Modulation of glutamatergic synaptic transmission in the bed nucleus of the stria terminalis

Progress in Neuro-Psychopharmacology and Biological Psychiatry - Tập 33 Số 8 - Trang 1329-1335 - 2009
Zoé A. McElligott1, Danny G. Winder2,3,1
1Vanderbilt Brain Institute, Vanderbilt University Medical Center, Nashville, TN, USA
2Department of Molecular, Physiology and Biophysics, Vanderbilt University Medical Center, Nashville, TN USA.
3Kennedy Center For Human Development, Vanderbilt University Medical Center, Nashville, TN, USA

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Allen Institute for Brain Science, 2008, Allen Brain Atlas

Arluison, 1990, Origin of some enkephalin-containing afferents to the ventro-medial region of the globus pallidus in the rat, Brain Res Bull, 25, 25, 10.1016/0361-9230(90)90249-Y

Banihashemi, 2006, Noradrenergic inputs to the bed nucleus of the stria terminalis and paraventricular nucleus of the hypothalamus underlie hypothalamic-pituitary-adrenal axis but not hypophagic or conditioned avoidance responses to systemic yohimbine, J Neurosci, 26, 11442, 10.1523/JNEUROSCI.3561-06.2006

Bienkowski, 2008, Noradrenergic inputs to the paraventricular hypothalamus contribute to hypothalamic-pituitary-adrenal axis and central Fos activation in rats after acute systemic endotoxin exposure, Neuroscience, 156, 1093, 10.1016/j.neuroscience.2008.08.011

Bohn, 2000, Potentiated opioid analgesia in norepinephrine transporter knock-out mice, J Neurosci, 20, 9040, 10.1523/JNEUROSCI.20-24-09040.2000

Boudaba, 1996, Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus, J Neurosci, 16, 7151, 10.1523/JNEUROSCI.16-22-07151.1996

Breese, 2005, Stress enhancement of craving during sobriety: a risk for relapse, Alcohol Clin Exp Res, 29, 185, 10.1097/01.ALC.0000153544.83656.3C

Cain, 2004, Adrenergic transmission facilitates extinction of conditional fear in mice, Learn Mem, 11, 179, 10.1101/lm.71504

Carboni, 2000, Stimulation of in vivo dopamine transmission in the bed nucleus of stria terminalis by reinforcing drugs, J Neurosci, 20, RC102, 10.1523/JNEUROSCI.20-20-j0002.2000

Cecchi, 2002, Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress, Neuroscience, 112, 13, 10.1016/S0306-4522(02)00062-3

Champagne, 1998, CRFergic innervation of the paraventricular nucleus of the rat hypothalamus: a tract-tracing study, J Neuroendocrinol, 10, 119, 10.1046/j.1365-2826.1998.00179.x

Chiamulera, 2001, Reinforcing and locomotor stimulant effects of cocaine are absent in mGluR5 null mutant mice, Nat Neurosci, 4, 873, 10.1038/nn0901-873

Choi, 2007, Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs, J Neurosci, 27, 2025, 10.1523/JNEUROSCI.4301-06.2007

Choi, 2008, The anteroventral bed nucleus of the stria terminalis differentially regulates hypothalamic-pituitary-adrenocortical axis responses to acute and chronic stress, Endocrinology, 149, 818, 10.1210/en.2007-0883

Choi, 2008, The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamic-pituitary-adrenocortical axis responsiveness to acute and chronic stress, Psychoneuroendocrinology, 33, 659, 10.1016/j.psyneuen.2008.02.006

Crane, 2003, Evidence that the bed nucleus of the stria terminalis contributes to the modulation of hypophysiotropic corticotropin-releasing factor cell responses to systemic interleukin-1beta, J Comp Neurol, 467, 232, 10.1002/cne.10918

Crankshaw, 2003, Effects of intracerebroventricular ethanol on ingestive behavior and induction of c-Fos immunoreactivity in selected brain regions, Physiol Behav, 79, 113, 10.1016/S0031-9384(03)00111-2

