation in the ventral bed nucleus of the stria terminalis (vBNST) and anteroventral thalamic nucleus (AV) to biological function and animal behaviors is poorly understood due to the small size of these nuclei. The aim of this study was to compare norepinephrine release and uptake in the vBNST with that in the AV of anesthetized rats. Measurements were made in vivo with fast‐scan cyclic voltammetry following electrical stimulation of noradrenergic projection pathways, either the dorsal noradrenergic bundle (DNB) or the ventral noradrenergic bundle (VNB). The substance detected was identified as norepinephrine based upon voltammetric, anatomical, neurochemical and pharmacological evidence. Fast‐scan cyclic voltammetry enables the selective monitoring of local norepinephrine overflow in the vBNST evoked by the stimulation of either the DNB or the VNB while norepinephrine in the AV was only evoked by DNB stimulation. The α2‐adrenoceptor antagonist yohimbine and the norepinephrine uptake inhibitor desipramine increased norepinephrine overflow and slowed its disappearance in both regions. However, control of extracellular norepinephrine by both autoreceptors and uptake was greater in the AV. The greater control exerted by autoreceptors and uptake in the AV resulted in reduced extracellular concentration compared with the v BNST when large numbers of stimulation pulses were employed. The differences in noradrenergic transmission observed in the terminal fields of the v BNST and the AV may differentially regulate activity in these two regions that both contain high densities of norepinephrine terminals.

[1]  F. Gonon,et al.  Continuousin vivo monitoring of evoked dopamine release in the rat nucleus accumbens by amperometry , 1994, Neuroscience.

[2]  P. Garris,et al.  Evoked Extracellular Dopamine In Vivo in the Medial Prefrontal Cortex , 1993, Journal of neurochemistry.

[3]  K. Gysling,et al.  Medullary noradrenergic neurons projecting to the bed nucleus of the stria terminalis express mRNA for the NMDA-NR1 receptor , 2000, Brain Research Bulletin.

[4]  R. Wightman,et al.  Dynamic changes in accumbens dopamine correlate with learning during intracranial self-stimulation , 2008, Proceedings of the National Academy of Sciences.

[5]  M. Suaud-Chagny,et al.  In vivo monitoring of evoked noradrenaline release in the rat anteroventral thalamic nucleus by continuous amperometry , 2002, Journal of neurochemistry.

[6]  F. Gonon,et al.  Facilitation and depression of ATP and noradrenaline release from sympathetic nerves of rat tail artery , 1999, The Journal of physiology.

[7]  K. Kishi,et al.  Ultrastructure of ascending cholinergic terminals in the anteroventral thalamic nucleus of the rat: A comparison with the mammillothalamic terminals , 2003, Brain Research Bulletin.

[8]  M. Gabriel,et al.  Local norepinephrine depletion and learning-related neuronal activity in cingulate cortex and anterior thalamus of rabbits , 2004, Experimental Brain Research.

[9]  J. Galligan,et al.  In vitro continuous amperometry with a diamond microelectrode coupled with video microscopy for simultaneously monitoring endogenous norepinephrine and its effect on the contractile response of a rat mesenteric artery. , 2006, Analytical chemistry.

[10]  A. Negro-Vilar,et al.  Effect of ventral noradrenergic bundle lesions on concentrations of monoamine neurotransmitters and metabolites in several discrete areas of the rat brain , 1987, Cellular and Molecular Neurobiology.

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

[12]  G. Paxinos.  The Rat nervous system , 1985 .

[13]  K. Yagi,et al.  Role of noradrenergic projections to the bed nucleus of the stria terminalis in neuroendocrine and behavioral responses to fear-related stimuli in rats , 1998, Brain Research.

[14]  K. Gysling,et al.  Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic–pituitary–adrenal axis , 2004, Brain Research Reviews.

[15]  R. Wightman,et al.  Resolving neurotransmitters detected by fast-scan cyclic voltammetry. , 2004, Analytical chemistry.

[16]  G. Aston-Jones,et al.  Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion , 2000, Nature.

[17]  R. Wightman,et al.  Microelectrodes for the measurement of catecholamines in biological systems. , 1996, Analytical chemistry.

[18]  A. Oke,et al.  In Vivo Dynamics of Norepinephrine Release‐Reuptake in Multiple Terminal Field Regions of Rat Brain , 1994, Journal of neurochemistry.

[19]  M. Millan,et al.  Simultaneous quantification of serotonin, dopamine and noradrenaline levels in single frontal cortex dialysates of freely-moving rats reveals a complex pattern of reciprocal auto- and heteroreceptor-mediated control of release , 1998, Neuroscience.

[20]  M. Fendt,et al.  Noradrenaline Transmission within the Ventral Bed Nucleus of the Stria Terminalis Is Critical for Fear Behavior Induced by Trimethylthiazoline, a Component of Fox Odor , 2005, The Journal of Neuroscience.

[21]  D. Jacobowitz,et al.  Biochemical mapping of noradrenergic nerves arising from the rat locus coeruleus. , 1974, Brain research.

[22]  M. Palkovits,et al.  Regional distribution of adrenaline in rat brain , 1976, Brain Research.

[23]  Garret D Stuber,et al.  Overoxidation of carbon-fiber microelectrodes enhances dopamine adsorption and increases sensitivity. , 2003, The Analyst.

[24]  F. Gonon,et al.  Electrically evoked noradrenaline release in the rat hypothalamic para ventricular nucleus studied by in vivo electrochemistry: Characterization and facilitation by increasing the stimulation frequency , 1990, Neuroscience.

