Skip to main content
SpringerLink
Log in

The comparative distributions of the monoamine transporters in the rodent, monkey, and human amygdala

  • Review
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The monoamines in the amygdala modulate multiple aspects of emotional processing in the mammalian brain, and organic or pharmacological dysregulation of these systems can result in affective pathologies. Knowledge of the normal distribution of these neurotransmitters, therefore, is central to our understanding of both the normal processes regulated by the amygdala and the pathological conditions associated with monoaminergic dysregulation. The monoaminergic transporters have proven to be accurate and reliable markers of the distributions of their substrates. The purpose of this review was twofold: First, to briefly recount the functional relevance of dopamine, serotonin, and norepinephrine transmission in the amygdala, and second, to describe and compare the distributions of the monoamine transporters in the rodent, monkey, and human brain. The transporters were found to be heterogeneously distributed in the amygdala. The dopamine transporter (DAT) is consistently found to be extremely sparsely distributed, however the various accounts of its subregional topography are inconsistent, making any cross-species comparisons difficult. The serotonin transporter (SERT) had the greatest overall degree of labeling of the three markers, and was characterized by substantial inter-species variability in its relative distribution. The norepinephrine transporter (NET) was shown to possess an intermediate level of labeling, and like the SERT, its distribution is not consistent across the three species. The results of these comparisons indicate that caution should be exercised when using animal models to investigate the complex processes modulated by the monoamines in the amygdala, as their relative contributions to these functions may differ across species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abercrombie HC, Schaefer SM, Larson CL, Oakes TR, Lindgren KA, Holden JE, Perlman SB, Turski PA, Krahn DD, Benca RM, Davidson RJ (1998) Metabolic rate in the right amygdala predicts negative affect in depressed patients. Neuroreport 9:3301–3307

    Article  PubMed  CAS  Google Scholar 

  • Adolphs R (2003) Is the human amygdala specialized for processing social information? Ann N Y Acad Sci 985:326–340

    Article  PubMed  Google Scholar 

  • Adolphs R, Spezio M (2006) Role of the amygdala in processing visual social stimuli. Prog Brain Res 156:363–378

    Article  PubMed  Google Scholar 

  • Aleman A, Kahn RS (2005) Strange feelings: do amygdala abnormalities dysregulate the emotional brain in schizophrenia? Prog Neurobiol 77:283–298

    PubMed  Google Scholar 

  • Alleweireldt AT, Hobbs RJ, Taylor AR, Neisewander JL (2006) Effects of SCH-23390 infused into the amygdala or adjacent cortex and basal ganglia on cocaine seeking and self-administration in rats. Neuropsychopharmacology 31:363–374

    Article  PubMed  CAS  Google Scholar 

  • Altemus M, Smith MA, Diep V, Aulakh CS, Murphy DL (1994) Increased mRNA for corticotrophin releasing hormone in the amygdala of fawn-hooded rats: a potential animal model of anxiety. Anxiety 1:251–257

    PubMed  Google Scholar 

  • Altshuler LL, Bartzokis G, Grieder T, Curran J, Mintz J (1998) Amygdala enlargement in bipolar disorder and hippocampal reduction in schizophrenia: an MRI study demonstrating neuroanatomic specificity. Arch Gen Psychiatry 55:663–664

    Article  PubMed  CAS  Google Scholar 

  • Amaral DG, Price JL, Pitkanen A, Carmichael ST (1992) Anatomical organization of the primate amygdaloid complex. In: Aggleton JP (ed) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York, pp 1–66

    Google Scholar 

  • Apparsundaram S, Schroeter S, Giovanetti E, Blakely RD (1998) Acute regulation of norepinephrine transport: II. PKC-modulated surface expression of human norepinephrine transporter proteins. J Pharmacol Exp Ther 287:744–751

    PubMed  CAS  Google Scholar 

  • Asan E, Yilmazer-Hanke DM, Eliava M, Hantsch M, Lesch KP, Schmitt A (2005) The corticotropin-releasing factor (CRF)-system and monoaminergic afferents in the central amygdala: investigations in different mouse strains and comparison with the rat. Neuroscience 131:953–967

    PubMed  CAS  Google Scholar 

  • Augood SJ, Westmore K, McKenna PJ, Emson PC (1993) Co-expression of dopamine transporter mRNA and tyrosine hydroxylase mRNA in ventral mesencephalic neurones. Brain Res Mol Brain Res 20:328–334

    Article  PubMed  CAS  Google Scholar 

  • Backstrom IT, Marcusson JO (1990) High- and low-affinity [3H]desipramine-binding sites in human postmortem brain tissue. Neuropsychobiology 23:68–73

    Article  PubMed  CAS  Google Scholar 

  • Backstrom IT, Ross SB, Marcusson JO (1989) [3H]desipramine binding to rat brain tissue: binding to both noradrenaline uptake sites and sites not related to noradrenaline neurons. J Neurochem 52:1099–1106

    Article  PubMed  CAS  Google Scholar 

  • Bannon MJ, Whitty CJ (1997) Age-related and regional differences in dopamine transporter mRNA expression in human midbrain. Neurology 48:969–977

    PubMed  CAS  Google Scholar 

  • Bartolo A, Benuzzi F, Nocetti L, Baraldi P, Nichelli P (2006) Humor comprehension and appreciation: an FMRI study. J Cogn Neurosci 18:1789–1798

    Article  PubMed  Google Scholar 

  • Bassett JL, Foote SL (1992) Distribution of corticotropin-releasing factor-like immunoreactivity in squirrel monkey (Saimiri sciureus) amygdala. J Comp Neurol 323:91–102

    Article  PubMed  CAS  Google Scholar 

  • Bauman MD, Amaral DG (2005) The distribution of serotonergic fibers in the macaque monkey amygdala: an immunohistochemical study using antisera to 5-hydroxytryptamine. Neuroscience 136:193–203

    Article  PubMed  CAS  Google Scholar 

  • Belej T, Manji D, Sioutis S, Barros HM, Nobrega JN (1996) Changes in serotonin and norepinephrine uptake sites after chronic cocaine: pre- vs. post-withdrawal effects. Brain Res 736:287–296

    Article  PubMed  CAS  Google Scholar 

  • Benmansour S, Altamirano AV, Jones DJ, Sanchez TA, Gould GG, Pardon M-J, Morilak DA, Frazer A (2004) Regulation of the norepinephrine transporter by chronic administration of antidepressants. Biol Psychiatry 55:313–316

    Article  PubMed  CAS  Google Scholar 

  • Berger B, Gaspar P, Verney C (1991) Dopaminergic innervation of the cerebral cortex: unexpected differences between rodents and primates. Trends Neurosci 14:21–27

    Article  PubMed  CAS  Google Scholar 

  • Berglind WJ, Case JM, Parker MP, Fuchs RA, See RE (2006) Dopamine D1 or D2 receptor antagonism within the basolateral amygdala differentially alters the acquisition of cocaine-cue associations necessary for cue-induced reinstatement of cocaine-seeking. Neuroscience 137:699–706

    Article  PubMed  CAS  Google Scholar 

  • Blakely RD, Ramamoorthy S, Schroeter S, Qian Y, Apparsundaram S, Galli A, DeFelice LJ (1998) Regulated phosphorylation and trafficking of antidepressant-sensitive serotonin transporter proteins. Biol Psychiatry 44:169–178

    Article  PubMed  CAS  Google Scholar 

  • Blanchard V, Raisman-Vozari R, Vyas S, Michel PP, Javoy-Agid F, Uhl G, Agid Y (1994) Differential expression of tyrosine hydroxylase and membrane dopamine transporter genes in subpopulations of dopaminergic neurons of the rat mesencephalon. Brain Res Mol Brain Res 22:29–38

