Histochemistry and Cell Biology

, Volume 139, Issue 6, pp 785–813 | Cite as

Serotonergic innervation of the amygdala: targets, receptors, and implications for stress and anxiety



The amygdala is a core component of neural circuits that mediate processing of emotional, particularly anxiety and fear-related stimuli across species. In addition, the nuclear complex plays a key role in the central nervous system stress response, and alterations in amygdala responsivity are found in neuropsychiatric disorders, especially those precipitated or sustained by stressors. Serotonin has been shown to shape and fine-tune neural plasticity in development and adulthood, thereby allowing for network flexibility and adaptive capacity in response to environmental challenges, and is implicated in the modulation of stimulus processing and stress sensitivity in the amygdala. The fact that altered amygdala activity patterns are observed upon pharmacological manipulations of serotonergic transmission, as well as in carriers of genetic variations in serotonin pathway-associated signaling molecules representing risk factors for neuropsychiatric disorders, underlines the importance of understanding the role and mode of action of serotonergic transmission in the amygdala for human psychopathology. Here, we present a short overview over organizational principles of the amygdala in rodents, non-human primates and humans, and review findings on the origin, morphology, and targets of serotonergic innervation, the distribution patterns and cellular expression of serotonin receptors, and the consequences of stress and pharmacological manipulations of serotonergic transmission in the amygdala, focusing particularly on the extensively studied basolateral complex and central nucleus.


Basolateral amygdala Central amygdala nucleus Serotonin receptors Emotion Rodent Primate 



5-Hydroxytryptamin, serotonin


Serotonin receptor(s)


Serotonin transporter


Amino-3-hydroxy-5-methyl-4-isoxazoleproprionic acid


Basolateral nucleus


Basolateral amygdala


Basolateral complex


Basomedial nucleus


Bed nucleus of the stria terminalis


Calcium/calmodulin-dependent protein kinase II




Cannabinoid-receptor 1




Central nucleus


Lateral central nucleus


Lateral capsular subdivision of the central nucleus


Medial central nucleus


Central nervous system


Cortical nucleus




Corticotropin releasing factor


Dorsal raphe nuclei




Extracellular signal-regulated kinase(s)