[25]  O. Lindvall,et al.  Dopamine and noradrenaline neurons projecting to the septal area in the rat , 1978, Cell and Tissue Research.

[26]  Y. Oomura,et al.  Inhibitory action of the ventral noradrenergic bundle on the lateral hypothalamic neurons through alpha-noradrenergic mechanisms in the rat , 1982, Brain Research.

[27]  S. T. Mason,et al.  The neuropsychology and neuropharmacology of the dorsal ascending noradrenergic bundle—a review , 1980, Progress in Neurobiology.

[28]  P. Garris,et al.  Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  D. Saphier.  Electrophysiology and neuropharmacology of noradrenergic projections to rat PVN magnocellular neurons. , 1993, The American journal of physiology.

[30]  C. Berridge,et al.  The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes , 2003, Brain Research Reviews.

[31]  Hong-wei Dong,et al.  Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis , 2004, The Journal of comparative neurology.

[32]  F. Georges,et al.  Cannabinoid Receptors in the Bed Nucleus of the Stria Terminalis Control Cortical Excitation of Midbrain Dopamine Cells In Vivo , 2008, The Journal of Neuroscience.

[33]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[34]  C. Kilts,et al.  The simultaneous quantification of dopamine, norepinephrine and epinephrine in micropunched rat brain nuclei by on-line trace enrichment HPLC with electrochemical detection: Distribution of catecholamines in the limbic system , 1986, Neurochemistry International.

[35]  F. Bloom,et al.  The projections of the nucleus locus coeruleus: an autoradiographic study. , 1973, Life sciences.

[36]  F. Gonon,et al.  In vivo noradrenaline release evoked in the anteroventral thalamic nucleus by locus coeruleus activation: An electrochemical study , 1993, Neuroscience.

[37]  D. Rasmusson,et al.  Time course and effective spread of lidocaine and tetrodotoxin delivered via microdialysis: an electrophysiological study in cerebral cortex , 2001, Journal of Neuroscience Methods.

[38]  J. Stamford,et al.  Real-time monitoring of endogenous noradrenaline release in rat brain slices using fast cyclic voltammetry. 2. Operational characteristics of theα2 autoreceptor in the bed nucleus of stria terminalis, pars ventralis , 1993, Brain Research.

[39]  R. Adams,et al.  Real‐Time Monitoring of Electrically Stimulated Norepinephrine Release in Rat Thalamus: I. Resolution of Transmitter and Metabolite Signal Components , 1993, Journal of neurochemistry.

[40]  T. Kozicz.  Axon terminals containing tyrosine hydroxylase- and dopamine-β-hydroxylase immunoreactivity form synapses with galanin immunoreactive neurons in the lateral division of the bed nucleus of the stria terminalis in the rat , 2001, Brain Research.

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

[42]  M. Palkovits,et al.  Regional concentrations of noradrenaline and dopamine in rat brain , 1976, Brain Research.

[43]  J. Stamford,et al.  Real-time monitoring of endogenous noradrenaline release in rat brain slices using fast cyclic voltammetry: 1. Characterisation of evoked noradrenaline efflux and uptake from nerve terminals in the bed nucleus of stria terminalis, pars ventralis , 1992, Brain Research.

[44]  F E Bloom,et al.  Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. , 1979, Annual review of neuroscience.

[45]  H. Tanila,et al.  Noradrenaline overflow in mouse dentate gyrus following locus coeruleus and natural stimulation: real‐time monitoring by in vivo voltammetry , 2005, Journal of neurochemistry.

[46]  R. Wightman,et al.  Release and uptake of catecholamines in the bed nucleus of the stria terminalis measured in the mouse brain slice , 2002, Synapse.

[47]  F. Gonon,et al.  In Vivo Voltammetric Monitoring of Catecholamine Metabolism in the A1 and A2 Regions of the Rat Medulla Oblongata , 1986, Journal of neurochemistry.

[48]  M. Cassell,et al.  Distribution of dopaminergic fibers in the central division of the extended amygdala of the rat , 1994, Brain Research.

[49]  Inga Kadish,et al.  Role of the anterodorsal and anteroventral nuclei of the thalamus in spatial memory in the rat , 2002, Behavioural Brain Research.

[50]  F. Tarazi,et al.  [3H]beta-CIT: a radioligand for dopamine transporters in rat brain tissue. , 1999, European journal of pharmacology.

[51]  P. Garris,et al.  Heterogeneity of evoked dopamine overflow wihin the striatal and striatoamygdaloid regions , 1994, Neuroscience.

[52]  R. Moore.  Catecholamine innervation of the basal forebrain. I. The septal area , 1978 .

[53]  M. Gabriel,et al.  Interaction of laminae of the cingulate cortex with the anteroventral thalamus during behavioral learning. , 1980, Science.

[54]  B. K. Hartman,et al.  The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine‐B‐hydroxylase as a marker , 1975, The Journal of comparative neurology.

[55]  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.

[56]  M. G. Terenzi,et al.  A combined immunocytochemical and retrograde tracing study of noradrenergic connections between the caudal medulla and bed nuclei of the stria terminalis , 1995, Brain Research.

[57]  A. Oke,et al.  Catecholamine distribution patterns in rat thalamus , 1983, Brain Research.

[58]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[59]  P. Seeman,et al.  Dopamine receptor pharmacology. , 1994, Trends in pharmacological sciences.

[60]  C. Phelix,et al.  Monoamine innervation of bed nucleus of stria terminalis: An electron microscopic investigation , 1992, Brain Research Bulletin.

[61]  F. Tarazi,et al.  [3H]β-CIT: a radioligand for dopamine transporters in rat brain tissue , 1999 .