    Article  PubMed  CAS  Google Scholar 

  • Blood AJ, Zatorre RJ (2001) Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc Natl Acad Sci USA 98:11818–11823

    Article  PubMed  CAS  Google Scholar 

  • Boso M, Politi P, Barale F, Enzo E (2006) Neurophysiology and neurobiology of the musical experience. Funct Neurol 21:187–191

    PubMed  Google Scholar 

  • Bowden DM, German DC, Poynter WD (1978) An autoradiographic, semistereotaxic mapping of major projections from locus coeruleus and adjacent nuclei in Macaca mulatta. Brain Res 145:257–276

    Article  PubMed  CAS  Google Scholar 

  • Bowley MP, Drevets WC, Ongur D, Price JL (2002) Low glial numbers in the amygdala in major depressive disorder. Biol Psychiatry 52:404–412

    Article  PubMed  Google Scholar 

  • Bremner JD (2006) The relationship between cognitive and brain changes in posttraumatic stress disorder. Ann NY Acad Sci 1071:80–86

    Article  PubMed  Google Scholar 

  • Bremner JD, Krystal JH, Southwick SM, Charney DS (1995) Functional neuroanatomical correlates of the effects of stress on memory. J Trauma Stress 8:527–553

    PubMed  CAS  Google Scholar 

  • Bremner JD, Krystal JH, Southwick SM, Charney DS (1996) Noradrenergic mechanisms in stress and anxiety: I. Preclinical studies. Synapse 23:28–38

    Article  PubMed  CAS  Google Scholar 

  • Brimberg L, Flaisher-Grinberg S, Schilman EA, Joel D (2007) Strain differences in ‘compulsive’ lever-pressing. Behav Brain Res 179:141–151

    Article  PubMed  Google Scholar 

  • Brown GL, Goodwin FK (1986) Cerebrospinal fluid correlates of suicide attempts and aggression. Ann NY Acad Sci 487:175–188

    Article  PubMed  CAS  Google Scholar 

  • Brown GL, Goodwin FK, Bunney WE Jr (1982) Human aggression and suicide: their relationship to neuropsychiatric diagnoses and serotonin metabolism. Adv Biochem Psychopharmacol 34:287–307

    PubMed  CAS  Google Scholar 

  • Brunet-Gouet E, Decety J (2006) Social brain dysfunctions in schizophrenia: a review of neuroimaging studies. Psychiatry Res 148:75–92

    Article  PubMed  Google Scholar 

  • Castellano C, Cestari V, Cabib S, Puglisi-Allegra S (1994) The effects of morphine on memory consolidation in mice involve both D1 and D2 dopamine receptors. Behav Neural Biol 61:156–161

    Article  PubMed  CAS  Google Scholar 

  • Cecchi M, Khoshbouei H, Morilak DA (2002) Modulatory effects of norepinephrine, acting on alpha 1 receptors in the central nucleus of the amygdala, on behavioral and neuroendocrine responses to acute immobilization stress. Neuropharmacology 43:1139–1147

    Article  PubMed  CAS  Google Scholar 

  • Cervilla JA, Rivera M, Molina E, Torres-Gonzalez F, Bellon JA, Moreno B, de Dios Luna J, Lorente JA, de Diego-Otero Y, King M, Nazareth I, Gutierrez B (2006) The 5-HTTLPR s/s genotype at the serotonin transporter gene (SLC6A4) increases the risk for depression in a large cohort of primary care attendees: the PREDICT-gene study. Am J Med Genet B Neuropsychiatr Genet 141:912–917

    Google Scholar 

  • Chen HT, Clark M, Goldman D (1992) Quantitative autoradiography of 3H-paroxetine binding sites in rat brain. J Pharmacol Toxicol Methods 27:209–216

    Article  PubMed  CAS  Google Scholar 

  • Ciccocioppo R, Sanna PP, Weiss F (2001) Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D(1) antagonists. Proc Natl Acad Sci USA 98:1976–1981

    Article  PubMed  CAS  Google Scholar 

  • Ciliax BJ, Heilman C, Demchyshyn LL, Pristupa ZB, Ince E, Hersch SM, Niznik HB, Levey AI (1995) The dopamine transporter: immunochemical characterization and localization in brain. J Neurosci 15:1714–1723

    PubMed  CAS  Google Scholar 

  • Ciliax BJ, Drash GW, Staley JK, Haber S, Mobley CJ, Miller GW, Mufson EJ, Mash DC, Levey AI (1999) Immunocytochemical localization of the dopamine transporter in human brain. J Comp Neurol 409:38–56

    Article  PubMed  CAS  Google Scholar 

  • Cortes R, Soriano E, Pazos A, Probst A, Palacios JM (1988) Autoradiography of antidepressant binding sites in the human brain: localization using [3H]imipramine and [3H]paroxetine. Neuroscience 27:473–496

    Article  PubMed  CAS  Google Scholar 

  • D’Amato RJ, Largent BL, Snowman AM, Snyder SH (1987) Selective labeling of serotonin uptake sites in rat brain by [3H]citalopram contrasted to labeling of multiple sites by [3H]imipramine. J Pharmacol Exp Ther 242:364–371

    PubMed  CAS  Google Scholar 

  • Daniels GM, Amara SG (1999) Regulated trafficking of the human dopamine transporter. Clathrin-mediated internalization and lysosomal degradation in response to phorbol esters. J Biol Chem 274:35794–35801

    Article  PubMed  CAS  Google Scholar 

  • Dannlowski U, Ohrmann P, Bauer J, Kugel H, Baune BT, Hohoff C, Kersting A, Arolt V, Heindel W, Deckert J, Suslow T (2007) Serotonergic genes modulate amygdala activity in major depression. Genes Brain Behav 6(7):672–676

    Article  PubMed  CAS  Google Scholar 

  • Dannlowski U, Ohrmann P, Bauer J, Deckert J, Hohoff C, Kugel H, Arolt V, Heindel W, Kersting A, Baune BT, Suslow T (2008) 5-HTTLPR biases amygdala activity in response to masked facial expressions in major depression. Neuropsychopharmacology 33(2):418–424

    Article  PubMed  CAS  Google Scholar 

  • Daunais JB, Letchworth SR, Sim-Selley LJ, Smith HR, Childers SR, Porrino LJ (2001) Functional and anatomical localization of mu opioid receptors in the striatum, amygdala, and extended amygdala of the nonhuman primate. J Comp Neurol 433:471–485

    Article  PubMed  CAS  Google Scholar 

  • De La Garza R 2nd, Meltzer PC, Madras BK (1999) Non-amine dopamine transporter probe [(3)H]tropoxene distributes to dopamine-rich regions of monkey brain. Synapse 34:20–27

    Article  PubMed  Google Scholar 

  • De Souza EB, Kuyatt BL (1987) Autoradiographic localization of 3H-paroxetine-labeled serotonin uptake sites in rat brain. Synapse 1:488–496

    Article  PubMed  Google Scholar 

  • Debiec J, Ledoux JE (2004) Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala. Neuroscience 129:267–272

    Article  PubMed  CAS  Google Scholar 

  • Debiec J, LeDoux JE (2006) Noradrenergic signaling in the amygdala contributes to the reconsolidation of fear memory: treatment implications for PTSD. Ann NY Acad Sci 1071:521–524

    Article  PubMed  CAS  Google Scholar 

  • Delgado PL (2000) Depression: the case for a monoamine deficiency. J Clin Psychiatry 61(Suppl 6):7–11