Gamma-amino butyric acid


Glutamic acid decarboxylase


Intercalated cells


Paracapsular intercalated cell islands








In situ hybridization


Lateral nucleus




Medial nucleus




Median raphe nuclei




Neurokinin-1 receptor


Neuropeptide Y


Periamygdaloid cortex


Paralaminar nucleus






Selective serotonin reuptake inhibitor


Tryptophan hydroxylase 2


Vasoactive intestinal polypeptide


  1. Abrams JK, Johnson PL, Hollis JH, Lowry CA (2004) Anatomic and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 1018:46–57PubMedCrossRefGoogle Scholar
  2. Abrams JK, Johnson PL, Hay-Schmidt A, Mikkelsen JD, Shekhar A, Lowry CA (2005) Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 133:983–997PubMedCrossRefGoogle Scholar
  3. Agnati LF, Fuxe K, Zoli M, Ozini I, Toffano G, Ferraguti F (1986) A correlation analysis of the regional distribution of central enkephalin and beta-endorphin immunoreactive terminals and of opiate receptors in adult and old male rats. Evidence for the existence of two main types of communication in the central nervous system: the volume transmission and the wiring transmission. Acta Physiol Scand 128:201–207PubMedCrossRefGoogle Scholar
  4. Agnati LF, Zoli M, Stromberg I, Fuxe K (1995) Intercellular communication in the brain: wiring versus volume transmission. Neuroscience 69:711–726PubMedCrossRefGoogle Scholar
  5. Agnati LF, Guidolin D, Guescini M, Genedani S, Fuxe K (2010) Understanding wiring and volume transmission. Brain Res Rev 64:137–159PubMedCrossRefGoogle Scholar
  6. Akmaev IG, Kalimullina LB, Sharipova LA (2004) The central nucleus of the amygdaloid body of the brain: cytoarchitectonics, neuronal organization, connections. Neurosci Behav Physiol 34:603–610PubMedCrossRefGoogle Scholar
  7. Albizu L, Holloway T, Gonzalez-Maeso J, Sealfon SC (2011) Functional crosstalk and heteromerization of serotonin 5-HT2A and dopamine D2 receptors. Neuropharmacology 61:770–777PubMedCrossRefGoogle Scholar
  8. Alheid GF (2003) Extended amygdala and basal forebrain. Ann N Y Acad Sci 985:185–205PubMedCrossRefGoogle Scholar
  9. Alheid GF, de Olmos JS, Beltramino CA (1995) Amygdala and extended amygdala. In: Paxinos G (ed) The rat nervous system. Academic Press, London, pp 495–578Google Scholar
  10. Allen JA, Yadav PN, Roth BL (2008) Insights into the regulation of 5-HT2A serotonin receptors by scaffolding proteins and kinases. Neuropharmacology 55:961–968PubMedCrossRefGoogle Scholar
  11. Amaral DG, Price JL, Pitkänen A, Carmichael ST (1992) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. In: Aggleton JP (ed) Anatomical organization of the primate amygdaloid complex. Wiley-Liss, New York, pp 1–66Google Scholar
  12. Amat J, Matus-Amat P, Watkins LR, Maier SF (1998) Escapable and inescapable stress differentially alter extracellular levels of 5-HT in the basolateral amygdala of the rat. Brain Res 812:113–120PubMedCrossRefGoogle Scholar
  13. Amat J, Tamblyn JP, Paul ED, Bland ST, Amat P, Foster AC, Watkins LR, Maier SF (2004) Microinjection of urocortin 2 into the dorsal raphe nucleus activates serotonergic neurons and increases extracellular serotonin in the basolateral amygdala. Neuroscience 129:509–519PubMedCrossRefGoogle Scholar
  14. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365–371PubMedCrossRefGoogle Scholar
  15. Andrade R (2011) Serotonergic regulation of neuronal excitability in the prefrontal cortex. Neuropharmacology 61:382–386PubMedCrossRefGoogle Scholar
  16. Arce E, Simmons AN, Lovero KL, Stein MB, Paulus MP (2008) Escitalopram effects on insula and amygdala BOLD activation during emotional processing. Psychopharmacology 196:661–672PubMedCrossRefGoogle Scholar
  17. Asan E (1997) Interrelationships between tyrosine hydroxylase-immunoreactive dopaminergic afferents and somatostatinergic neurons in the rat central amygdaloid nucleus. Histochem Cell Biol 107:65–79PubMedCrossRefGoogle Scholar
  18. Asan E (1998) The catecholaminergic innervation of the rat amygdala. Adv Anat Embryol Cell Biol 142:1–118PubMedCrossRefGoogle Scholar
  19. 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 131:953–967PubMedCrossRefGoogle Scholar
  20. Avila MA, Real MA, Guirado S (2011) Patterns of GABA and GABA Transporter-1 immunoreactivities in the developing and adult mouse brain amygdala. Brain Res 1388:1–11PubMedCrossRefGoogle Scholar
  21. Azmitia EC, Gannon PJ, Kheck NM, Whitaker-Azmitia PM (1996) Cellular localization of the 5-HT1A receptor in primate brain neurons and glial cells. Neuropsychopharmacology 14:35–46PubMedCrossRefGoogle Scholar
  22. Aznar S, Qian Z, Shah R, Rahbek B, Knudsen GM (2003) The 5-HT1A serotonin receptor is located on calbindin- and parvalbumin-containing neurons in the rat brain. Brain Res 959:58–67PubMedCrossRefGoogle Scholar
  23. Barad M, Gean PW, Lutz B (2006) The role of the amygdala in the extinction of conditioned fear. Biol Psychiatry 60:322–328PubMedCrossRefGoogle Scholar
  24. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083–1152PubMedCrossRefGoogle Scholar
  25. Barton DA, Esler MD, Dawood T, Lambert EA, Haikerwal D, Brenchley C, Socratous F, Hastings J, Guo L, Wiesner G, Kaye DM, Bayles R, Schlaich MP, Lambert GW (2008) Elevated brain serotonin turnover in patients with depression: effect of genotype and therapy. Arch Gen Psychiatry 65:38–46PubMedCrossRefGoogle Scholar
  26. Bassett JL, Foote SL (1992) Distribution of corticotropin-releasing factor-like immunoreactivity in squirrel monkey (Saimiri sciureus) amygdala. J Comp Neurol 323:91–102PubMedCrossRefGoogle Scholar
  27. Bauman MD, Amaral DG (2005) The distribution of serotonergic fibers in the macaque monkey amygdala: an immunohistochemical study using antisera to 5-hydroxytryptamine. Neuroscience 136:193–203PubMedCrossRefGoogle Scholar
  28. Becamel C, Gavarini S, Chanrion B, Alonso G, Galeotti N, Dumuis A, Bockaert J, Marin P (2004) The serotonin 5-HT2A and 5-HT2C receptors interact with specific sets of PDZ proteins. J Biol Chem 279:20257–20266PubMedCrossRefGoogle Scholar
  29. Belova MA, Paton JJ, Salzman CD (2008) Moment-to-moment tracking of state value in the amygdala. J Neurosci 28:10023–10030PubMedCrossRefGoogle Scholar
  30. Berretta S (2005) Cortico-amygdala circuits: role in the conditioned stress response. Stress 8:221–232PubMedCrossRefGoogle Scholar
  31. Bhatnagar S, Vining C, Denski K (2004) Regulation of chronic stress-induced changes in hypothalamic-pituitary-adrenal activity by the basolateral amygdala. Ann N Y Acad Sci 1032:315–319PubMedCrossRefGoogle Scholar
  32. Bigos KL, Pollock BG, Aizenstein HJ, Fisher PM, Bies RR, Hariri AR (2008) Acute 5-HT reuptake blockade potentiates human amygdala reactivity. Neuropsychopharmacology 33:3221–3225PubMedCrossRefGoogle Scholar
  33. Bjork K, Sjogren B, Svenningsson P (2010) Regulation of serotonin receptor function in the nervous system by lipid rafts and adaptor proteins. Exp Cell Res 316:1351–1356PubMedCrossRefGoogle Scholar
  34. Boll S, Gamer M, Kalisch R, Buchel C (2011) Processing of facial expressions and their significance for the observer in subregions of the human amygdala. NeuroImage 56:299–306PubMedCrossRefGoogle Scholar
  35. Bombardi C (2011) Distribution of 5-HT2A receptor immunoreactivity in the rat amygdaloid complex and colocalization with gamma-aminobutyric acid. Brain Res 1370:112–128PubMedCrossRefGoogle Scholar
  36. Bonn M, Schmitt A, Asan E (2012) Double and triple in situ hybridization for coexpression studies: combined fluorescent and chromogenic detection of neuropeptide Y (NPY) and serotonin receptor subtype mRNAs expressed at different abundance levels. Histochem Cell Biol 137:11–24PubMedCrossRefGoogle Scholar
  37. Bonn M, Schmitt A, Lesch KP, Van Bockstaele EJ, Asan E (2013) Serotonergic innervation and serotonin receptor expression of NPY-producing neurons in the rat lateral and basolateral amygdaloid nuclei. Brain Struct Funct 218:421–435PubMedCrossRefGoogle Scholar
  38. Bosker FJ, Cremers TI, Jongsma ME, Westerink BH, Wikstrom HV, den Boer JA (2001) Acute and chronic effects of citalopram on postsynaptic 5-hydroxytryptamine(1A) receptor-mediated feedback: a microdialysis study in the amygdala. J Neurochem 76:1645–1653PubMedCrossRefGoogle Scholar
  39. Brown P, Molliver ME (2000) Dual serotonin (5-HT) projections to the nucleus accumbens core and shell: relation of the 5-HT transporter to amphetamine-induced neurotoxicity. J Neurosci 20:1952–1963PubMedGoogle Scholar
  40. Bunin MA, Wightman RM (1998) Quantitative evaluation of 5-hydroxytryptamine (serotonin) neuronal release and uptake: an investigation of extrasynaptic transmission. J Neurosci 18:4854–4860PubMedGoogle Scholar
  41. Burns CM, Chu H, Rueter SM, Hutchinson LK, Canton H, Sanders-Bush E, Emeson RB (1997) Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 387:303–308PubMedCrossRefGoogle Scholar
  42. Campbell BM, Merchant KM (2003) Serotonin 2C receptors within the basolateral amygdala induce acute fear-like responses in an open-field environment. Brain Res 993:1–9PubMedCrossRefGoogle Scholar
  43. Canli T, Lesch KP (2007) Long story short: the serotonin transporter in emotion regulation and social cognition. Nat Neurosci 10:1103–1109PubMedCrossRefGoogle Scholar
  44. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321–352PubMedCrossRefGoogle Scholar
  45. Cassell MD, Gray TS, Kiss JZ (1986) Neuronal architecture in the rat central nucleus of the amygdala: a cytological, hodological, and immunocytochemical study. J Comp Neurol 246:478–499PubMedCrossRefGoogle Scholar
  46. Centeno ML, Sanchez RL, Reddy AP, Cameron JL, Bethea CL (2007) Corticotropin-releasing hormone and pro-opiomelanocortin gene expression in female monkeys with differences in sensitivity to stress. Neuroendocrinology 86:277–288PubMedCrossRefGoogle Scholar
  47. Charnay Y, Leger L (2010) Brain serotonergic circuitries. Dialogues Clin Neurosci 12:471–487PubMedGoogle Scholar
  48. Charney DS (2003) Neuroanatomical circuits modulating fear andanxiety behaviors. Acta Psychiatr Scand Suppl 417:38–50PubMedCrossRefGoogle Scholar