Cullinan, 1993, Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis, J Comp Neurol, 332, 1, 10.1002/cne.903320102

Cullinan, 1996, Fos expression in forebrain afferents to the hypothalamic paraventricular nucleus following swim stress, J Comp Neurol, 368, 88, 10.1002/(SICI)1096-9861(19960422)368:1<88::AID-CNE6>3.0.CO;2-G

Cullinan, 2008, Functional role of local GABAergic influences on the HPA axis, Brain Struct Funct, 213, 63, 10.1007/s00429-008-0192-2

Davis, 2008, Yohimbine impairs extinction of cocaine-conditioned place preference in an alpha2-adrenergic receptor independent process, Learn Mem, 15, 667, 10.1101/lm.1079308

Day, 1997, Distribution of alpha 1a-, alpha 1b- and alpha 1d-adrenergic receptor mRNA in the rat brain and spinal cord, J Chem Neuroanat, 13, 115, 10.1016/S0891-0618(97)00042-2

Delfs, 2000, Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion, Nature, 403, 430, 10.1038/35000212

Deyama, 2007, Involvement of the bed nucleus of the stria terminalis in the negative affective component of visceral and somatic pain in rats, Behav Brain Res, 176, 367, 10.1016/j.bbr.2006.10.021

Deyama, 2009, Role of enhanced noradrenergic transmission within the ventral bed nucleus of the stria terminalis in visceral pain-induced aversion in rats, Behav Brain Res, 197, 279, 10.1016/j.bbr.2008.08.024

Deyama, 2008, Activation of the beta-adrenoceptor-protein kinase A signaling pathway within the ventral bed nucleus of the stria terminalis mediates the negative affective component of pain in rats, J Neurosci, 28, 7728, 10.1523/JNEUROSCI.1480-08.2008

Dong, 2004, Organization of axonal projections from the anterolateral area of the bed nuclei of the stria terminalis, J Comp Neurol, 468, 277, 10.1002/cne.10949

Dong, 2000, Organization of projections from the juxtacapsular nucleus of the BST: a PHAL study in the rat, Brain Res, 859, 1, 10.1016/S0006-8993(99)02246-5

Dong, 2001, Topography of projections from amygdala to bed nuclei of the stria terminalis, Brain Res Brain Res Rev, 38, 192, 10.1016/S0165-0173(01)00079-0

Dong, 2001, Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain, J Comp Neurol, 436, 430, 10.1002/cne.1079

Dong, 2004, Cocaine-induced potentiation of synaptic strength in dopamine neurons: behavioral correlates in GluRA(−/−) mice, Proc Natl Acad Sci U S A, 101, 14282, 10.1073/pnas.0401553101

Dumont, 2004, Noradrenaline triggers GABAA inhibition of bed nucleus of the stria terminalis neurons projecting to the ventral tegmental area, J Neurosci, 24, 8198, 10.1523/JNEUROSCI.0425-04.2004

Dumont, 2005, Self-administration enhances excitatory synaptic transmission in the bed nucleus of the stria terminalis, Nat Neurosci, 8, 413, 10.1038/nn1414

Dumont, 2008, Morphine produces circuit-specific neuroplasticity in the bed nucleus of the stria terminalis, Neuroscience, 153, 232, 10.1016/j.neuroscience.2008.01.039

Dunn, 1987, Plasma corticosterone responses to electrical stimulation of the bed nucleus of the stria terminalis, Brain Res, 407, 327, 10.1016/0006-8993(87)91111-5

Dziedzicka-Wasylewska, 2006, Effect of antidepressant drugs in mice lacking the norepinephrine transporter, Neuropsychopharmacology, 31, 2424, 10.1038/sj.npp.1301064

Egli, 2003, Dorsal and ventral distribution of excitable and synaptic properties of neurons of the bed nucleus of the stria terminalis, J Neurophysiol, 90, 405, 10.1152/jn.00228.2003

Egli, 2005, Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis, Neuropsychopharmacology, 30, 657, 10.1038/sj.npp.1300639