    PubMed  CAS  Google Scholar 

  • Delgado PL, Moreno FA (2000) Role of norepinephrine in depression. J Clin Psychiatry 61(Suppl 1):5–12

    PubMed  CAS  Google Scholar 

  • Dersch CM, Akunne HC, Partilla JS, Char GU, de Costa BR, Rice KC, Carroll FI, Rothman RB (1994) Studies of the biogenic amine transporters. 1. Dopamine reuptake blockers inhibit [3H]mazindol binding to the dopamine transporter by a competitive mechanism: preliminary evidence for different binding domains. Neurochem Res 19:201–208

    Article  PubMed  CAS  Google Scholar 

  • Di Ciano P, Everitt BJ (2004) Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats. J Neurosci 24:7167–7173

    Article  PubMed  CAS  Google Scholar 

  • Domschke K, Braun M, Ohrmann P, Suslow T, Kugel H, Bauer J, Hohoff C, Kersting A, Engelien A, Arolt V, Heindel W, Deckert J (2006) Association of the functional -1019C/G 5-HT1A polymorphism with prefrontal cortex and amygdala activation measured with 3 T fMRI in panic disorder. Int J Neuropsychopharmacol 9:349–355

    Article  PubMed  CAS  Google Scholar 

  • Donnan GA, Kaczmarczyk SJ, Paxinos G, Chilco PJ, Kalnins RM, Woodhouse DG, Mendelsohn FA (1991) Distribution of catecholamine uptake sites in human brain as determined by quantitative [3H] mazindol autoradiography. J Comp Neurol 304:419–434

    Article  PubMed  CAS  Google Scholar 

  • Dorado P, Penas-Lledo EM, Gonzalez AP, Caceres MC, Cobaleda J, Llerena A (2007) Increased risk for major depression associated with the short allele of the serotonin transporter promoter region (5-HTTLPR-S) and the CYP2C9*3 allele. Fundam Clin Pharmacol 21:451–453

    Article  PubMed  CAS  Google Scholar 

  • Drevets WC, Raichle ME (1992) Neuroanatomical circuits in depression: implications for treatment mechanisms. Psychopharmacol Bull 28:261–274

    PubMed  CAS  Google Scholar 

  • DuBois DW, Perlegas A, Floyd DW, Weiner JL, McCool BA (2006) Distinct functional characteristics of the lateral/basolateral amygdala GABAergic system in C57BL/6J and DBA/2J mice. J Pharmacol Exp Ther 318:629–640

    Article  PubMed  CAS  Google Scholar 

  • Duncan GE, Little KY, Kirkman JA, Kaldas RS, Stumpf WE, Breese GR (1992) Autoradiographic characterization of [3H]imipramine and [3H]citalopram binding in rat and human brain: species differences and relationships to serotonin innervation patterns. Brain Res 591:181–197

    Article  PubMed  CAS  Google Scholar 

  • Eldar E, Ganor O, Admon R, Bleich A, Hendler T (2007) Feeling the real world: limbic response to music depends on related content. Cereb Cortex 17(12):2828–2840

    Article  PubMed  Google Scholar 

  • Elkins RL, Orr TE, Rausch JL, Fei YJ, Carl GF, Hobbs SH, Buccafusco JJ, Edwards GL (2003) Cocaine-induced expression differences in glutamate receptor subunits and transporters in amygdalae of taste aversion-prone and taste aversion-resistant rats. Ann NY Acad Sci 1003:381–385

    Article  PubMed  CAS  Google Scholar 

  • Erb S, Hitchcott PK, Rajabi H, Mueller D, Shaham Y, Stewart J (2000) Alpha-2 adrenergic receptor agonists block stress-induced reinstatement of cocaine seeking. Neuropsychopharmacology 23:138–150

    Article  PubMed  CAS  Google Scholar 

  • Evans KC, Wright CI, Wedig MM, Gold AL, Pollack MH, Rauch SL (2007) A functional MRI study of amygdala responses to angry schematic faces in social anxiety disorder. Depress Anxiety [Epub ahead of print]

  • Fallon J, Ciofi P (1992) Distribution of monoamines within the amygdala. In: Aggleton JP (ed) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York, pp 97–114

    Google Scholar 

  • Fallon JH, Koziell DA, Moore RY (1978) Catecholamine innervation of the basal forebrain. II. Amygdala, suprarhinal cortex and entorhinal cortex. J Comp Neurol 180:509–532

    Article  PubMed  CAS  Google Scholar 

  • Farley IJ, Hornykiewicz O (1977) Noradrenaline distribution insubcortical areas of the human brain. Brain Res 126:53–62

    Article  PubMed  CAS  Google Scholar 

  • Ferry B, Roozendaal B, McGaugh JL (1999a) Basolateral amygdala noradrenergic influences on memory storage are mediated by an interaction between beta- and alpha1-adrenoceptors. J Neurosci 19:5119–5123

    PubMed  CAS  Google Scholar 

  • Ferry B, Roozendaal B, McGaugh JL (1999b) Role of norepinephrine in mediating stress hormone regulation of long-term memory storage: a critical involvement of the amygdala. Biol Psychiatry 46:1140–1152

    Article  PubMed  CAS  Google Scholar 

  • Freedman LJ, Cassell MD (1994) Distribution of dopaminergic fibers in the central division of the extended amygdala of the rat. Brain Res 633:243–252

    Article  PubMed  CAS  Google Scholar 

  • Freedman LJ, Shi C (2001) Monoaminergic innervation of the macaque extended amygdala. Neuroscience 104:1067–1084

    Article  PubMed  CAS  Google Scholar 

  • Fujita M, Shimada S, Fukuchi K, Tohyama M, Nishimura T (1994) Distribution of cocaine recognition sites in rat brain: in vitro and ex vivo autoradiography with [125I]RTI-55. J Chem Neuroanat 7:13–23

    Article  PubMed  CAS  Google Scholar 

  • Furmark T, Tillfors M, Garpenstrand H, Marteinsdottir I, Langstrom B, Oreland L, Fredrikson M (2004) Serotonin transporter polymorphism related to amygdala excitability and symptom severity in patients with social phobia. Neurosci Lett 362:189–192

    Article  PubMed  CAS  Google Scholar 

  • Fuxe K, Jacobsen KX, Hoistad M, Tinner B, Jansson A, Staines WA, Agnati LF (2003) The dopamine D1 receptor-rich main and paracapsular intercalated nerve cell groups of the rat amygdala: relationship to the dopamine innervation. Neuroscience 119:733–746

    Article  PubMed  CAS  Google Scholar 

  • Garris PA, Wightman RM (1994) Different kinetics govern dopaminergic transmission in the amygdala, prefrontal cortex, and striatum: an in vivo voltammetric study. J Neurosci 14:442–450

    PubMed  CAS  Google Scholar 

  • Gonzalez-Hernandez T, Barroso-Chinea P, De La Cruz Muros I, Del Mar Perez-Delgado M, Rodriguez M (2004) Expression of dopamine and vesicular monoamine transporters and differential vulnerability of mesostriatal dopaminergic neurons. J Comp Neurol 479:198–215

    Article  PubMed  CAS  Google Scholar 

  • Gosselin N, Peretz I, Johnsen E, Adolphs R (2007) Amygdala damage impairs emotion recognition from music. Neuropsychologia 45:236–244

    Article  PubMed  Google Scholar 

  • Gothard KM, Battaglia FP, Erickson CA, Spitler KM, Amaral DG (2007) Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 97:1671–1683