  49. Christianson JP, Ragole T, Amat J, Greenwood BN, Strong PV, Paul ED, Fleshner M, Watkins LR, Maier SF (2010) 5-hydroxytryptamine 2C receptors in the basolateral amygdala are involved in the expression of anxiety after uncontrollable traumatic stress. Biol Psychiatry 67:339–345PubMedCrossRefGoogle Scholar
  50. Ciocchi S, Herry C, Grenier F, Wolff SB, Letzkus JJ, Vlachos I, Ehrlich I, Sprengel R, Deisseroth K, Stadler MB, Muller C, Luthi A (2010) Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:277–282PubMedCrossRefGoogle Scholar
  51. Clemett DA, Punhani T, Duxon MS, Blackburn TP, Fone KC (2000) Immunohistochemical localisation of the 5-HT2C receptor protein in the rat CNS. Neuropharmacology 39:123–132PubMedCrossRefGoogle Scholar
  52. Cliffer KD, Burstein R, Giesler GJ Jr (1991) Distributions of spinothalamic, spinohypothalamic, and spinotelencephalic fibers revealed by anterograde transport of PHA-L in rats. J Neurosci 11:852–868PubMedGoogle Scholar
  53. Commons KG, Connolley KR, Valentino RJ (2003) A neurochemically distinct dorsal raphe-limbic circuit with a potential role in affective disorders. Neuropsychopharmacology 28:206–215PubMedCrossRefGoogle Scholar
  54. Compan V (2007) Do limits of neuronal plasticity represent an opportunity for mental diseases, such as addiction to food and illegal drugs? Use and utilities of serotonin receptor knock-out mice. In: Chattopadhay A (ed) Serotonin receptors in neurobiology, Frontiers in Neuroscience, chap 8. CRC Press, Boca RatonGoogle Scholar
  55. Conti LH, Costello DG, Martin LA, White MF, Abreu ME (1994) Mouse strain differences in the behavioral effects of corticotropin-releasing factor (CRF) and the CRF antagonist alpha-helical CRF9-41. Pharmacol Biochem Behav 48:497–503PubMedCrossRefGoogle Scholar
  56. Cools R, Calder AJ, Lawrence AD, Clark L, Bullmore E, Robbins TW (2005) Individual differences in threat sensitivity predict serotonergic modulation of amygdala response to fearful faces. Psychopharmacology 180:670–679PubMedCrossRefGoogle Scholar
  57. Cornea-Hebert V, Riad M, Wu C, Singh SK, Descarries L (1999) Cellular and subcellular distribution of the serotonin 5-HT2A receptor in the central nervous system of adult rat. J Comp Neurol 409:187–209PubMedCrossRefGoogle Scholar
  58. Coste SC, Kesterson RA, Heldwein KA, Stevens SL, Heard AD, Hollis JH, Murray SE, Hill JK, Pantely GA, Hohimer AR, Hatton DC, Phillips TJ, Finn DA, Low MJ, Rittenberg MB, Stenzel P, Stenzel-Poore MP (2000) Abnormal adaptations to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nat Genet 24:403–409PubMedCrossRefGoogle Scholar
  59. Crawford LK, Craige CP, Beck SG (2010) Increased intrinsic excitability of lateral wing serotonin neurons of the dorsal raphe: a mechanism for selective activation in stress circuits. J Neurophysiol 103:2652–2663PubMedCrossRefGoogle Scholar
  60. Damsa C, Kosel M, Moussally J (2009) Current status of brain imaging in anxiety disorders. Curr Opin Psychiatry 22:96–110PubMedCrossRefGoogle Scholar
  61. Davila JC, Olmos L, Legaz I, Medina L, Guirado S, Real MA (2008) Dynamic patterns of colocalization of calbindin, parvalbumin and GABA in subpopulations of mouse basolateral amygdalar cells during development. J Chem Neuroanat 35:67–76PubMedCrossRefGoogle Scholar
  62. Davis M (1992) The role of the amygdala in fear and anxiety. Annu Rev Neurosci 15:353–375PubMedCrossRefGoogle Scholar
  63. deCampo DM, Fudge JL (2012) Where and what is the paralaminar nucleus? A review on a unique and frequently overlooked area of the primate amygdala. Neurosci Biobehav Rev 36:520–535PubMedCrossRefGoogle Scholar
  64. Descarries L, Cornea-Hébert V, Riad M (2006) Cellular and subcellular localization of serotonin receptors in the central nervous system. In: Roth BL (ed) The serotonin receptors: from molecular pharmacology to human therapeutics. Humana Press, Totowa, NJ, pp 277–317CrossRefGoogle Scholar
  65. Dirks A, de Jongh R, Groenink L, van der Gugten J, Hijzen TH, Olivier B (2001) Footshock-induced sensitization of the acoustic startle response in two strains of mice. Behav Brain Res 123:17–21PubMedCrossRefGoogle Scholar
  66. Drago A, Serretti A (2009) Focus on HTR2C: a possible suggestion for genetic studies of complex disorders. Am J Med Genet B Neuropsychiatr Genet 150B:601–637PubMedCrossRefGoogle Scholar
  67. Drevets WC, Price JL, Furey ML (2008) Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 213:93–118PubMedCrossRefGoogle Scholar
  68. Duchesne A, Dufresne MM, Sullivan RM (2009) Sex differences in corticolimbic dopamine and serotonin systems in the rat and the effect of postnatal handling. Prog Neuropsychopharmacol Biol Psychiatry 33:251–261PubMedCrossRefGoogle Scholar
  69. Duvarci S, Popa D, Pare D (2011) Central amygdala activity during fear conditioning. J Neurosci 31:289–294PubMedCrossRefGoogle Scholar
  70. Duxon MS, Kennett GA, Lightowler S, Blackburn TP, Fone KC (1997) Activation of 5-HT2B receptors in the medial amygdala causes anxiolysis in the social interaction test in the rat. Neuropharmacology 36:601–608PubMedCrossRefGoogle Scholar
  71. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757–771PubMedCrossRefGoogle Scholar
  72. Eliava M, Yilmazer-Hanke D, Asan E (2003) Interrelations between monoaminergic afferents and corticotropin-releasing factor-immunoreactive neurons in the rat central amygdaloid nucleus: ultrastructural evidence for dopaminergic control of amygdaloid stress systems. Histochem Cell Biol 120:183–197PubMedCrossRefGoogle Scholar
  73. Englander MT, Dulawa SC, Bhansali P, Schmauss C (2005) How stress and fluoxetine modulate serotonin 2C receptor pre-mRNA editing. J Neurosci 25:648–651PubMedCrossRefGoogle Scholar
  74. Entis JJ, Doerga P, Barrett LF, Dickerson BC (2012) A reliable protocol for the manual segmentation of the human amygdala and its subregions using ultra-high resolution MRI. NeuroImage 60:1226–1235PubMedCrossRefGoogle Scholar
  75. Esler M, Lambert E, Alvarenga M, Socratous F, Richards J, Barton D, Pier C, Brenchley C, Dawood T, Hastings J, Guo L, Haikerwal D, Kaye D, Jennings G, Kalff V, Kelly M, Wiesner G, Lambert G (2007) Increased brain serotonin turnover in panic disorder patients in the absence of a panic attack: reduction by a selective serotonin reuptake inhibitor. Stress 10:295–304PubMedCrossRefGoogle Scholar
  76. Evans AK, Heerkens JL, Lowry CA (2009) Acoustic stimulation in vivo and corticotropin-releasing factor in vitro increase tryptophan hydroxylase activity in the rat caudal dorsal raphe nucleus. Neurosci Lett 455:36–41PubMedCrossRefGoogle Scholar
  77. Everitt BJ, Parkinson JA, Olmstead MC, Arroyo M, Robledo P, Robbins TW (1999) Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann N Y Acad Sci 877:412–438PubMedCrossRefGoogle Scholar
  78. Evers EA, Sambeth A, Ramaekers JG, Riedel WJ, van der Veen FM (2010) The effects of acute tryptophan depletion on brain activation during cognition and emotional processing in healthy volunteers. Curr Pharm Des 16:1998–2011PubMedCrossRefGoogle Scholar
  79. Fallon JH, Ciofi P (1992) Distribution of monoamines within the amygdala. In: Aggleton JP (ed) The amygdala. Wiley-Liss, New York, pp 97–114Google Scholar
  80. Feldman S, Newman ME, Weidenfeld J (2000) Effects of adrenergic and serotonergic agonists in the amygdala on the hypothalamo-pituitary-adrenocortical axis. Brain Res Bull 52:531–536PubMedCrossRefGoogle Scholar
  81. Fernandez SP, Gaspar P (2011) Investigating anxiety and depressive-like phenotypes in genetic mouse models of serotonin depletion. Neuropharmacology 62:144–154PubMedCrossRefGoogle Scholar
  82. Fink KB, Gothert M (2007) 5-HT receptor regulation of neurotransmitter release. Pharmacol Rev 59:360–417PubMedGoogle Scholar
  83. Forster GL, Feng N, Watt MJ, Korzan WJ, Mouw NJ, Summers CH, Renner KJ (2006) Corticotropin-releasing factor in the dorsal raphe elicits temporally distinct serotonergic responses in the limbic system in relation to fear behavior. Neuroscience 141:1047–1055PubMedCrossRefGoogle Scholar
  84. Forster GL, Pringle RB, Mouw NJ, Vuong SM, Watt MJ, Burke AR, Lowry CA, Summers CH, Renner KJ (2008) Corticotropin-releasing factor in the dorsal raphe nucleus increases medial prefrontal cortical serotonin via type 2 receptors and median raphe nucleus activity. Eur J Neurosci 28:299–310PubMedCrossRefGoogle Scholar
  85. Freedman LJ, Shi C (2001) Monoaminergic innervation of the macaque extended amygdala. Neuroscience 104:1067–1084PubMedCrossRefGoogle Scholar
  86. Fribourg M, Moreno JL, Holloway T, Provasi D, Baki L, Mahajan R, Park G, Adney SK, Hatcher C, Eltit JM, Ruta JD, Albizu L, Li Z, Umali A, Shim J, Fabiato A, MacKerell AD Jr, Brezina V, Sealfon SC, Filizola M, Gonzalez-Maeso J, Logothetis DE (2011) Decoding the signaling of a GPCR heteromeric complex reveals a unifying mechanism of action of antipsychotic drugs. Cell 147:1011–1023PubMedCrossRefGoogle Scholar
  87. Fudge JL, Tucker T (2009) Amygdala projections to central amygdaloid nucleus subdivisions and transition zones in the primate. Neuroscience 159:819–841PubMedCrossRefGoogle Scholar
  88. Furmark T (2009) Neurobiological aspects of social anxiety disorder. Isr J Psychiatry Relat Sci 46:5–12PubMedGoogle Scholar
  89. Fuxe K, Dahlstrom A, Hoistad M, Marcellino D, Jansson A, Rivera A, Diaz-Cabiale Z, Jacobsen K, Tinner-Staines B, Hagman B, Leo G, Staines W, Guidolin D, Kehr J, Genedani S, Belluardo N, Agnati LF (2007) From the Golgi-Cajal mapping to the transmitter-based characterization of the neuronal networks leading to two modes of brain communication: wiring and volume transmission. Brain Res Rev 55:17–54PubMedCrossRefGoogle Scholar
  90. Gardner KL, Thrivikraman KV, Lightman SL, Plotsky PM, Lowry CA (2005) Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience 136:181–191PubMedCrossRefGoogle Scholar
  91. Gardner KL, Hale MW, Oldfield S, Lightman SL, Plotsky PM, Lowry CA (2009) Adverse experience during early life and adulthood interact to elevate tph2 mRNA expression in serotonergic neurons within the dorsal raphe nucleus. Neuroscience 163:991–1001PubMedCrossRefGoogle Scholar