Eiler, 2003, D1 dopamine receptor regulates alcohol-motivated behaviors in the bed nucleus of the stria terminalis in alcohol-preferring (P) rats, Synapse, 48, 45, 10.1002/syn.10181

Epping-Jordan, 1998, The dopamine D-1 receptor antagonist SCH 23390 injected into the dorsolateral bed nucleus of the stria terminalis decreased cocaine reinforcement in the rat, Brain Res, 784, 105, 10.1016/S0006-8993(97)01190-6

Erb, 2000, Alpha-2 adrenergic receptor agonists block stress-induced reinstatement of cocaine seeking, Neuropsychopharmacology, 23, 138, 10.1016/S0893-133X(99)00158-X

Fendt, 2005, Noradrenaline transmission within the ventral bed nucleus of the stria terminalis is critical for fear behavior induced by trimethylthiazoline, a component of fox odor, J Neurosci, 25, 5998, 10.1523/JNEUROSCI.1028-05.2005

Forray, 2004, Role of noradrenergic projections to the bed nucleus of the stria terminalis in the regulation of the hypothalamic-pituitary-adrenal axis, Brain Res Brain Res Rev, 47, 145, 10.1016/j.brainresrev.2004.07.011

Fu, 2007, Long-term potentiation (LTP) in the central amygdala (CeA) is enhanced after prolonged withdrawal from chronic cocaine and requires CRF1 receptors, J Neurophysiol, 97, 937, 10.1152/jn.00349.2006

George, 1990, Alcoholism and panic disorder: is the comorbidity more than coincidence?, Acta Psychiatr Scand, 81, 97, 10.1111/j.1600-0447.1990.tb06460.x

Georges, 2002, Activation of ventral tegmental area cells by the bed nucleus of the stria terminalis: a novel excitatory amino acid input to midbrain dopamine neurons, J Neurosci, 22, 5173, 10.1523/JNEUROSCI.22-12-05173.2002

Gordon, 2003, Priming of excitatory synapses by alpha1 adrenoceptor-mediated inhibition of group III metabotropic glutamate receptors, J Neurosci, 23, 6223, 10.1523/JNEUROSCI.23-15-06223.2003

Gordon, 2005, Noradrenaline triggers multivesicular release at glutamatergic synapses in the hypothalamus, J Neurosci, 25, 11385, 10.1523/JNEUROSCI.2378-05.2005

Gordon, 2005, Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy, Nat Neurosci, 8, 1078, 10.1038/nn1498

Grueter, 2005, Group II and III metabotropic glutamate receptors suppress excitatory synaptic transmission in the dorsolateral bed nucleus of the stria terminalis, Neuropsychopharmacology, 30, 1302, 10.1038/sj.npp.1300672

Grueter, 2006, Extracellular-signal regulated kinase 1-dependent metabotropic glutamate receptor 5-induced long-term depression in the bed nucleus of the stria terminalis is disrupted by cocaine administration, J Neurosci, 26, 3210, 10.1523/JNEUROSCI.0170-06.2006

Grueter, 2007, Group I mGluRs and long-term depression: potential roles in addiction?, Mol Neurobiol, 36, 232, 10.1007/s12035-007-0037-7

Grueter, 2008, In vivo metabotropic glutamate receptor 5 (mGluR5) antagonism prevents cocaine-induced disruption of postsynaptically maintained mGluR5-dependent long-term depression, J Neurosci, 28, 9261, 10.1523/JNEUROSCI.2886-08.2008

Hall, 2002, Cocaine mechanisms: enhanced cocaine, fluoxetine and nisoxetine place preferences following monoamine transporter deletions, Neuroscience, 115, 153, 10.1016/S0306-4522(02)00379-2

Hammack, 2007, Differential expression of intrinsic membrane currents in defined cell types of the anterolateral bed nucleus of the stria terminalis, J Neurophysiol, 98, 638, 10.1152/jn.00382.2007

Hasue, 2002, Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: a combined retrograde tracing and immunohistochemical study in the rat, J Comp Neurol, 454, 15, 10.1002/cne.10420