    Article  PubMed  CAS  Google Scholar 

  • Greba Q, Kokkinidis L (2000) Peripheral and intraamygdalar administration of the dopamine D1 receptor antagonist SCH 23390 blocks fear-potentiated startle but not shock reactivity or the shock sensitization of acoustic startle. Behav Neurosci 114:262–272

    Article  PubMed  CAS  Google Scholar 

  • Gross-Isseroff R, Israeli M, Biegon A (1988) Autoradiographic analysis of [3H]desmethylimipramine binding in the human brain postmortem. Brain Res 456:120–126

    Article  PubMed  CAS  Google Scholar 

  • Guarraci FA, Frohardt RJ, Kapp BS (1999) Amygdaloid D1 dopamine receptor involvement in Pavlovian fear conditioning. Brain Res 827:28–40

    Article  PubMed  CAS  Google Scholar 

  • Guitart-Masip M, Johansson B, Fernandez-Teruel A, Canete T, Tobena A, Terenius L, Gimenez-Llort L (2006) Divergent anatomical pattern of D1 and D3 binding and dopamine- and cyclic AMP-regulated phosphoprotein of 32 kDa mRNA expression in the Roman rat strains: implications for drug addiction. Neuroscience 142:1231–1243

    Article  PubMed  CAS  Google Scholar 

  • Gurevich EV, Joyce JN (1996) Comparison of [3H]paroxetine and [3H]cyanoimipramine for quantitative measurement of serotonin transporter sites in human brain. Neuropsychopharmacology 14:309–323

    Article  PubMed  CAS  Google Scholar 

  • Haber SN, Ryoo H, Cox C, Lu W (1995) Subsets of midbrain dopaminergic neurons in monkeys are distinguished by different levels of mRNA for the dopamine transporter: comparison with the mRNA for the D2 receptor, tyrosine hydroxylase and calbindin immunoreactivity. J Comp Neurol 362:400–410

    Article  PubMed  CAS  Google Scholar 

  • Hariri AR, Drabant EM, Munoz KE, Kolachana BS, Mattay VS, Egan MF, Weinberger DR (2005) A susceptibility gene for affective disorders and the response of the human amygdala. Arch Gen Psychiatry 62:146–152

    Article  PubMed  CAS  Google Scholar 

  • Hatfield T, McGaugh JL (1999) Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiol Learn Mem 71:232–239

    Article  PubMed  CAS  Google Scholar 

  • Heberlein AS, Adolphs R (2004) Impaired spontaneous anthropomorphizing despite intact perception and social knowledge. Proc Natl Acad Sci USA 101:7487–7491

    Article  PubMed  CAS  Google Scholar 

  • Heinz A, Braus DF, Smolka MN, Wrase J, Puls I, Hermann D, Klein S, Grusser SM, Flor H, Schumann G, Mann K, Buchel C (2005) Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nat Neurosci 8:20–21

    Article  PubMed  CAS  Google Scholar 

  • Heinz A, Smolka MN, Braus DF, Wrase J, Beck A, Flor H, Mann K, Schumann G, Buchel C, Hariri AR, Weinberger DR (2007) Serotonin transporter genotype (5-HTTLPR): effects of neutral and undefined conditions on amygdala activation. Biol Psychiatry 61:1011–1014

    Article  PubMed  CAS  Google Scholar 

  • Hensler JG, Hodge CW, Overstreet DH (2004) Reduced 5-HT3 receptor binding and lower baseline plus maze anxiety in the alcohol-preferring inbred fawn-hooded rat. Pharmacol Biochem Behav 77:281–289

    Article  PubMed  CAS  Google Scholar 

  • Higley JD, King ST Jr, Hasert MF, Champoux M, Suomi SJ, Linnoila M (1996) Stability of interindividual differences in serotonin function and its relationship to severe aggression and competent social behavior in rhesus macaque females. Neuropsychopharmacology 14:67–76

    Article  PubMed  CAS  Google Scholar 

  • Hipolide DC, Moreira KM, Barlow KB, Wilson AA, Nobrega JN, Tufik S (2005) Distinct effects of sleep deprivation on binding to norepinephrine and serotonin transporters in rat brain. Prog Neuropsychopharmacol Biol Psychiatry 29(2):297–303

    Article  PubMed  CAS  Google Scholar 

  • Hoffman KL, Gothard KM, Schmid MC, Logothetis NK (2007) Facial-expression and gaze-selective responses in the monkey amygdala. Curr Biol 17:766–772

    Article  PubMed  CAS  Google Scholar 

  • Hoover BR, Everett CV, Sorkin A, Zahniser NR (2007) Rapid regulation of dopamine transporters by tyrosine kinases in rat neuronal preparations. J Neurochem 101:1258–1271

    Article  PubMed  CAS  Google Scholar 

  • Hrdina PD, Foy B, Hepner A, Summers RJ (1990) Antidepressant binding sites in brain: autoradiographic comparison of [3H]paroxetine and [3H]imipramine localization and relationship to serotonin transporter. J Pharmacol Exp Ther 252:410–418

    PubMed  CAS  Google Scholar 

  • Huff RA, Vaughan RA, Kuhar MJ, Uhl GR (1997) Phorbol esters increase dopamine transporter phosphorylation and decrease transport Vmax. J Neurochem 68:225–232

    PubMed  CAS  Google Scholar 

  • Hurd YL, Pristupa ZB, Herman MM, Niznik HB, Kleinman JE (1994) The dopamine transporter and dopamine D2 receptor messenger RNAs are differentially expressed in limbic- and motor-related subpopulations of human mesencephalic neurons. Neuroscience 63:357–362

    Article  PubMed  CAS  Google Scholar 

  • Hurlemann R, Hawellek B, Matusch A, Kolsch H, Wollersen H, Madea B, Vogeley K, Maier W, Dolan RJ (2005) Noradrenergic modulation of emotion-induced forgetting and remembering. J Neurosci 25:6343–6349

    Article  PubMed  CAS  Google Scholar 

  • Ida Y, Elsworth JD, Roth RH (1991) Anxiogenic beta-carboline FG 7142 produces activation of noradrenergic neurons in specific brain regions of rats. Pharmacol Biochem Behav 39:791–793

    Article  PubMed  CAS  Google Scholar 

  • Inoue T, Izumi T, Maki Y, Muraki I, Koyama T (2000) Effect of the dopamine D(1/5) antagonist SCH 23390 on the acquisition of conditioned fear. Pharmacol Biochem Behav 66:573–578

    Article  PubMed  CAS  Google Scholar 

  • Javitch JA, Strittmatter SM, Snyder SH (1985) Differential visualization of dopamine and norepinephrine uptake sites in rat brain using [3H]mazindol autoradiography. J Neurosci 5:1513–1521

    PubMed  CAS  Google Scholar 

  • Jiao X, Pare WP, Tejani-Butt S (2003) Strain differences in the distribution of dopamine transporter sites in rat brain. Prog Neuropsychopharmacol Biol Psychiatry 27:913–919

    Article  PubMed  CAS  Google Scholar 

  • Kalia M (2005) Neurobiological basis of depression: an update. Metabolism 54:24–27

    Article  PubMed  CAS  Google Scholar 

  • Kaufman MJ, Spealman RD, Madras BK (1991) Distribution of cocaine recognition sites in monkey brain: I. In vitro autoradiography with [3H]CFT. Synapse 9:177–187

    Article  PubMed  CAS  Google Scholar 

  • Keele NB, Randall DR (2003) Altered modulation of excitatory neurotransmission in the amygdala by serotonin in an animal model of impulsive aggression. Ann NY Acad Sci 985:528–532

    Article  Google Scholar 

  • Khoshbouei H, Cecchi M, Dove S, Javors M, Morilak DA (2002) Behavioral reactivity to stress: amplification of stress-induced noradrenergic activation elicits a galanin-mediated anxiolytic effect in central amygdala. Pharmacol Biochem Behav 71:407–417