  92. Goldstein LE, Rasmusson AM, Bunney BS, Roth RH (1996) Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J Neurosci 16:4787–4798PubMedGoogle Scholar
  93. Gonzalez LE, Andrews N, File SE (1996) 5-HT1A and benzodiazepine receptors in the basolateral amygdala modulate anxiety in the social interaction test, but not in the elevated plus-maze. Brain Res 732:145–153PubMedCrossRefGoogle Scholar
  94. Gonzalez-Maeso J, Ang RL, Yuen T, Chan P, Weisstaub NV, Lopez-Gimenez JF, Zhou M, Okawa Y, Callado LF, Milligan G, Gingrich JA, Filizola M, Meana JJ, Sealfon SC (2008) Identification of a serotonin/glutamate receptor complex implicated in psychosis. Nature 452:93–97PubMedCrossRefGoogle Scholar
  95. 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 97:1671–1683PubMedCrossRefGoogle Scholar
  96. Graeff FG (2002) On serotonin and experimental anxiety. Psychopharmacology 163:467–476PubMedCrossRefGoogle Scholar
  97. Graeff FG, Guimaraes FS, De Andrade TG, Deakin JF (1996) Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54:129–141PubMedCrossRefGoogle Scholar
  98. Grahn RE, Will MJ, Hammack SE, Maswood S, McQueen MB, Watkins LR, Maier SF (1999) Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res 826:35–43PubMedCrossRefGoogle Scholar
  99. Gray TS (1993) Amygdaloid CRF pathways. Role in autonomic, neuroendocrine, and behavioral responses to stress. Ann N Y Acad Sci 697:53–60PubMedCrossRefGoogle Scholar
  100. Greenwood BN, Strong PV, Loughridge AB, Day HE, Clark PJ, Mika A, Hellwinkel JE, Spence KG, Fleshner M (2012) 5-HT2C receptors in the basolateral amygdala and dorsal striatum are a novel target for the anxiolytic and antidepressant effects of exercise. PLoS ONE 7:e46118PubMedCrossRefGoogle Scholar
  101. Groenink L, Joordens RJ, Hijzen TH, Dirks A, Olivier B (2000) Infusion of flesinoxan into the amygdala blocks the fear-potentiated startle. NeuroReport 11:2285–2288PubMedCrossRefGoogle Scholar
  102. Groenink L, Pattij T, De Jongh R, Van der Gugten J, Oosting RS, Dirks A, Olivier B (2003) 5-HT1A receptor knockout mice and mice overexpressing corticotropin-releasing hormone in models of anxiety. Eur J Pharmacol 463:185–197PubMedCrossRefGoogle Scholar
  103. Guest PC, Salim K, Skynner HA, George SE, Bresnick JN, McAllister G (2000) Identification and characterization of a truncated variant of the 5-hydroxytryptamine(2A) receptor produced by alternative splicing. Brain Res 876:238–244PubMedCrossRefGoogle Scholar
  104. Gurevich EV, Joyce JN (1996) Comparison of [3H]paroxetine and [3H]cyanoimipramine for quantitative measurement of serotonin transporter sites in human brain. Neuropsychopharmacology 14:309–323PubMedCrossRefGoogle Scholar
  105. Gurevich I, Englander MT, Adlersberg M, Siegal NB, Schmauss C (2002) Modulation of serotonin 2C receptor editing by sustained changes in serotonergic neurotransmission. J Neurosci 22:10529–10532PubMedGoogle Scholar
  106. Gutknecht L, Kriegebaum C, Waider J, Schmitt A, Lesch KP (2009) Spatio-temporal expression of tryptophan hydroxylase isoforms in murine and human brain: convergent data from Tph2 knockout mice. Eur Neuropsychopharmacol 19:266–282PubMedCrossRefGoogle Scholar
  107. Hackler EA, Airey DC, Shannon CC, Sodhi MS, Sanders-Bush E (2006) 5-HT(2C) receptor RNA editing in the amygdala of C57BL/6 J, DBA/2 J, and BALB/cJ mice. Neurosci Res 55:96–104PubMedCrossRefGoogle Scholar
  108. Hackler EA, Turner GH, Gresch PJ, Sengupta S, Deutch AY, Avison MJ, Gore JC, Sanders-Bush E (2007) 5-Hydroxytryptamine2C receptor contribution to m-chlorophenylpiperazine and N-methyl-beta-carboline-3-carboxamide-induced anxiety-like behavior and limbic brain activation. J Pharmacol Exp Ther 320:1023–1029PubMedCrossRefGoogle Scholar
  109. Hafizi S, Serres F, Pei Q, Totterdell S, Sharp T (2011) Evidence for the differential co-localization of neurokinin-1 receptors with 5-HT receptor subtypes in rat forebrain. J Psychopharmacol 26(4):505–515Google Scholar
  110. Halberstadt AL, Balaban CD (2006) Serotonergic and nonserotonergic neurons in the dorsal raphe nucleus send collateralized projections to both the vestibular nuclei and the central amygdaloid nucleus. Neuroscience 140:1067–1077PubMedCrossRefGoogle Scholar
  111. Hale MW, Lowry CA (2010) Functional topography of midbrain and pontine serotonergic systems: implications for synaptic regulation of serotonergic circuits. Psychopharmacology 213:243–264PubMedCrossRefGoogle Scholar
  112. Hale MW, Hay-Schmidt A, Mikkelsen JD, Poulsen B, Bouwknecht JA, Evans AK, Stamper CE, Shekhar A, Lowry CA (2008) Exposure to an open-field arena increases c-Fos expression in a subpopulation of neurons in the dorsal raphe nucleus, including neurons projecting to the basolateral amygdaloid complex. Neuroscience 157:733–748PubMedCrossRefGoogle Scholar
  113. Hale MW, Johnson PL, Westerman AM, Abrams JK, Shekhar A, Lowry CA (2010) Multiple anxiogenic drugs recruit a parvalbumin-containing subpopulation of GABAergic interneurons in the basolateral amygdala. Prog Neuropsychopharmacol Biol Psychiatry 34:1285–1293PubMedCrossRefGoogle Scholar
  114. Hale MW, Dady KF, Evans AK, Lowry CA (2011) Evidence for in vivo thermosensitivity of serotonergic neurons in the rat dorsal raphe nucleus and raphe pallidus nucleus implicated in thermoregulatory cooling. Exp Neurol 227:264–278PubMedCrossRefGoogle Scholar
  115. Hall H, Lundkvist C, Halldin C, Farde L, Pike VW, McCarron JA, Fletcher A, Cliffe IA, Barf T, Wikstrom H, Sedvall G (1997) Autoradiographic localization of 5-HT1A receptors in the post-mortem human brain using [3H]WAY-100635 and [11C]way-100635. Brain Res 745:96–108PubMedCrossRefGoogle Scholar
  116. Hannon J, Hoyer D (2008) Molecular biology of 5-HT receptors. Behav Brain Res 195:198–213PubMedCrossRefGoogle Scholar
  117. Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D, Egan MF, Weinberger DR (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297:400–403PubMedCrossRefGoogle Scholar
  118. Harmer CJ, Mackay CE, Reid CB, Cowen PJ, Goodwin GM (2006) Antidepressant drug treatment modifies the neural processing of nonconscious threat cues. Biol Psychiatry 59:816–820PubMedCrossRefGoogle Scholar
  119. Haubensak W, Kunwar PS, Cai H, Ciocchi S, Wall NR, Ponnusamy R, Biag J, Dong HW, Deisseroth K, Callaway EM, Fanselow MS, Luthi A, Anderson DJ (2010) Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 468:270–276PubMedCrossRefGoogle Scholar
  120. Hayes DJ, Greenshaw AJ (2011) 5-HT receptors and reward-related behaviour: a review. Neurosci Biobehav Rev 35:1419–1449PubMedCrossRefGoogle Scholar
  121. Hensler JG (2006) Serotonergic modulation of the limbic system. Neurosci Biobehav Rev 30:203–214PubMedCrossRefGoogle Scholar
  122. Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev 2:880–888CrossRefGoogle Scholar
  123. Hikosaka O, Bromberg-Martin E, Hong S, Matsumoto M (2008) New insights on the subcortical representation of reward. Curr Opin Neurobiol 18:203–208PubMedCrossRefGoogle Scholar
  124. Hiroi R, McDevitt RA, Neumaier JF (2006) Estrogen selectively increases tryptophan hydroxylase-2 mRNA expression in distinct subregions of rat midbrain raphe nucleus: association between gene expression and anxiety behavior in the open field. Biol Psychiatry 60:288–295PubMedCrossRefGoogle Scholar
  125. Holmes A (2008) Genetic variation in cortico-amygdala serotonin function and risk for stress-related disease. Neurosci Biobehav Rev 32:1293–1314PubMedCrossRefGoogle Scholar
  126. Homberg JR (2012) The stress-coping (mis)match hypothesis for naturexnurture interactions. Brain Res 1432:114–121PubMedCrossRefGoogle Scholar
  127. Hornung JP (2003) The human raphe nuclei and the serotonergic system. J Chem Neuroanat 26:331–343PubMedCrossRefGoogle Scholar
  128. Huang XF, Han M, Storlien LH (2004) Differential expression of 5-HT(2A) and 5-HT(2C) receptor mRNAs in mice prone, or resistant, to chronic high-fat diet-induced obesity. Brain Res Mol Brain Res 127:39–47PubMedCrossRefGoogle Scholar
  129. Ichise M, Vines DC, Gura T, Anderson GM, Suomi SJ, Higley JD, Innis RB (2006) Effects of early life stress on [11C]DASB positron emission tomography imaging of serotonin transporters in adolescent peer- and mother-reared rhesus monkeys. J Neurosci 26:4638–4643PubMedCrossRefGoogle Scholar
  130. Imai H, Steindler DA, Kitai ST (1986) The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 243:363–380PubMedCrossRefGoogle Scholar
  131. Inoue T, Li XB, Abekawa T, Kitaichi Y, Izumi T, Nakagawa S, Koyama T (2004) Selective serotonin reuptake inhibitor reduces conditioned fear through its effect in the amygdala. Eur J Pharmacol 497:311–316PubMedCrossRefGoogle Scholar
  132. Jacobs BL, Fornal CA (1999) Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21:9S–15SPubMedGoogle Scholar
  133. Jacobs BL, Foote SL, Bloom FE (1978) Differential projections of neurons within the dorsal raphe nucleus of the rat: a horseradish peroxidase (HRP) study. Brain Res 147:149–153PubMedCrossRefGoogle Scholar
  134. Jasinska AJ, Lowry CA, Burmeister M (2012) Serotonin transporter gene, stress and raphe-raphe interactions: a molecular mechanism of depression. Trends Neurosci 35(7):395–402Google Scholar
  135. Jiang X, Xing G, Yang C, Verma A, Zhang L, Li H (2009) Stress impairs 5-HT2A receptor-mediated serotonergic facilitation of GABA release in juvenile rat basolateral amygdala. Neuropsychopharmacology 34:410–423PubMedCrossRefGoogle Scholar
  136. Kawahara H, Yoshida M, Yokoo H, Nishi M, Tanaka M (1993) Psychological stress increases serotonin release in the rat amygdala and prefrontal cortex assessed by in vivo microdialysis. Neurosci Lett 162:81–84PubMedCrossRefGoogle Scholar
  137. Kia HK, Brisorgueil MJ, Hamon M, Calas A, Verge D (1996a) Ultrastructural localization of 5-hydroxytryptamine1A receptors in the rat brain. J Neurosci Res 46:697–708PubMedCrossRefGoogle Scholar
  138. Kia HK, Miquel MC, Brisorgueil MJ, Daval G, Riad M, El Mestikawy S, Hamon M, Verge D (1996b) Immunocytochemical localization of serotonin1A receptors in the rat central nervous system. J Comp Neurol 365:289–305PubMedCrossRefGoogle Scholar