Healey, 2008, Chronic ethanol exposure leads to divergent control of dopaminergic synapses in distinct target regions, Alcohol, 42, 179, 10.1016/j.alcohol.2008.01.003

Herrero, 2008, Psychiatric comorbidity in young cocaine users: induced versus independent disorders, Addiction, 103, 284, 10.1111/j.1360-0443.2007.02076.x

Herring, 2004, Ethanol-induced Fos immunoreactivity in the extended amygdala and hypothalamus of the rat brain: focus on cholinergic interneurons of the nucleus accumbens, Alcohol Clin Exp Res, 28, 588, 10.1097/01.ALC.0000122765.58324.6D

Herzig, 2004, Effects of MPEP on locomotion, sensitization and conditioned reward induced by cocaine or morphine, Neuropharmacology, 47, 973, 10.1016/j.neuropharm.2004.07.037

Herzig, 2005, Effects of MPEP on expression of food-, MDMA- or amphetamine-conditioned place preference in rats, Addict Biol, 10, 243, 10.1080/13556210500223272

Kash, 2006, Neuropeptide Y and corticotropin-releasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis, Neuropharmacology, 51, 1013, 10.1016/j.neuropharm.2006.06.011

Kash, 2008, Alcohol inhibits NR2B-containing NMDA receptors in the ventral bed nucleus of the stria terminalis, Neuropsychopharmacology, 33, 1379, 10.1038/sj.npp.1301504

Kash, 2008, Dopamine enhances fast excitatory synaptic transmission in the extended amygdala by a CRF-R1-dependent process, J Neurosci, 28, 13856, 10.1523/JNEUROSCI.4715-08.2008

Kauer, 2007, Synaptic plasticity and addiction, Nat Rev Neurosci, 8, 844, 10.1038/nrn2234

Keller, 2006, Norepinephrine transporter-deficient mice respond to anxiety producing and fearful environments with bradycardia and hypotension, Neuroscience, 139, 931, 10.1016/j.neuroscience.2006.01.008

Kirkwood, 1999, Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine, J Neurosci, 19, 1599, 10.1523/JNEUROSCI.19-05-01599.1999

Knapp, 2001, Regional specificity of ethanol and NMDA action in brain revealed with FOS-like immunohistochemistry and differential routes of drug administration, Alcohol Clin Exp Res, 25, 1662, 10.1111/j.1530-0277.2001.tb02173.x

Kushner, 2000, The relationship between anxiety disorders and alcohol use disorders: a review of major perspectives and findings, Clin Psychol Rev, 20, 149, 10.1016/S0272-7358(99)00027-6

Lahdesmaki, 2002, Behavioral and neurochemical characterization of alpha(2A)-adrenergic receptor knockout mice, Neuroscience, 113, 289, 10.1016/S0306-4522(02)00185-9

Larriva-Sahd, 2006, Histological and cytological study of the bed nuclei of the stria terminalis in adult rat. II. Oval nucleus: extrinsic inputs, cell types, neuropil, and neuronal modules, J Comp Neurol, 497, 772, 10.1002/cne.21011

Lee, 1997, Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex, J Neurosci, 17, 6434, 10.1523/JNEUROSCI.17-16-06434.1997

Liu, 2004, Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity, Science, 304, 1021, 10.1126/science.1096615

Malenka, 2004, LTP and LTD: an embarrassment of riches, Neuron, 44, 5, 10.1016/j.neuron.2004.09.012

Mallon, 2005, Selective subunit antagonists suggest an inhibitory relationship between NR2B and NR2A-subunit containing N-methyl-D: -aspartate receptors in hippocampal slices, Exp Brain Res, 162, 374, 10.1007/s00221-004-2193-6

Malsbury, 1987, A sex difference in the pattern of substance P-like immunoreactivity in the bed nucleus of the stria terminalis, Brain Res, 420, 365, 10.1016/0006-8993(87)91258-3

Massey, 2004, Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression, J Neurosci, 24, 7821, 10.1523/JNEUROSCI.1697-04.2004