    Article  PubMed  CAS  Google Scholar 

  • Kitayama S, Dohi T, Uhl GR (1994) Phorbol esters alter functions of the expressed dopamine transporter. Eur J Pharmacol 268:115–119

    Article  PubMed  CAS  Google Scholar 

  • Klimek V, Schenck JE, Han H, Stockmeier CA, Ordway GA (2002) Dopaminergic abnormalities in amygdaloid nuclei in major depression: a postmortem study. Biol Psychiatry 52:740–748

    Article  PubMed  CAS  Google Scholar 

  • Kovachich GB, Aronson CE, Brunswick DJ, Frazer A (1988) Quantitative autoradiography of serotonin uptake sites in rat brain using [3H]cyanoimipramine. Brain Res 454:78–88

    Article  PubMed  CAS  Google Scholar 

  • Kuraoka K, Nakamura K (2007) Responses of single neurons in monkey amygdala to facial and vocal emotions. J Neurophysiol 97:1379–1387

    Article  PubMed  Google Scholar 

  • LaLumiere RT, Buen TV, McGaugh JL (2003) Post-training intra-basolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. J Neurosci 23:6754–6758

    PubMed  CAS  Google Scholar 

  • LaLumiere RT, Nawar EM, McGaugh JL (2005) Modulation of memory consolidation by the basolateral amygdala or nucleus accumbens shell requires concurrent dopamine receptor activation in both brain regions. Learn Mem 12:296–301

    Article  PubMed  Google Scholar 

  • Lalumiere RT, Nguyen LT, McGaugh JL (2004) Post-training intrabasolateral amygdala infusions of dopamine modulate consolidation of inhibitory avoidance memory: involvement of noradrenergic and cholinergic systems. Eur J Neurosci 20:2804–2810

    Article  PubMed  Google Scholar 

  • Leppanen JM (2006) Emotional information processing in mood disorders: a review of behavioral and neuroimaging findings. Curr Opin Psychiatry 19:34–39

    Article  PubMed  Google Scholar 

  • Leri F, Flores J, Rodaros D, Stewart J (2002) Blockade of stress-induced but not cocaine-induced reinstatement by infusion of noradrenergic antagonists into the bed nucleus of the stria terminalis or the central nucleus of the amygdala. J Neurosci 22:5713–5718

    PubMed  CAS  Google Scholar 

  • Letchworth SR, Smith HR, Porrino LJ, Bennett BA, Davies HM, Sexton T, Childers SR (2000) Characterization of a tropane radioligand, [(3)H]2beta-propanoyl-3beta-(4-tolyl) tropane ([(3)H]PTT), for dopamine transport sites in rat brain. J Pharmacol Exp Ther 293:686–696

    PubMed  CAS  Google Scholar 

  • Liang KC, Chen LL, Huang TE (1995) The role of amygdala norepinephrine in memory formation: involvement in the memory enhancing effect of peripheral epinephrine. Chin J Physiol 38:81–91

    PubMed  CAS  Google Scholar 

  • Liberzon I, Britton JC, Phan KL (2003) Neural correlates of traumatic recall in posttraumatic stress disorder. Stress 6:151–156

    Article  PubMed  Google Scholar 

  • Liberzon I, Taylor SF, Amdur R, Jung TD, Chamberlain KR, Minoshima S, Koeppe RA, Fig LM (1999) Brain activation in PTSD in response to trauma-related stimuli. Biol Psychiatry 45:817–826

    Article  PubMed  CAS  Google Scholar 

  • Little KY, Carroll FI, Cassin BJ (1995) Characterization and localization of [125I]RTI-121 binding sites in human striatum and medial temporal lobe. J Pharmacol Exp Ther 274:1473–1483

    PubMed  CAS  Google Scholar 

  • Lorang D, Amara SG, Simerly RB (1994) Cell-type-specific expression of catecholamine transporters in the rat brain. J Neurosci 14:4903–4914

    PubMed  CAS  Google Scholar 

  • Macedo CE, Martinez RC, Albrechet-Souza L, Molina VA, Brandao ML (2007) 5-HT2- and D1-mechanisms of the basolateral nucleus of the amygdala enhance conditioned fear and impair unconditioned fear. Behav Brain Res 177:100–108

    Article  PubMed  CAS  Google Scholar 

  • Malison RT, Price LH, Berman R, van Dyck CH, Pelton GH, Carpenter L, Sanacora G, Owens MJ, Nemeroff CB, Rajeevan N, Baldwin RM, Seibyl JP, Innis RB, Charney DS (1998) Reduced brain serotonin transporter availability in major depression as measured by [123I]-2 beta-carbomethoxy-3 beta-(4-iodophenyl)tropane and single photon emission computed tomography. Biol Psychiatry 44:1090–1098

    Article  PubMed  CAS  Google Scholar 

  • Mathew SJ, Ho S (2006) Etiology and neurobiology of social anxiety disorder. J Clin Psychiatry 67(Suppl 12):9–13

    PubMed  CAS  Google Scholar 

  • McGaugh JL (2004) The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27:1–28

    Article  PubMed  CAS  Google Scholar 

  • Mehlman PT, Higley JD, Faucher I, Lilly AA, Taub DM, Vickers J, Suomi SJ, Linnoila M (1994) Low CSF 5-HIAA concentrations and severe aggression and impaired impulse control in nonhuman primates. Am J Psychiatry 151:1485–1491

    PubMed  CAS  Google Scholar 

  • Melchitzky DS, Lewis DA (2001) Dopamine transporter-immunoreactive axons in the mediodorsal thalamic nucleus of the macaque monkey. Neuroscience 103:1033–1042

    Article  PubMed  CAS  Google Scholar 

  • Meoni P, Bunnemann BH, Trist DG, Bowery NG (1998) N-terminal splice variants of the NMDAR1 glutamate receptor subunit: differential expression in human and monkey brain. Neurosci Lett 249:45–48

    Article  PubMed  CAS  Google Scholar 

  • Meyer M, Baumann S, Wildgruber D, Alter K (2007) How the brain laughs. Comparative evidence from behavioral, electrophysiological and neuroimaging studies in human and monkey. Behav Brain Res 182(2):245–260

    Article  PubMed  Google Scholar 

  • Miczek KA, Weerts E, Haney M, Tidey J (1994) Neurobiological mechanisms controlling aggression: preclinical developments for pharmacotherapeutic interventions. Neurosci Biobehav Rev 18:97–110

    Article  PubMed  CAS  Google Scholar 

  • Miller GM, Yatin SM, De La Garza R 2nd, Goulet M, Madras BK (2001) Cloning of dopamine, norepinephrine and serotonin transporters from monkey brain: relevance to cocaine sensitivity. Brain Res Mol Brain Res 87:124–143

    Article  PubMed  CAS  Google Scholar 

  • Miranda MI, LaLumiere RT, Buen TV, Bermudez-Rattoni F, McGaugh JL (2003) Blockade of noradrenergic receptors in the basolateral amygdala impairs taste memory. Eur J Neurosci 18:2605–2610

    Article  PubMed  CAS  Google Scholar 

  • Mitterschiffthaler MT, Fu CH, Dalton JA, Andrew CM, Williams SC (2007) A functional MRI study of happy and sad affective states induced by classical music. Hum Brain Mapp 28(11):1150–1162

    Article  PubMed  Google Scholar 

  • Mobbs D, Hagan CC, Azim E, Menon V, Reiss AL (2005) Personality predicts activity in reward and emotional regions associated with humor. Proc Natl Acad Sci USA 102:16502–16506