  139. Kilpatrick LA, Labus JS, Coveleskie K, Hammer C, Rappold G, Tillisch K, Bueller JA, Suyenobu B, Jarcho JM, McRoberts JA, Niesler B, Mayer EA (2011) The HTR3A polymorphism c. -42C > T is associated with amygdala responsiveness in patients with irritable bowel syndrome. Gastroenterology 140:1943–1951PubMedCrossRefGoogle Scholar
  140. Kirby LG, Allen AR, Lucki I (1995) Regional differences in the effects of forced swimming on extracellular levels of 5-hydroxytryptamine and 5-hydroxyindoleacetic acid. Brain Res 682:189–196PubMedCrossRefGoogle Scholar
  141. Kishimoto K, Koyama S, Akaike N (2000) Presynaptic modulation of synaptic gamma-aminobutyric acid transmission by tandospirone in rat basolateral amygdala. Eur J Pharmacol 407:257–265PubMedCrossRefGoogle Scholar
  142. Kiyasova V, Fernandez SP, Laine J, Stankovski L, Muzerelle A, Doly S, Gaspar P (2011) A genetically defined morphologically and functionally unique subset of 5-HT neurons in the mouse raphe nuclei. J Neurosci 31:2756–2768PubMedCrossRefGoogle Scholar
  143. Klink R, Robichaud M, Debonnel G (2002) Gender and gonadal status modulation of dorsal raphe nucleus serotonergic neurons. Part I: effects of gender and pregnancy. Neuropharmacology 43:1119–1128PubMedCrossRefGoogle Scholar
  144. Koch C, Zador A (1993) The function of dendritic spines: devices subserving biochemical rather than electrical compartmentalization. J Neurosci 13:413–422PubMedGoogle Scholar
  145. Kosofsky BE, Molliver ME (1987) The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1:153–168PubMedCrossRefGoogle Scholar
  146. Koyama S, Matsumoto N, Kubo C, Akaike N (2000) Presynaptic 5-HT3 receptor-mediated modulation of synaptic GABA release in the mechanically dissociated rat amygdala neurons. J Physiol 529(Pt 2):373–383PubMedCrossRefGoogle Scholar
  147. Koyama S, Matsumoto N, Murakami N, Kubo C, Nabekura J, Akaike N (2002) Role of presynaptic 5-HT1A and 5-HT3 receptors in modulation of synaptic GABA transmission in dissociated rat basolateral amygdala neurons. Life Sci 72:375–387PubMedCrossRefGoogle Scholar
  148. Krettek JE, Price JL (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178:225–254PubMedCrossRefGoogle Scholar
  149. Law AJ, Pei Q, Feldon J, Pryce CR, Harrison PJ (2009) Gene expression in the anterior cingulate cortex and amygdala of adolescent marmoset monkeys following parental separations in infancy. Int J Neuropsychopharmacol 12:761–772PubMedCrossRefGoogle Scholar
  150. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184PubMedCrossRefGoogle Scholar
  151. LeDoux J (2003) The emotional brain, fear, and the amygdala. Cell Mol Neurobiol 23:727–738PubMedCrossRefGoogle Scholar
  152. LeDoux J (2007) The amygdala. Curr Biol 17:R868–R874PubMedCrossRefGoogle Scholar
  153. LeDoux J (2012) Rethinking the emotional brain. Neuron 73:653–676PubMedCrossRefGoogle Scholar
  154. LeDoux JE, Iwata J, Cicchetti P, Reis DJ (1988) Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci 8:2517–2529PubMedGoogle Scholar
  155. Lee BT, Ham BJ (2008) Serotonergic genes and amygdala activity in response to negative affective facial stimuli in Korean women. Genes Brain Behav 7:899–905PubMedCrossRefGoogle Scholar
  156. Lehre KP, Danbolt NC (1998) The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J Neurosci 18:8751–8757PubMedGoogle Scholar
  157. Leite-Panissi CR, Ferrarese AA, Terzian AL, Menescal-de-Oliveira L (2006) Serotoninergic activation of the basolateral amygdala and modulation of tonic immobility in guinea pig. Brain Res Bull 69:356–364PubMedCrossRefGoogle Scholar
  158. Lesch KP, Waider J (2012) Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders. Neuron 76:175–191PubMedCrossRefGoogle Scholar
  159. Lesch KP, Bengel D, Heils A, Sabol SZ, Greenberg BD, Petri S, Benjamin J, Muller CR, Hamer DH, Murphy DL (1996) Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274:1527–1531PubMedCrossRefGoogle Scholar
  160. Lesch KP, Zeng Y, Reif A, Gutknecht L (2003) Anxiety-related traits in mice with modified genes of the serotonergic pathway. Eur J Pharmacol 480:185–204PubMedCrossRefGoogle Scholar
  161. Leuner B, Shors TJ (2012) Stress, anxiety, and dendritic spines: what are the connections? Neuroscience [Epub ahead of print]Google Scholar
  162. Levens SM, Devinsky O, Phelps EA (2011) Role of the left amygdala and right orbital frontal cortex in emotional interference resolution facilitation in working memory. Neuropsychologia 49:3201–3212PubMedCrossRefGoogle Scholar
  163. Li Q, Wichems CH, Ma L, Van de Kar LD, Garcia F, Murphy DL (2003) Brain region-specific alterations of 5-HT2A and 5-HT2C receptors in serotonin transporter knockout mice. J Neurochem 84:1256–1265PubMedCrossRefGoogle Scholar
  164. Li X, Inoue T, Abekawa T, Weng S, Nakagawa S, Izumi T, Koyama T (2006) 5-HT1A receptor agonist affects fear conditioning through stimulations of the postsynaptic 5-HT1A receptors in the hippocampus and amygdala. Eur J Pharmacol 532:74–80PubMedCrossRefGoogle Scholar
  165. Li Q, Luo T, Jiang X, Wang J (2012) Anxiolytic effects of 5-HTA receptors and anxiogenic effects of 5-HTC receptors in the amygdala of mice. Neuropharmacology 62:474–484PubMedCrossRefGoogle Scholar
  166. Liu S, Bubar MJ, Lanfranco MF, Hillman GR, Cunningham KA (2007) Serotonin2C receptor localization in GABA neurons of the rat medial prefrontal cortex: implications for understanding the neurobiology of addiction. Neuroscience 146:1677–1688PubMedCrossRefGoogle Scholar
  167. Lopez-Gimenez JF, Vilaro MT, Palacios JM, Mengod G (2001) Mapping of 5-HT2A receptors and their mRNA in monkey brain: [3H]MDL100,907 autoradiography and in situ hybridization studies. J Comp Neurol 429:571–589PubMedCrossRefGoogle Scholar
  168. Lowry CA, Johnson PL, Hay-Schmidt A, Mikkelsen J, Shekhar A (2005) Modulation of anxiety circuits by serotonergic systems. Stress 8:233–246PubMedCrossRefGoogle Scholar
  169. Lowry CA, Hale MW, Evans AK, Heerkens J, Staub DR, Gasser PJ, Shekhar A (2008) Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 1148:86–94PubMedCrossRefGoogle Scholar
  170. Luscher C, Slesinger PA (2010) Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat Rev 11:301–315Google Scholar
  171. Ma QP, Yin GF, Ai MK, Han JS (1991) Serotonergic projections from the nucleus raphe dorsalis to the amygdala in the rat. Neurosci Lett 134:21–24PubMedCrossRefGoogle Scholar
  172. Macedo CE, Martinez RC, de Souza Silva MA, Brandao ML (2005) Increases in extracellular levels of 5-HT and dopamine in the basolateral, but not in the central, nucleus of amygdala induced by aversive stimulation of the inferior colliculus. Eur J Neurosci 21:1131–1138PubMedCrossRefGoogle Scholar
  173. Magalhaes AC, Holmes KD, Dale LB, Comps-Agrar L, Lee D, Yadav PN, Drysdale L, Poulter MO, Roth BL, Pin JP, Anisman H, Ferguson SS (2010) CRF receptor 1 regulates anxiety behavior via sensitization of 5-HT2 receptor signaling. Nat Neurosci 13:622–629PubMedCrossRefGoogle Scholar
  174. Mahan AL, Ressler KJ (2012) Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder. Trends Neurosci 35:24–35PubMedCrossRefGoogle Scholar
  175. Maier SF, Watkins LR (2005) Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev 29:829–841PubMedCrossRefGoogle Scholar
  176. Mamounas LA, Molliver ME (1988) Evidence for dual serotonergic projections to neocortex: axons from the dorsal and median raphe nuclei are differentially vulnerable to the neurotoxin p-chloroamphetamine (PCA). Exp Neurol 102:23–36PubMedCrossRefGoogle Scholar
  177. Man MS, Mikheenko Y, Braesicke K, Cockcroft G, Roberts AC (2012) Serotonin at the level of the amygdala and orbitofrontal cortex modulates distinct aspects of positive emotion in primates. Int J Neuropsychopharmacol 15:1–15Google Scholar
  178. Marazziti D, Baroni S, Pirone A, Giannaccini G, Betti L, Schmid L, Vatteroni E, Palego L, Borsini F, Bordi F, Piano I, Gargini C, Castagna M, Catena-Dell’osso M, Lucacchini A (2012) Distribution of serotonin receptor of type 6 (5-HT(6)) in human brain post-mortem. a pharmacology, autoradiography and immunohistochemistry study. Neurochem Res 37(5):920–927Google Scholar
  179. Maren S, Quirk GJ (2004) Neuronal signalling of fear memory. Nat Rev 5:844–852CrossRefGoogle Scholar
  180. Marion S, Weiner DM, Caron MG (2004) RNA editing induces variation in desensitization and trafficking of 5-hydroxytryptamine 2c receptor isoforms. J Biol Chem 279:2945–2954PubMedCrossRefGoogle Scholar
  181. Mascagni F, McDonald AJ (2007) A novel subpopulation of 5-HT type 3A receptor subunit immunoreactive interneurons in the rat basolateral amygdala. Neuroscience 144:1015–1024PubMedCrossRefGoogle Scholar
  182. Mascagni F, Muly EC, Rainnie DG, McDonald AJ (2009) Immunohistochemical characterization of parvalbumin-containing interneurons in the monkey basolateral amygdala. Neuroscience 158:1541–1550PubMedCrossRefGoogle Scholar
  183. McDonald AJ (1982a) Cytoarchitecture of the central amygdaloid nucleus of the rat. J Comp Neurol 208:401–418PubMedCrossRefGoogle Scholar
  184. McDonald AJ (1982b) Neurons of the lateral and basolateral amygdaloid nuclei: a Golgi study in the rat. J Comp Neurol 212:293–312PubMedCrossRefGoogle Scholar
  185. McDonald AJ (1989) Coexistence of somatostatin with neuropeptide Y, but not with cholecystokinin or vasoactive intestinal peptide, in neurons of the rat amygdala. Brain Res 500:37–45PubMedCrossRefGoogle Scholar
  186. McDonald AJ (1992) Cell types and intrinsic connections of the amvgdala. In: Aggleton JP (ed) The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction. Wiley-Liss, New York, pp 67–96Google Scholar
  187. McDonald AJ (1997) Calbindin-D28 k immunoreactivity in the rat amygdala. J Comp Neurol 383:231–244PubMedCrossRefGoogle Scholar
  188. McDonald AJ (1998) Cortical pathways to the mammalian amygdala. Prog Neurobiol 55:257–332PubMedCrossRefGoogle Scholar
  189. McDonald AJ, Betette RL (2001) Parvalbumin-containing neurons in the rat basolateral amygdala: morphology and co-localization of Calbindin-D(28 k). Neuroscience 102:413–425PubMedCrossRefGoogle Scholar