Massi, 2008, Cannabinoid receptors in the bed nucleus of the stria terminalis control cortical excitation of midbrain dopamine cells in vivo, J Neurosci, 28, 10496, 10.1523/JNEUROSCI.2291-08.2008

McDonald, 1983, Neurons of the bed nucleus of the stria terminalis: a golgi study in the rat, Brain Res Bull, 10, 111, 10.1016/0361-9230(83)90082-5

McDonald, 1998, Cortical pathways to the mammalian amygdala, Prog Neurobiol, 55, 257, 10.1016/S0301-0082(98)00003-3

McElligott, 2008, Alpha1-adrenergic receptor-induced heterosynaptic long-term depression in the bed nucleus of the stria terminalis is disrupted in mouse models of affective disorders, Neuropsychopharmacology, 33, 2313, 10.1038/sj.npp.1301635

McGeehan, 2003, The mGluR5 antagonist MPEP reduces the conditioned rewarding effects of cocaine but not other drugs of abuse, Synapse, 47, 240, 10.1002/syn.10166

Meloni, 2006, Role of the bed nucleus of the stria terminalis (BST) in the expression of conditioned fear, Ann N Y Acad Sci, 1071, 538, 10.1196/annals.1364.059

Newman-Tancredi, 1998, Actions of alpha2 adrenoceptor ligands at alpha2A and 5-HT1A receptors: the antagonist, atipamezole, and the agonist, dexmedetomidine, are highly selective for alpha2A adrenoceptors, Naunyn Schmiedebergs Arch Pharmacol, 358, 197, 10.1007/PL00005243

Olson, 2006, Role of noradrenergic signaling by the nucleus tractus solitarius in mediating opiate reward, Science, 311, 1017, 10.1126/science.1119311

Pacak, 1995, Effects of immobilization on in vivo release of norepinephrine in the bed nucleus of the stria terminalis in conscious rats, Brain Res, 688, 242, 10.1016/0006-8993(95)00566-9

Pernow, 1988, Co-release and functional interactions of neuropeptide Y and noradrenaline in peripheral sympathetic vascular control, Acta Physiol Scand Suppl, 568, 1

Powell, 2005, Yohimbine disrupts prepulse inhibition in rats via action at 5-HT1A receptors, not alpha2-adrenoceptors, Psychopharmacology (Berl), 180, 491, 10.1007/s00213-005-2193-7

Rainnie, 1999, Neurons of the bed nucleus of the stria terminalis (BNST). Electrophysiological properties and their response to serotonin, Ann N Y Acad Sci, 877, 695, 10.1111/j.1749-6632.1999.tb09304.x

Ricardo, 1978, Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat, Brain Res, 153, 1, 10.1016/0006-8993(78)91125-3

Riegel, 2008, CRF facilitates calcium release from intracellular stores in midbrain dopamine neurons, Neuron, 57, 559, 10.1016/j.neuron.2007.12.029

Rodaros, 2007, Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area, Neuroscience, 150, 8, 10.1016/j.neuroscience.2007.09.043

Saal, 2003, Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons, Neuron, 37, 577, 10.1016/S0896-6273(03)00021-7

Sakanaka, 1986, Distribution and efferent projections of corticotropin-releasing factor-like immunoreactivity in the rat amygdaloid complex, Brain Res, 382, 213, 10.1016/0006-8993(86)91332-6

Sareen, 2006, Illicit drug use and anxiety disorders: findings from two community surveys, Psychiatry Res, 142, 11, 10.1016/j.psychres.2006.01.009

Sawada, 1981, Postsynaptic inhibitory actions of catecholamines and opioid peptides in the bed nucleus of the stria terminalis, Exp Brain Res, 41, 264, 10.1007/BF00238883

Sawchenko, 1985, Colocalization of neuropeptide Y immunoreactivity in brainstem catecholaminergic neurons that project to the paraventricular nucleus of the hypothalamus, J Comp Neurol, 241, 138, 10.1002/cne.902410203