    Article  PubMed  CAS  Google Scholar 

  • Moore RY, Bloom FE (1978) Central catecholamine neuron systems: anatomy and physiology of the dopamine systems. Annu Rev Neurosci 1:129–169

    Article  PubMed  CAS  Google Scholar 

  • Moore RY, Bloom FE (1979) Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. Ann Rev Neurosci 2:113–168

    Article  PubMed  CAS  Google Scholar 

  • Moran JM, Wig GS, Adams RB Jr, Janata P, Kelley WM (2004) Neural correlates of humor detection and appreciation. Neuroimage 21:1055–1060

    Article  PubMed  Google Scholar 

  • Morilak DA, Barrera G, Echevarria DJ, Garcia AS, Hernandez A, Ma S, Petre CO (2005) Role of brain norepinephrine in the behavioral response to stress. Prog Neuropsychopharmacol Biol Psychiatry 29:1214–1224

    Article  PubMed  CAS  Google Scholar 

  • Nader K, LeDoux JE (1999) Inhibition of the mesoamygdala dopaminergic pathway impairs the retrieval of conditioned fear associations. Behav Neurosci 113:891–901

    Article  PubMed  CAS  Google Scholar 

  • Nadler JJ, Zou F, Huang H, Moy SS, Lauder J, Crawley JN, Threadgill DW, Wright FA, Magnuson TR (2006) Large-scale gene expression differences across brain regions and inbred strains correlate with a behavioral phenotype. Genetics 174:1229–1236

    Article  PubMed  CAS  Google Scholar 

  • Naudts K, Hodgins S (2006) Neurobiological correlates of violent behavior among persons with schizophrenia. Schizophr Bull 32:562–572

    Article  PubMed  Google Scholar 

  • Nemeroff CB, Bremner JD, Foa EB, Mayberg HS, North CS, Stein MB (2006) Posttraumatic stress disorder: a state-of-the-science review. J Psychiatr Res 40:1–21

    Article  PubMed  Google Scholar 

  • Neumeister A, Hu XZ, Luckenbaugh DA, Schwarz M, Nugent AC, Bonne O, Herscovitch P, Goldman D, Drevets WC, Charney DS (2006) Differential effects of 5-HTTLPR genotypes on the behavioral and neural responses to tryptophan depletion in patients with major depression and controls. Arch Gen Psychiatry 63:978–986

    Article  PubMed  CAS  Google Scholar 

  • Newport DJ, Nemeroff CB (2000) Neurobiology of posttraumatic stress disorder. Curr Opin Neurobiol 10:211–218

    Article  PubMed  CAS  Google Scholar 

  • Niehoff DL, Whitehouse PJ (1983) Multiple benzodiazepine receptors: autoradiographic localization in normal human amygdala. Brain Res 276:237–245

    Article  PubMed  CAS  Google Scholar 

  • Ninan PT (1999) The functional anatomy, neurochemistry, and pharmacology of anxiety. J Clin Psychiatry 60(Suppl 22):12–17

    PubMed  CAS  Google Scholar 

  • O’Carroll RE, Drysdale E, Cahill L, Shajahan P, Ebmeier KP (1999) Stimulation of the noradrenergic system enhances and blockade reduces memory for emotional material in man. Psychol Med 29:1083–1088

    Article  PubMed  CAS  Google Scholar 

  • O’Rourke H, Fudge JL (2006) Distribution of serotonin transporter labeled fibers in amygdaloid subregions: implications for mood disorders. Biol Psychiatry 60:479–490

    Article  PubMed  CAS  Google Scholar 

  • Olivier B, Mos J, van Oorschot R, Hen R (1995) Serotonin receptors and animal models of aggressive behavior. Pharmacopsychiatry 28(Suppl 2):80–90

    Article  PubMed  Google Scholar 

  • Ordway GA, Stockmeier CA, Cason GW, Klimek V (1997) Pharmacology and distribution of norepinephrine transporters in the human locus coeruleus and raphe nuclei. J Neurosci 17:1710–1719

    PubMed  CAS  Google Scholar 

  • Owashi T, Iritani S, Niizato K, Ikeda K, Kamijima K (2004) The distribution of serotonin immunoreactivity in the hippocampal formation in monkeys and rats. Brain Res 1010:166–168

    Article  PubMed  CAS  Google Scholar 

  • Owens MJ, Nemeroff CB (1998) The serotonin transporter and depression. Depress Anxiety 8(Suppl 1):5–12

    Article  PubMed  Google Scholar 

  • Parent A, Descarries L, Beaudet A (1981) Organization of ascending serotonin systems in the adult rat brain. A radioautographic study after intraventricular administration of [3H]5-hydroxytryptamine. Neuroscience 6:115–138

    Article  PubMed  CAS  Google Scholar 

  • Patel A, Uhl G, Kuhar MJ (1993) Species differences in dopamine transporters: postmortem changes and glycosylation differences. J Neurochem 61:496–500

    Article  PubMed  CAS  Google Scholar 

  • Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, Egan MF, Mattay VS, Hariri AR, Weinberger DR (2005) 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat Neurosci 8:828–834

    Article  PubMed  CAS  Google Scholar 

  • Phillips ML, Vieta E (2007) Identifying functional neuroimaging biomarkers of bipolar disorder: toward DSM-V. Schizophr Bull 33:893–904

    Article  PubMed  Google Scholar 

  • Phillips ML, Williams L, Senior C, Bullmore ET, Brammer MJ, Andrew C, Williams SC, David AS (1999) A differential neural response to threatening and non-threatening negative facial expressions in paranoid and non-paranoid schizophrenics. Psychiatry Res 92:11–31

    Article  PubMed  CAS  Google Scholar 

  • Pickel VM, Chan J (1999) Ultrastructural localization of the serotonin transporter in limbic and motor compartments of the nucleus accumbens. J Neurosci 19:7356–7366

    PubMed  CAS  Google Scholar 

  • Pitkanen A, Kemppainen S (2002) Comparison of the distribution of calcium-binding proteins and intrinsic connectivity in the lateral nucleus of the rat, monkey, and human amygdala. Pharmacol Biochem Behav 71:369–377

    Article  PubMed  CAS  Google Scholar 

  • Plenge P, Mellerup ET, Laursen H (1990) Regional distribution of the serotonin transport complex in human brain, identified with 3H-paroxetine, 3H-citalopram and 3H-imipramine. Prog Neuropsychopharmacol Biol Psychiatry 14:61–72

    Article  PubMed  CAS  Google Scholar 

  • Pristupa ZB, McConkey F, Liu F, Man HY, Lee FJ, Wang YT, Niznik HB (1998) Protein kinase-mediated bidirectional trafficking and functional regulation of the human dopamine transporter. Synapse 30:79–87

    Article  PubMed  CAS  Google Scholar 

  • Ramamoorthy S, Melikian HE, Qian Y, Blakely RD (1998) Biosynthesis, N-glycosylation, and surface trafficking of biogenic amine transporter proteins. Methods Enzymol 296:347–370

    Article  PubMed  CAS  Google Scholar 

  • Rauch SL, Shin LM, Phelps EA (2006) Neurocircuitry models of posttraumatic stress disorder and extinction: human neuroimaging research—past, present, and future. Biol Psychiatry 60:376–382

    Article  PubMed  Google Scholar 

  • Reis FL, Masson S, de Oliveira AR, Brandao ML (2004) Dopaminergic mechanisms in the conditioned and unconditioned fear as assessed by the two-way avoidance and light switch-off tests. Pharmacol Biochem Behav 79:359–365