  190. McDonald AJ, Mascagni F (2001) Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala. Neuroscience 105:681–693PubMedCrossRefGoogle Scholar
  191. McDonald AJ, Mascagni F (2007) Neuronal localization of 5-HT type 2A receptor immunoreactivity in the rat basolateral amygdala. Neuroscience 146:306–320PubMedCrossRefGoogle Scholar
  192. McDonald AJ, Pearson JC (1989) Coexistence of GABA and peptide immunoreactivity in non-pyramidal neurons of the basolateral amygdala. Neurosci Lett 100:53–58PubMedCrossRefGoogle Scholar
  193. McDonald AJ, Mascagni F, Augustine JR (1995) Neuropeptide Y and somatostatin-like immunoreactivity in neurons of the monkey amygdala. Neuroscience 66:959–982PubMedCrossRefGoogle Scholar
  194. McDonald AJ, Shammah-Lagnado SJ, Shi C, Davis M (1999) Cortical afferents to the extended amygdala. Ann N Y Acad Sci 877:309–338PubMedCrossRefGoogle Scholar
  195. McEuen JG, Beck SG, Bale TL (2008) Failure to mount adaptive responses to stress results in dysregulation and cell death in the midbrain raphe. J Neurosci 28:8169–8177PubMedCrossRefGoogle Scholar
  196. McEwen BS, Eiland L, Hunter RG, Miller MM (2012) Stress and anxiety: structural plasticity and epigenetic regulation as a consequence of stress. Neuropharmacology 62:3–12PubMedCrossRefGoogle Scholar
  197. Medina L, Legaz I, Gonzalez G, De Castro F, Rubenstein JL, Puelles L (2004) Expression of Dbx1, Neurogenin 2, Semaphorin 5A, Cadherin 8, and Emx1 distinguish ventral and lateral pallial histogenetic divisions in the developing mouse claustroamygdaloid complex. J Comp Neurol 474:504–523PubMedCrossRefGoogle Scholar
  198. Menard J, Treit D (1999) Effects of centrally administered anxiolytic compounds in animal models of anxiety. Neurosci Biobehav Rev 23:591–613PubMedCrossRefGoogle Scholar
  199. Menetrey D, De Pommery J (1991) Origins of Spinal Ascending Pathways that Reach Central Areas Involved in Visceroception and Visceronociception in the Rat. Eur J Neurosci 3:249–259PubMedCrossRefGoogle Scholar
  200. Millhouse OE (1986) The intercalated cells of the amygdala. J Comp Neurol 247:246–271PubMedCrossRefGoogle Scholar
  201. Millhouse OE, DeOlmos J (1983) Neuronal configurations in lateral and basolateral amygdala. Neuroscience 10:1269–1300PubMedCrossRefGoogle Scholar
  202. Miner LA, Backstrom JR, Sanders-Bush E, Sesack SR (2003) Ultrastructural localization of serotonin2A receptors in the middle layers of the rat prelimbic prefrontal cortex. Neuroscience 116:107–117PubMedCrossRefGoogle Scholar
  203. Miquel MC, Doucet E, Boni C, El Mestikawy S, Matthiessen L, Daval G, Verge D, Hamon M (1991) Central serotonin 1A receptors: respective distributions of encoding mRNA, receptor protein and binding sites by in situ hybridization histochemistry, radioimmunohistochemistry and autoradiographic mapping in the rat brain. Neurochem Int 19:453–465CrossRefGoogle Scholar
  204. Miquel MC, Emerit MB, Nosjean A, Simon A, Rumajogee P, Brisorgueil MJ, Doucet E, Hamon M, Verge D (2002) Differential subcellular localization of the 5-HT3-As receptor subunit in the rat central nervous system. Eur J Neurosci 15:449–457PubMedCrossRefGoogle Scholar
  205. Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S (2005) Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci U S A 102:9371–9376PubMedCrossRefGoogle Scholar
  206. Mitra R, Adamec R, Sapolsky R (2009) Resilience against predator stress and dendritic morphology of amygdala neurons. Behav Brain Res 205:535–543PubMedCrossRefGoogle Scholar
  207. Mitsushima D, Yamada K, Takase K, Funabashi T, Kimura F (2006) Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur J Neurosci 24:3245–3254PubMedCrossRefGoogle Scholar
  208. Mo B, Feng N, Renner K, Forster G (2008) Restraint stress increases serotonin release in the central nucleus of the amygdala via activation of corticotropin-releasing factor receptors. Brain Res Bull 76:493–498PubMedCrossRefGoogle Scholar
  209. Moga MM, Gray TS (1985) Evidence for corticotropin-releasing factor, neurotensin, and somatostatin in the neural pathway from the central nucleus of the amygdala to the parabrachial nucleus. J Comp Neurol 241:275–284PubMedCrossRefGoogle Scholar
  210. Morales M, Bloom FE (1997) The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17:3157–3167PubMedGoogle Scholar
  211. Morales M, Battenberg E, de Lecea L, Sanna PP, Bloom FE (1996) Cellular and subcellular immunolocalization of the type 3 serotonin receptor in the rat central nervous system. Brain Res Mol Brain Res 36:251–260PubMedCrossRefGoogle Scholar
  212. Morales M, Wang SD, Diaz-Ruiz O, Jho DH (2004) Cannabinoid CB1 receptor and serotonin 3 receptor subunit A (5-HT3A) are co-expressed in GABA neurons in the rat telencephalon. J Comp Neurol 468:205–216PubMedCrossRefGoogle Scholar
  213. Morrison KE, Cooper MA (2012) A role for 5-HT1A receptors in the basolateral amygdala in the development of conditioned defeat in Syrian hamsters. Pharmacol Biochem Behav 100:592–600PubMedCrossRefGoogle Scholar
  214. Morrison KE, Swallows CL, Cooper MA (2011) Effects of dominance status on conditioned defeat and expression of 5-HT1A and 5-HT2A receptors. Physiol Behav 104:283–290PubMedCrossRefGoogle Scholar
  215. Moya PR, Fox MA, Jensen CL, Laporte JL, French HT, Wendland JR, Murphy DL (2011) Altered 5-HT2C receptor agonist-induced responses and 5-HT2C receptor RNA editing in the amygdala of serotonin transporter knockout mice. BMC Pharmacol 11:3PubMedCrossRefGoogle Scholar
  216. Mozhui K, Hamre KM, Holmes A, Lu L, Williams RW (2007) Genetic and structural analysis of the basolateral amygdala complex in BXD recombinant inbred mice. Behav Genet 37:223–243PubMedCrossRefGoogle Scholar
  217. Mozhui K, Karlsson RM, Kash TL, Ihne J, Norcross M, Patel S, Farrell MR, Hill EE, Graybeal C, Martin KP, Camp M, Fitzgerald PJ, Ciobanu DC, Sprengel R, Mishina M, Wellman CL, Winder DG, Williams RW, Holmes A (2010) Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 30:5357–5367PubMedCrossRefGoogle Scholar
  218. Muller MB, Keck ME (2002) Genetically engineered mice for studies of stress-related clinical conditions. J Psychiatr Res 36:53–76PubMedCrossRefGoogle Scholar
  219. Muller JF, Mascagni F, McDonald AJ (2003) Synaptic connections of distinct interneuronal subpopulations in the rat basolateral amygdalar nucleus. J Comp Neurol 456:217–236PubMedCrossRefGoogle Scholar
  220. Muller JF, Mascagni F, McDonald AJ (2005) Coupled networks of parvalbumin-immunoreactive interneurons in the rat basolateral amygdala. J Neurosci 25:7366–7376PubMedCrossRefGoogle Scholar
  221. Muller JF, Mascagni F, McDonald AJ (2006) Pyramidal cells of the rat basolateral amygdala: synaptology and innervation by parvalbumin-immunoreactive interneurons. J Comp Neurol 494:635–650PubMedCrossRefGoogle Scholar
  222. Muller JF, Mascagni F, McDonald AJ (2007a) Postsynaptic targets of somatostatin-containing interneurons in the rat basolateral amygdala. J Comp Neurol 500:513–529PubMedCrossRefGoogle Scholar
  223. Muller JF, Mascagni F, McDonald AJ (2007b) Serotonin-immunoreactive axon terminals innervate pyramidal cells and interneurons in the rat basolateral amygdala. J Comp Neurol 505:314–335PubMedCrossRefGoogle Scholar
  224. Murray EA, Izquierdo A (2007) Orbitofrontal cortex and amygdala contributions to affect and action in primates. Ann N Y Acad Sci 1121:273–296PubMedCrossRefGoogle Scholar
  225. Murrough JW, Czermak C, Henry S, Nabulsi N, Gallezot JD, Gueorguieva R, Planeta-Wilson B, Krystal JH, Neumaier JF, Huang Y, Ding YS, Carson RE, Neumeister A (2011a) The effect of early trauma exposure on serotonin type 1B receptor expression revealed by reduced selective radioligand binding. Arch Gen Psychiatry 68:892–900PubMedCrossRefGoogle Scholar
  226. Murrough JW, Huang Y, Hu J, Henry S, Williams W, Gallezot JD, Bailey CR, Krystal JH, Carson RE, Neumeister A (2011b) Reduced amygdala serotonin transporter binding in posttraumatic stress disorder. Biol Psychiatry 70:1033–1038PubMedCrossRefGoogle Scholar
  227. Narayanan V, Heiming RS, Jansen F, Lesting J, Sachser N, Pape HC, Seidenbecher T (2011) Social defeat: impact on fear extinction and amygdala-prefrontal cortical theta synchrony in 5-HTT deficient mice. PLoS ONE 6:e22600PubMedCrossRefGoogle Scholar
  228. Neumaier JF, Sexton TJ, Yracheta J, Diaz AM, Brownfield M (2001) Localization of 5-HT(7) receptors in rat brain by immunocytochemistry, in situ hybridization, and agonist stimulated cFos expression. J Chem Neuroanat 21:63–73PubMedCrossRefGoogle Scholar
  229. Nietzer SL, Bonn M, Jansen F, Heiming RS, Lewejohann L, Sachser N, Asan ES, Lesch KP, Schmitt AG (2011) Serotonin transporter knockout and repeated social defeat stress: impact on neuronal morphology and plasticity in limbic brain areas. Behav Brain Res 220:42–54PubMedCrossRefGoogle Scholar
  230. Norbury R, Taylor MJ, Selvaraj S, Murphy SE, Harmer CJ, Cowen PJ (2009) Short-term antidepressant treatment modulates amygdala response to happy faces. Psychopharmacology 206:197–204PubMedCrossRefGoogle Scholar
  231. O’Rourke H, Fudge JL (2006) Distribution of serotonin transporter labeled fibers in amygdaloid subregions: implications for mood disorders. Biol Psychiatry 60:479–490PubMedCrossRefGoogle Scholar
  232. Ottersen OP (1980) Afferent connections to the amygdaloid complex of the rat and cat: II. Afferents from the hypothalamus and the basal telencephalon. J Comp Neurol 194:267–289PubMedCrossRefGoogle Scholar
  233. Ottersen OP (1981) Afferent connections to the amygdaloid complex of the rat with some observations in the cat. III. Afferents from the lower brain stem. J Comp Neurol 202:335–356PubMedCrossRefGoogle Scholar
  234. Ottersen OP, Ben-Ari Y (1979) Afferent connections to the amygdaloid complex of the rat and cat. I. Projections from the thalamus. J Comp Neurol 187:401–424PubMedCrossRefGoogle Scholar
  235. Palomares-Castillo E, Hernandez-Perez OR, Perez-Carrera D, Crespo-Ramirez M, Fuxe K, Perez de la Mora M (2012) The intercalated paracapsular islands as a module for integration of signals regulating anxiety in the amygdala. Brain Res 1476:211–234Google Scholar