Scheiderer, 2004, Novel form of long-term synaptic depression in rat hippocampus induced by activation of alpha 1 adrenergic receptors, J Neurophysiol, 91, 1071, 10.1152/jn.00420.2003

Schramm, 2001, The alpha(2a)-adrenergic receptor plays a protective role in mouse behavioral models of depression and anxiety, J Neurosci, 21, 4875, 10.1523/JNEUROSCI.21-13-04875.2001

Schulz, 2000, Lesion of the bed nucleus of the stria terminalis enhances learned despair, Brain Res Bull, 52, 83, 10.1016/S0361-9230(00)00235-5

Shaham, 2000, Stress-induced relapse to heroin and cocaine seeking in rats: a review, Brain Res Brain Res Rev, 33, 13, 10.1016/S0165-0173(00)00024-2

Sullivan, 2004, Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus, Neuroscience, 128, 7, 10.1016/j.neuroscience.2004.06.015

Thompson, 2005, Cocaine-induced modulation of long-term potentiation in the CA1 region of rat hippocampus, Neuropharmacology, 49, 185, 10.1016/j.neuropharm.2005.03.005

Ungless, 2001, Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons, Nature, 411, 583, 10.1038/35079077

Valjent, 2004, Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain, Eur J Neurosci, 19, 1826, 10.1111/j.1460-9568.2004.03278.x

Vik, 2007, Methamphetamine use by incarcerated women: comorbid mood and anxiety problems, Womens Health Issues, 17, 256, 10.1016/j.whi.2006.12.004

Waddell, 2006, Effects of bed nucleus of the stria terminalis lesions on conditioned anxiety: aversive conditioning with long-duration conditional stimuli and reinstatement of extinguished fear, Behav Neurosci, 120, 324, 10.1037/0735-7044.120.2.324

Walker, 1997, Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear, J Neurosci, 17, 9375, 10.1523/JNEUROSCI.17-23-09375.1997

Walker, 2000, Microinjections of an opiate receptor antagonist into the bed nucleus of the stria terminalis suppress heroin self-administration in dependent rats, Brain Res, 854, 85, 10.1016/S0006-8993(99)02288-X

Walter, 1991, Differential distribution of immunohistochemical markers in the bed nucleus of the stria terminalis in the human brain, J Chem Neuroanat, 4, 281, 10.1016/0891-0618(91)90019-9

Wanat, 2008, Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih, J Physiol, 586, 2157, 10.1113/jphysiol.2007.150078

Wang, 2001, Noradrenaline in the bed nucleus of the stria terminalis is critical for stress-induced reactivation of morphine-conditioned place preference in rats, Eur J Pharmacol, 432, 153, 10.1016/S0014-2999(01)01487-X

Weitlauf, 2004, High-frequency stimulation induces ethanol-sensitive long-term potentiation at glutamatergic synapses in the dorsolateral bed nucleus of the stria terminalis, J Neurosci, 24, 5741, 10.1523/JNEUROSCI.1181-04.2004

Weitlauf, 2005, Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptor-dependent long-term potentiation, J Neurosci, 25, 8386, 10.1523/JNEUROSCI.2388-05.2005

Weinshenker, 2007, There and back again: a tale of norepinephrine and drug addiction, Neuropsychopharmacology, 32, 1433, 10.1038/sj.npp.1301263

Whitlock, 2006, Learning induces long-term potentiation in the hippocampus, Science, 313, 1093, 10.1126/science.1128134

Wise, 1998, Drug-activation of brain reward pathways, Drug Alcohol Depend, 51, 13, 10.1016/S0376-8716(98)00063-5

Wolf, 1998, The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants, Prog Neurobiol, 54, 679, 10.1016/S0301-0082(97)00090-7

Woulfe, 1988, Collateral axonal projections from the A1 noradrenergic cell group to the paraventricular nucleus and bed nucleus of the stria terminalis in the rat, Exp Neurol, 102, 121, 10.1016/0014-4886(88)90084-2

Xu, 2000, Mice lacking the norepinephrine transporter are supersensitive to psychostimulants, Nat Neurosci, 3, 465, 10.1038/74839