    Article  PubMed  CAS  Google Scholar 

  • Reith ME, Xu C, Chen NH (1997) Pharmacology and regulation of the neuronal dopamine transporter. Eur J Pharmacol 324:1–10

    Article  PubMed  CAS  Google Scholar 

  • Remy P, Doder M, Lees A, Turjanski N, Brooks D (2005) Depression in Parkinson’s disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain 128:1314–1322

    Article  PubMed  Google Scholar 

  • Ressler KJ, Nemeroff CB (2000) Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 12(Suppl 1):2–19

    Article  PubMed  Google Scholar 

  • Revay R, Vaughan R, Grant S, Kuhar MJ (1996) Dopamine transporter immunohistochemistry in median eminence, amygdala, and other areas of the rat brain. Synapse 22:93–99

    Article  PubMed  CAS  Google Scholar 

  • Roozendaal B, Nguyen BT, Power AE, McGaugh JL (1999) Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc Natl Acad Sci USA 96:11642–11647

    Article  PubMed  CAS  Google Scholar 

  • Rudoy CA, Van Bockstaele EJ (2005) Cocaine effects on norepinephrine in the amygdala: Cocaine withdrawal-related anxiety and stress-related relapse. Cellscience Rev 2:193–206. http://cellscience.com/reviews6/Rudoy.pdf. Accessed 8 July 2007

    Google Scholar 

  • Rudoy CA, Van Bockstaele EJ (2007) Betaxolol, a selective beta(1)-adrenergic receptor antagonist, diminishes anxiety-like behavior during early withdrawal from chronic cocaine administration in rats. Prog Neuropsychopharmacol Biol Psychiatry 31:1119–1129

    Article  PubMed  CAS  Google Scholar 

  • Sadikot AF, Parent A (1990) The monoaminergic innervation of the amygdala in the squirrel monkey: an immunohistochemical study. Neuroscience 36:431–447

    Article  PubMed  CAS  Google Scholar 

  • Sanchez-Gonzalez MA, Garcia-Cabezas MA, Rico B, Cavada C (2005) The primate thalamus is a key target for brain dopamine. J Neurosci 25:6076–6083

    Article  PubMed  CAS  Google Scholar 

  • Sanders JD, Happe HK, Bylund DB, Murrin LC (2005) Development of the norepinephrine transporter in the rat CNS. Neuroscience 130:107–117

    Article  PubMed  CAS  Google Scholar 

  • Savaki H, Malgouris C, Benavides J, Laplace C, Uzan A, Gueremy C, Le Fur G (1985) Quantitative autoradiography of [3H]indalpine binding sites in the rat brain: II. Regional distribution. J Neurochem 45:521–526

    Article  PubMed  CAS  Google Scholar 

  • Schneider F, Weiss U, Kessler C, Salloum JB, Posse S, Grodd W, Muller-Gartner HW (1998) Differential amygdala activation in schizophrenia during sadness. Schizophr Res 34:133–142

    Article  PubMed  CAS  Google Scholar 

  • Schroeter S, Apparsundaram S, Wiley RG, Miner LH, Sesack SR, Blakely RD (2000) Immunolocalization of the cocaine- and antidepressant-sensitive l-norepinephrine transporter. J Comp Neurol 420:211–232

    Article  PubMed  CAS  Google Scholar 

  • See RE, Kruzich PJ, Grimm JW (2001) Dopamine, but not glutamate, receptor blockade in the basolateral amygdala attenuates conditioned reward in a rat model of relapse to cocaine-seeking behavior. Psychopharmacology (Berl) 154:301–310

    Article  CAS  Google Scholar 

  • Shastry BS (2005) Bipolar disorder: an update. Neurochem Int 46:273–279

    Article  PubMed  CAS  Google Scholar 

  • Shayegan DK, Stahl SM (2005) Emotion processing, the amygdala, and outcome in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 29:840–845

    Article  PubMed  Google Scholar 

  • Sheline YI, Barch DM, Donnelly JM, Ollinger JM, Snyder AZ, Mintun MA (2001) Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol Psychiatry 50:651–658

    Article  PubMed  CAS  Google Scholar 

  • Sheline YI, Gado MH, Price JL (1998) Amygdala core nuclei volumes are decreased in recurrent major depression. Neuroreport 9:2023–2028

    Article  PubMed  CAS  Google Scholar 

  • Shimada S, Kitayama S, Walther D, Uhl G (1992) Dopamine transporter mRNA: dense expression in ventral midbrain neurons. Brain Res Mol Brain Res 13:359–362

    Article  PubMed  CAS  Google Scholar 

  • Shin LM, Rauch SL, Pitman RK (2006) Amygdala, medial prefrontal cortex, and hippocampal function in PTSD. Ann NY Acad Sci 1071:67–79

    Article  PubMed  Google Scholar 

  • Shively CA, Friedman DP, Gage HD, Bounds MC, Brown-Proctor C, Blair JB, Henderson JA, Smith MA, Buchheimer N (2006) Behavioral depression and positron emission tomography-determined serotonin 1A receptor binding potential in cynomolgus monkeys. Arch Gen Psychiatry 63:396–403

    Article  PubMed  CAS  Google Scholar 

  • Smith HR, Beveridge TJ, Porrino LJ (2006) Distribution of norepinephrine transporters in the non-human primate brain. Neuroscience 138:703–714

    Article  PubMed  CAS  Google Scholar 

  • Smith HR, Daunais JB, Nader MA, Porrino LJ (1999) Distribution of [3H]citalopram binding sites in the nonhuman primate brain. Ann NY Acad Sci 877:700–702

    Article  PubMed  CAS  Google Scholar 

  • Smolka MN, Buhler M, Schumann G, Klein S, Hu XZ, Moayer M, Zimmer A, Wrase J, Flor H, Mann K, Braus DF, Goldman D, Heinz A (2007) Gene-gene effects on central processing of aversive stimuli. Mol Psychiatry 12:307–317

    PubMed  CAS  Google Scholar 

  • Southwick SM, Krystal JH, Bremner JD, Morgan CA 3rd, Nicolaou AL, Nagy LM, Johnson DR, Heninger GR, Charney DS (1997) Noradrenergic and serotonergic function in posttraumatic stress disorder. Arch Gen Psychiatry 54:749–758

    PubMed  CAS  Google Scholar 

  • Staley JK, Basile M, Flynn DD, Mash DC (1994) Visualizing dopamine and serotonin transporters in the human brain with the potent cocaine analogue [125I]RTI-55: in vitro binding and autoradiographic characterization. J Neurochem 62:549–556

    Article  PubMed  CAS  Google Scholar 

  • Staley JK, Boja JW, Carroll FI, Seltzman HH, Wyrick CD, Lewin AH, Abraham P, Mash DC (1995) Mapping dopamine transporters in the human brain with novel selective cocaine analog [125I]RTI-121. Synapse 21:364–372

    Article  PubMed  CAS  Google Scholar 

  • Steinbusch HW (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557–618

    Article  PubMed  CAS  Google Scholar 

  • Storvik M, Tiihonen J, Haukijarvi T, Tupala E (2007) Amygdala serotonin transporters in alcoholics measured by whole hemisphere autoradiography. Synapse 61:629–636

    Article  PubMed  CAS  Google Scholar 

  • Strakowski SM, DelBello MP, Sax KW, Zimmerman ME, Shear PK, Hawkins JM, Larson ER (1999) Brain magnetic resonance imaging of structural abnormalities in bipolar disorder. Arch Gen Psychiatry 56:254–260