  236. Pape HC, Pare D (2010) Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear. Physiol Rev 90:419–463PubMedCrossRefGoogle Scholar
  237. Pasqualetti M, Ori M, Castagna M, Marazziti D, Cassano GB, Nardi I (1999) Distribution and cellular localization of the serotonin type 2C receptor messenger RNA in human brain. Neuroscience 92:601–611PubMedCrossRefGoogle Scholar
  238. Paton JJ, Belova MA, Morrison SE, Salzman CD (2006) The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439:865–870PubMedCrossRefGoogle Scholar
  239. Peddie CJ, Davies HA, Colyer FM, Stewart MG, Rodriguez JJ (2008) Colocalisation of serotonin2A receptors with the glutamate receptor subunits NR1 and GluR2 in the dentate gyrus: an ultrastructural study of a modulatory role. Exp Neurol 211:561–573PubMedCrossRefGoogle Scholar
  240. Petrov T, Krukoff TL, Jhamandas JH (1994) Chemically defined collateral projections from the pons to the central nucleus of the amygdala and hypothalamic paraventricular nucleus in the rat. Cell Tissue Res 277:289–295PubMedCrossRefGoogle Scholar
  241. Petrovich GD, Swanson LW (1997) Projections from the lateral part of the central amygdalar nucleus to the postulated fear conditioning circuit. Brain Res 763:247–254PubMedCrossRefGoogle Scholar
  242. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–187PubMedCrossRefGoogle Scholar
  243. Pitkänen 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 71:369–377PubMedCrossRefGoogle Scholar
  244. Pitkänen A, Savander V, LeDoux JE (1997) Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala. Trends Neurosci 20:517–523PubMedCrossRefGoogle Scholar
  245. Pitkänen A, Tuunanen J, Kalviainen R, Partanen K, Salmenpera T (1998) Amygdala damage in experimental and human temporal lobe epilepsy. Epilepsy Res 32:233–253PubMedCrossRefGoogle Scholar
  246. Plappert CF, Pilz PK (2002) Difference in anxiety and sensitization of the acoustic startle response between the two inbred mouse strains BALB/cAN and DBA/2 N. Genes Brain Behav 1:178–186PubMedCrossRefGoogle Scholar
  247. Polter AM, Li X (2010) 5-HT1A receptor-regulated signal transduction pathways in brain. Cell Signal 22:1406–1412PubMedCrossRefGoogle Scholar
  248. Pompeiano M, Palacios JM, Mengod G (1994) Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res Mol Brain Res 23:163–178PubMedCrossRefGoogle Scholar
  249. Price JL (2003) Comparative aspects of amygdala connectivity. Ann N Y Acad Sci 985:50–58PubMedCrossRefGoogle Scholar
  250. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, Rubenstein JL (2000) Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-2.1, Pax-6, and Tbr-1. J Comp Neurol 424:409–438PubMedCrossRefGoogle Scholar
  251. Puig MV, Gulledge AT (2011) Serotonin and prefrontal cortex function: neurons, networks, and circuits. Mol Neurobiol 44:449–464PubMedCrossRefGoogle Scholar
  252. Rainnie DG (1999) Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82:69–85PubMedGoogle Scholar
  253. Rainnie DG (2003) Inhibitory and excitatory circuitries in amygdala nuclei: a synopsis of session II. Ann N Y Acad Sci 985:59–66PubMedCrossRefGoogle Scholar
  254. Rainnie DG, Mania I, Mascagni F, McDonald AJ (2006) Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala. J Comp Neurol 498:142–161PubMedCrossRefGoogle Scholar
  255. Ravinder S, Pillai AG, Chattarji S (2011) Cellular correlates of enhanced anxiety caused by acute treatment with the selective serotonin reuptake inhibitor fluoxetine in rats. Front Behav Neurosci 5:88PubMedCrossRefGoogle Scholar
  256. Rea K, Lang Y, Finn DP (2009) Alterations in extracellular levels of gamma-aminobutyric acid in the rat basolateral amygdala and periaqueductal gray during conditioned fear, persistent pain and fear-conditioned analgesia. J Pain 10:1088–1098PubMedCrossRefGoogle Scholar
  257. Real MA, Heredia R, Labrador Mdel C, Davila JC, Guirado S (2009) Expression of somatostatin and neuropeptide Y in the embryonic, postnatal, and adult mouse amygdalar complex. J Comp Neurol 513:335–348PubMedCrossRefGoogle Scholar
  258. Reyes BA, Drolet G, Van Bockstaele EJ (2008) Dynorphin and stress-related peptides in rat locus coeruleus: contribution of amygdalar efferents. J Comp Neurol 508:663–675PubMedCrossRefGoogle Scholar
  259. Reyes BA, Carvalho AF, Vakharia K, Van Bockstaele EJ (2011) Amygdalar peptidergic circuits regulating noradrenergic locus coeruleus neurons: linking limbic and arousal centers. Exp Neurol 230:96–105PubMedCrossRefGoogle Scholar
  260. Reznikov LR, Reagan LP, Fadel JR (2008) Activation of phenotypically distinct neuronal subpopulations in the anterior subdivision of the rat basolateral amygdala following acute and repeated stress. J Comp Neurol 508:458–472PubMedCrossRefGoogle Scholar
  261. Riad M, Garcia S, Watkins KC, Jodoin N, Doucet E, Langlois X, el Mestikawy S, Hamon M, Descarries L (2000) Somatodendritic localization of 5-HT1A and preterminal axonal localization of 5-HT1B serotonin receptors in adult rat brain. J Comp Neurol 417:181–194PubMedCrossRefGoogle Scholar
  262. Rinaman L, Schwartz G (2004) Anterograde transneuronal viral tracing of central viscerosensory pathways in rats. J Neurosci 24:2782–2786PubMedCrossRefGoogle Scholar
  263. Roche M, Commons KG, Peoples A, Valentino RJ (2003) Circuitry underlying regulation of the serotonergic system by swim stress. J Neurosci 23:970–977Google Scholar
  264. Rodriguez JJ, Garcia DR, Pickel VM (1999) Subcellular distribution of 5-hydroxytryptamine2A and N-methyl-d-aspartate receptors within single neurons in rat motor and limbic striatum. J Comp Neurol 413:219–231PubMedCrossRefGoogle Scholar
  265. Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev 10:423–433Google Scholar
  266. Rose C, Schwegler H, Hanke J, Rohl FW, Yilmazer-Hanke DM (2006) Differential effects of embryo transfer and maternal factors on anxiety-related behavior and numbers of neuropeptide Y (NPY) and parvalbumin (PARV) containing neurons in the amygdala of inbred C3H/HeN and DBA/2 J mice. Behav Brain Res 173:163–168PubMedCrossRefGoogle Scholar
  267. Roychowdhury S, Haas H, Anderson EG (1994) 5-HT1A and 5-HT4 receptor colocalization on hippocampal pyramidal cells. Neuropharmacology 33:551–557PubMedCrossRefGoogle Scholar
  268. Rueter LE, Jacobs BL (1996) A microdialysis examination of serotonin release in the rat forebrain induced by behavioral/environmental manipulations. Brain Res 739:57–69PubMedCrossRefGoogle Scholar
  269. Sadikot AF, Parent A (1990) The monoaminergic innervation of the amygdala in the squirrel monkey: an immunohistochemical study. Neuroscience 36:431–447PubMedCrossRefGoogle Scholar
  270. Sah P, Faber ES, Lopez De Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834PubMedGoogle Scholar
  271. Saha S, Gamboa-Esteves FO, Batten TF (2010) Differential distribution of 5-HT 1A and 5-HT 1B-like immunoreactivities in rat central nucleus of the amygdala neurones projecting to the caudal dorsomedial medulla oblongata. Brain Res 1330:20–30PubMedCrossRefGoogle Scholar
  272. Sakai K, Crochet S (2001) Differentiation of presumed serotonergic dorsal raphe neurons in relation to behavior and wake-sleep states. Neuroscience 104:1141–1155PubMedCrossRefGoogle Scholar
  273. Saper CB, Loewy AD (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res 197:291–317PubMedCrossRefGoogle Scholar
  274. Sartori SB, Hauschild M, Bunck M, Gaburro S, Landgraf R, Singewald N (2011) Enhanced fear expression in a psychopathological mouse model of trait anxiety: pharmacological interventions. PLoS ONE 6:e16849PubMedCrossRefGoogle Scholar
  275. Schiller L, Jahkel M, Kretzschmar M, Brust P, Oehler J (2003) Autoradiographic analyses of 5-HT1A and 5-HT2A receptors after social isolation in mice. Brain Res 980:169–178PubMedCrossRefGoogle Scholar
  276. Scholl JL, Vuong SM, Forster GL (2010) Chronic amphetamine treatment enhances corticotropin-releasing factor-induced serotonin release in the amygdala. Eur J Pharmacol 644:80–87PubMedCrossRefGoogle Scholar
  277. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev 6:277–284Google Scholar
  278. Shekhar A, Sajdyk TJ, Gehlert DR, Rainnie DG (2003) The amygdala, panic disorder, and cardiovascular responses. Ann N Y Acad Sci 985:308–325PubMedCrossRefGoogle Scholar
  279. Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35:169–191PubMedCrossRefGoogle Scholar
  280. Shors TJ, Mathew PR (1998) NMDA receptor antagonism in the lateral/basolateral but not central nucleus of the amygdala prevents the induction of facilitated learning in response to stress. Learn Mem 5:220–230PubMedGoogle Scholar
  281. Sierra-Mercado D, Padilla-Coreano N, Quirk GJ (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36:529–538PubMedCrossRefGoogle Scholar
  282. Simon D, Craig KD, Miltner WH, Rainville P (2006) Brain responses to dynamic facial expressions of pain. Pain 126:309–318PubMedCrossRefGoogle Scholar
  283. Smith HR, Porrino LJ (2008) The comparative distributions of the monoamine transporters in the rodent, monkey, and human amygdala. Brain Struct Funct 213:73–91PubMedCrossRefGoogle Scholar
  284. Sorvari H, Soininen H, Paljarvi L, Karkola K, Pitkänen A (1995) Distribution of parvalbumin-immunoreactive cells and fibers in the human amygdaloid complex. J Comp Neurol 360:185–212PubMedCrossRefGoogle Scholar
  285. Sorvari H, Soininen H, Pitkänen A (1996a) Calbindin-D28 K-immunoreactive cells and fibres in the human amygdaloid complex. Neuroscience 75:421–443PubMedCrossRefGoogle Scholar
  286. Sorvari H, Soininen H, Pitkänen A (1996b) Calretinin-immunoreactive cells and fibers in the human amygdaloid complex. J Comp Neurol 369:188–208PubMedCrossRefGoogle Scholar
  287. Spannuth BM, Hale MW, Evans AK, Lukkes JL, Campeau S, Lowry CA (2011) Investigation of a central nucleus of the amygdala/dorsal raphe nucleus serotonergic circuit implicated in fear-potentiated startle. Neuroscience 179:104–119PubMedCrossRefGoogle Scholar
  288. Stanford IM, Kantaria MA, Chahal HS, Loucif KC, Wilson CL (2005) 5-Hydroxytryptamine induced excitation and inhibition in the subthalamic nucleus: action at 5-HT(2C), 5-HT(4) and 5-HT(1A) receptors. Neuropharmacology 49:1228–1234PubMedCrossRefGoogle Scholar
  289. Staub DR, Spiga F, Lowry CA (2005) Urocortin 2 increases c-Fos expression in topographically organized subpopulations of serotonergic neurons in the rat dorsal raphe nucleus. Brain Res 1044:176–189PubMedCrossRefGoogle Scholar
  290. Staub DR, Evans AK, Lowry CA (2006) Evidence supporting a role for corticotropin-releasing factor type 2 (CRF2) receptors in the regulation of subpopulations of serotonergic neurons. Brain Res 1070:77–89PubMedCrossRefGoogle Scholar
  291. Steinbusch HW, Nieuwenhuys R (1981) Localization of serotonin-like immunoreactivity in the central nervous system and pituitary of the rat, with special references to the innervation of the hypothalamus. Adv Exp Med Biol 133:7–35PubMedCrossRefGoogle Scholar
  292. Stiedl O, Palve M, Radulovic J, Birkenfeld K, Spiess J (1999) Differential impairment of auditory and contextual fear conditioning by protein synthesis inhibition in C57BL/6 N mice. Behav Neurosci 113:496–506PubMedCrossRefGoogle Scholar
  293. Stinnett GS, Seasholtz AF (2010) Stress and emotionality. In: Koob GF, Le Moal M, Tompson RF (eds) Encyclopedia of behavioral neuroscience: P-V & index. Academic Press, London, p 556Google Scholar
  294. Stockmeier CA (2003) Involvement of serotonin in depression: evidence from postmortem and imaging studies of serotonin receptors and the serotonin transporter. J Psychiatr Res 37:357–373PubMedCrossRefGoogle Scholar
  295. Storvik M, Tiihonen J, Haukijarvi T, Tupala E (2007) Amygdala serotonin transporters in alcoholics measured by whole hemisphere autoradiography. Synapse 61:629–636PubMedCrossRefGoogle Scholar
  296. Stutzmann GE, LeDoux JE (1999) GABAergic antagonists block the inhibitory effects of serotonin in the lateral amygdala: a mechanism for modulation of sensory inputs related to fear conditioning. J Neurosci 19:RC8PubMedGoogle Scholar
  297. Stutzmann GE, McEwen BS, LeDoux JE (1998) Serotonin modulation of sensory inputs to the lateral amygdala: dependency on corticosterone. J Neurosci 18:9529–9538PubMedGoogle Scholar
  298. Sur C, Betz H, Schloss P (1996) Immunocytochemical detection of the serotonin transporter in rat brain. Neuroscience 73:217–231PubMedCrossRefGoogle Scholar
  299. Swanson LW, Petrovich GD (1998) What is the amygdala? Trends Neurosci 21:323–331PubMedCrossRefGoogle Scholar
  300. Thomas DR (2006) 5-ht5A receptors as a therapeutic target. Pharmacol Ther 111:707–714PubMedCrossRefGoogle Scholar
  301. Toyoda H, Li XY, Wu LJ, Zhao MG, Descalzi G, Chen T, Koga K, Zhuo M (2011) Interplay of amygdala and cingulate plasticity in emotional fear. Neural Plast 2011:813749PubMedCrossRefGoogle Scholar
  302. Truitt WA, Johnson PL, Dietrich AD, Fitz SD, Shekhar A (2009) Anxiety-like behavior is modulated by a discrete subpopulation of interneurons in the basolateral amygdala. Neuroscience 160:284–294PubMedCrossRefGoogle Scholar
  303. Turner BH, Herkenham M (1991) Thalamoamygdaloid projections in the rat: a test of the amygdala’s role in sensory processing. J Comp Neurol 313:295–325PubMedCrossRefGoogle Scholar
  304. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev 10:397–409CrossRefGoogle Scholar
  305. Valentino RJ, Lucki I, Van Bockstaele E (2010) Corticotropin-releasing factor in the dorsal raphe nucleus: linking stress coping and addiction. Brain Res 1314:29–37PubMedCrossRefGoogle Scholar
  306. van der Veen FM, Evers EA, Deutz NE, Schmitt JA (2007) Effects of acute tryptophan depletion on mood and facial emotion perception related brain activation and performance in healthy women with and without a family history of depression. Neuropsychopharmacology 32:216–224PubMedCrossRefGoogle Scholar
  307. van Marle HJ, Hermans EJ, Qin S, Fernandez G (2009) From specificity to sensitivity: how acute stress affects amygdala processing of biologically salient stimuli. Biol Psychiatry 66:649–655PubMedCrossRefGoogle Scholar
  308. Varnas K, Halldin C, Hall H (2004) Autoradiographic distribution of serotonin transporters and receptor subtypes in human brain. Hum Brain Mapp 22:246–260PubMedCrossRefGoogle Scholar
  309. Varnas K, Hurd YL, Hall H (2005) Regional expression of 5-HT1B receptor mRNA in the human brain. Synapse 56:21–28PubMedCrossRefGoogle Scholar
  310. Veening JG (1978) Subcortical afferents of the amygdaloid complex in the rat: an HRP study. Neurosci Lett 8:197–202PubMedCrossRefGoogle Scholar
  311. Veening JG, Swanson LW, Sawchenko PE (1984) The organization of projections from the central nucleus of the amygdala to brainstem sites involved in central autonomic regulation: a combined retrograde transport-immunohistochemical study. Brain Res 303:337–357PubMedCrossRefGoogle Scholar
  312. Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555–582PubMedCrossRefGoogle Scholar
  313. Vicente MA, Zangrossi H (2011) Serotonin-2C receptors in the basolateral nucleus of the amygdala mediate the anxiogenic effect of acute imipramine and fluoxetine administration. Int J Neuropsychopharmacol 14:1–12Google Scholar
  314. Vizueta N, Patrick CJ, Jiang Y, Thomas KM, He S (2012) Dispositional fear, negative affectivity, and neuroimaging response to visually suppressed emotional faces. NeuroImage 59:761–771PubMedCrossRefGoogle Scholar
  315. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22:6810–6818PubMedGoogle Scholar
  316. Vyas A, Pillai AG, Chattarji S (2004) Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128:667–673PubMedCrossRefGoogle Scholar
  317. Vyas A, Jadhav S, Chattarji S (2006) Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 143:387–393PubMedCrossRefGoogle Scholar
  318. Waider J, Proft F, Langlhofer G, Asan E, Lesch KP, Gutknecht L (2012) GABA concentration and GABAergic neuron populations in limbic areas are differentially altered by brain serotonin deficiency in Tph2 knockout mice. Histochem Cell Biol 139(2):267–281Google Scholar
  319. Walther DJ, Bader M (2003) A unique central tryptophan hydroxylase isoform. Biochem Pharmacol 66:1673–1680PubMedCrossRefGoogle Scholar
  320. Wang DV, Wang F, Liu J, Zhang L, Wang Z, Lin L (2011) Neurons in the amygdala with response-selectivity for anxiety in two ethologically based tests. PLoS ONE 6:e18739PubMedCrossRefGoogle Scholar
  321. Waselus M, Valentino RJ, Van Bockstaele EJ (2011) Collateralized dorsal raphe nucleus projections: a mechanism for the integration of diverse functions during stress. J Chem Neuroanat 41:266–280PubMedCrossRefGoogle Scholar
  322. Weber M, Schmitt A, Wischmeyer E, Doring F (2008) Excitability of pontine startle processing neurones is regulated by the two-pore-domain K + channel TASK-3 coupled to 5-HT2C receptors. Eur J Neurosci 28:931–940PubMedCrossRefGoogle Scholar
  323. Wellman CL, Izquierdo A, Garrett JE, Martin KP, Carroll J, Millstein R, Lesch KP, Murphy DL, Holmes A (2007) Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci 27:684–691PubMedCrossRefGoogle Scholar
  324. Werry TD, Loiacono R, Sexton PM, Christopoulos A (2008) RNA editing of the serotonin 5HT2C receptor and its effects on cell signalling, pharmacology and brain function. Pharmacol Ther 119:7–23PubMedCrossRefGoogle Scholar
  325. Wills TA, Knapp DJ, Overstreet DH, Breese GR (2010) Interactions of stress and CRF in ethanol-withdrawal induced anxiety in adolescent and adult rats. Alcohol Clin Exp Res 34:1603–1612PubMedCrossRefGoogle Scholar
  326. Wilson MA, Molliver ME (1991) The organization of serotonergic projections to cerebral cortex in primates: retrograde transport studies. Neuroscience 44:555–570PubMedCrossRefGoogle Scholar
  327. Yamamoto H, Fujimiya M, Shirai Y, Nakashita M, Oyasu M, Saito N (1998) Immunohistochemical localization of serotonin transporter in normal and colchicine treated rat brain. Neurosci Res 32:305–312PubMedCrossRefGoogle Scholar
  328. Yilmazer-Hanke DM, Faber-Zuschratter H, Linke R, Schwegler H (2002) Contribution of amygdala neurons containing peptides and calcium-binding proteins to fear-potentiated startle and exploration-related anxiety in inbred Roman high- and low-avoidance rats. Eur J Neurosci 15:1206–1218PubMedCrossRefGoogle Scholar
  329. Yuen EY, Jiang Q, Chen P, Feng J, Yan Z (2008) Activation of 5-HT2A/C receptors counteracts 5-HT1A regulation of n-methyl-d-aspartate receptor channels in pyramidal neurons of prefrontal cortex. J Biol Chem 283:17194–17204PubMedCrossRefGoogle Scholar
  330. Zangrossi H Jr, Viana MB, Graeff FG (1999) Anxiolytic effect of intra-amygdala injection of midazolam and 8-hydroxy-2-(di-n-propylamino)tetralin in the elevated T-maze. Eur J Pharmacol 369:267–270PubMedCrossRefGoogle Scholar
  331. Zanoveli JM, Carvalho MC, Cunha JM, Brandao ML (2009) Extracellular serotonin level in the basolateral nucleus of the amygdala and dorsal periaqueductal gray under unconditioned and conditioned fear states: an in vivo microdialysis study. Brain Res 1294:106–115PubMedCrossRefGoogle Scholar
  332. Zhong P, Yuen EY, Yan Z (2008) Modulation of neuronal excitability by serotonin-NMDA interactions in prefrontal cortex. Mol Cell Neurosci 38:290–299PubMedCrossRefGoogle Scholar
  333. Zhou FC, Tao-Cheng JH, Segu L, Patel T, Wang Y (1998) Serotonin transporters are located on the axons beyond the synaptic junctions: anatomical and functional evidence. Brain Res 805:241–254PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Esther Asan
    • 1
  • Maria Steinke
    • 1
    • 4
  • Klaus-Peter Lesch
    • 2
    • 3
  1. 1.Institute of Anatomy and Cell BiologyUniversity of WuerzburgWuerzburgGermany
  2. 2.Division of Molecular Psychiatry, Laboratory of Translational Neuroscience, Department of Psychiatry, Psychosomatics and PsychotherapyUniversity of WuerzburgWuerzburgGermany
  3. 3.Department of Neuroscience, School for Mental Health and Neuroscience (MHENS)Maastricht UniversityER MaastrichtThe Netherlands
  4. 4.Department of Tissue Engineering and Regenerative MedicineUniversity of WuerzburgWuerzburgGermany

Personalised recommendations