    Article  PubMed  CAS  Google Scholar 

  • Strange BA, Hurlemann R, Dolan RJ (2003) An emotion-induced retrograde amnesia in humans is amygdala- and beta-adrenergic-dependent. Proc Natl Acad Sci USA 100:13626–13631

    Article  PubMed  CAS  Google Scholar 

  • Sullivan GM, Coplan JD, Kent JM, Gorman JM (1999) The noradrenergic system in pathological anxiety: a focus on panic with relevance to generalized anxiety and phobias. Biol Psychiatry 46:1205–1218

    Article  PubMed  CAS  Google Scholar 

  • Sur C, Betz H, Schloss P (1996) Immunocytochemical detection of the serotonin transporter in rat brain. Neuroscience 73:217–231

    Article  PubMed  CAS  Google Scholar 

  • Suzuki T, Ishigooka J, Watanabe S, Miyaoka H (2002) Enhancement of delayed release of dopamine in the amygdala induced by conditioned fear stress in methamphetamine-sensitized rats. Eur J Pharmacol 435:59–65

    Article  PubMed  CAS  Google Scholar 

  • Swanson LW, Hartman BK (1975) The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine-beta-hydroxylase as a marker. J Comp Neurol 163:467–505

    Article  PubMed  CAS  Google Scholar 

  • Tao-Cheng J-H, Zhou FC (1999) Differential polarization of serotonin transporters in axons versus soma-dendrites: an immunogold electron microscopy study. Neuroscience 94: 821–830

    Article  PubMed  CAS  Google Scholar 

  • Taylor JR, Punch LJ, Elsworth JD (1998) A comparison of the effects of clonidine and CNQX infusion into the locus coeruleus and the amygdala on naloxone-precipitated opiate withdrawal in the rat. Psychopharmacology (Berl) 138:133–142

    Article  CAS  Google Scholar 

  • Taylor SF, Liberzon I, Decker LR, Koeppe RA (2002) A functional anatomic study of emotion in schizophrenia. Schizophr Res 58:159–172

    Article  PubMed  Google Scholar 

  • Tejani-Butt SM (1992) [3H]nisoxetine: a radioligand for quantitation of norepinephrine uptake sites by autoradiography or by homogenate binding. J Pharmacol Exp Ther 260:427–436

    PubMed  CAS  Google Scholar 

  • Tillfors M (2004) Why do some individuals develop social phobia? A review with emphasis on the neurobiological influences. Nord J Psychiatry 58:267–276

    Article  PubMed  Google Scholar 

  • Tran-Nguyen LT, Fuchs RA, Coffey GP, Baker DA, O’Dell LE, Neisewander JL (1998) Time-dependent changes in cocaine-seeking behavior and extracellular dopamine levels in the amygdala during cocaine withdrawal. Neuropsychopharmacology 19:48–59

    Article  PubMed  CAS  Google Scholar 

  • Ukairo OT, Bondi CD, Newman AH, Kulkarni SS, Kozikowski AP, Pan S, Surratt CK (2005) Recognition of benztropine by the dopamine transporter (DAT) differs from that of the classical dopamine uptake inhibitors cocaine, methylphenidate, and mazindol as a function of a DAT transmembrane 1 aspartic acid residue. J Pharmacol Exp Ther 314:575–583

    Article  PubMed  CAS  Google Scholar 

  • van Stegeren AH, Goekoop R, Everaerd W, Scheltens P, Barkhof F, Kuijer JP, Rombouts SA (2005) Noradrenaline mediates amygdala activation in men and women during encoding of emotional material. Neuroimage 24:898–909

    Article  PubMed  Google Scholar 

  • Varnas K, Halldin C, Hall H (2004) Autoradiographic distribution of serotonin transporters and receptor subtypes in human brain. Hum Brain Mapp 22:246–260

    Article  PubMed  Google Scholar 

  • Vaughan RA, Agoston GE, Lever JR, Newman AH (1999) Differential binding of tropane-based photoaffinity ligands on the dopamine transporter. J Neurosci 19:630–636

    PubMed  CAS  Google Scholar 

  • Vaughan RA, Brown VL, McCoy MT, Kuhar MJ (1996) Species- and brain region-specific dopamine transporters: immunological and glycosylation characteristics. J Neurochem 66:2146–2152

    Article  PubMed  CAS  Google Scholar 

  • Volz TJ, Schenk JO (2005) A comprehensive atlas of the topography of functional groups of the dopamine transporter. Synapse 58:72–94

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Nakagawa T, Yamamoto R, Maeda A, Minami M, Satoh M (2003) Involvement of noradrenergic system within the central nucleus of the amygdala in naloxone-precipitated morphine withdrawal-induced conditioned place aversion in rats. Psychopharmacology (Berl) 170:80–88

    Article  CAS  Google Scholar 

  • Weiss F, Maldonado-Vlaar CS, Parsons LH, Kerr TM, Smith DL, Ben-Shahar O (2000) Control of cocaine-seeking behavior by drug-associated stimuli in rats: effects on recovery of extinguished operant-responding and extracellular dopamine levels in amygdala and nucleus accumbens. Proc Natl Acad Sci USA 97:4321–4326

    Article  PubMed  CAS  Google Scholar 

  • Wilson JM, Nobrega JN, Corrigall WA, Coen KM, Shannak K, Kish SJ (1994) Amygdala dopamine levels are markedly elevated after self- but not passive-administration of cocaine. Brain Res 668:39–45

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Reith ME (1997) WIN 35,428 and mazindol are mutually exclusive in binding to the cloned human dopamine transporter. J Pharmacol Exp Ther 282:920–927

    PubMed  CAS  Google Scholar 

  • Yilmazer-Hanke DM, Roskoden T, Zilles K, Schwegler H (2003) Anxiety-related behavior and densities of glutamate, GABAA, acetylcholine and serotonin receptors in the amygdala of seven inbred mouse strains. Behav Brain Res 145:145–159

    Article  PubMed  CAS  Google Scholar 

  • Yurgelun-Todd DA, Gruber SA, Kanayama G, Killgore WD, Baird AA, Young AD (2000) fMRI during affect discrimination in bipolar affective disorder. Bipolar Disord 2:237–248

    Article  PubMed  CAS  Google Scholar 

  • Zafar HM, Pare WP, Tejani-Butt SM (1997) Effect of acute or repeated stress on behavior and brain norepinephrine system in Wistar-Kyoto (WKY) rats. Brain Res Bull 44:289–295

    Article  PubMed  CAS  Google Scholar 

  • Zeng Z, Chen TB, Miller PJ, Dean D, Tang YS, Sur C, Williams DL Jr (2006) The serotonin transporter in rhesus monkey brain: comparison of DASB and citalopram binding sites. Nucl Med Biol 33:555–563

    Article  PubMed  CAS  Google Scholar 

  • Zhou FC, Tao-Cheng J-H, Segu L, Patel T, Wang Y (1998) Serotonin transporters are located on the axons beyond the synaptic junctions: anatomical and functional evidence. Brain Res 805:241–254

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Supported by NIH grants DA06634, DA09085, and DA020648.

Author information

Authors and Affiliations

  1. Department of Physiology and Pharmacology, Center for the Neurobiological Investigation of Drugs of Abuse, Wake Forest University Health Sciences, Winston-Salem, NC, 27157-1083, USA

    Hilary R. Smith & Linda J. Porrino

Authors
  1. Hilary R. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Linda J. Porrino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hilary R. Smith.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, H.R., Porrino, L.J. The comparative distributions of the monoamine transporters in the rodent, monkey, and human amygdala. Brain Struct Funct 213, 73–91 (2008). https://doi.org/10.1007/s00429-008-0176-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-008-0176-2

Keywords

Search

Navigation