Investigation of a central nucleus of the amygdala/dorsal raphe nucleus serotonergic circuit implicated in fear-potentiated startle

Neuroscience

Volumn 179, Issue , 2011, Pages 104-119

  Spannuth, B M ^a   Hale, M W ^a   Evans, A K ^a   Lukkes, J L ^a   Campeau, S ^a   Lowry, C A ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Anxiety; Fear; Fear potentiated startle; Raphe; Serotonergic; Serotonin

Indexed keywords

PROTEIN C FOS; TRYPTOPHAN HYDROXYLASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; AUDITORY STIMULATION; CENTRAL NUCLEUS (AMYGDALA); CONDITIONING; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; EMOTION; FEAR; FOOTSHOCK; IMMEDIATE EARLY GENE; LIGHT; MALE; MOTOR ACTIVITY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEROTONINERGIC NERVE CELL; SEROTONINERGIC SYSTEM; STARTLE REFLEX;

AMYGDALA; ANIMALS; CONDITIONING, CLASSICAL; FEAR; IMMUNOHISTOCHEMISTRY; MALE; NEURAL PATHWAYS; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RAPHE NUCLEI; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; STARTLE REACTION;

EID: 79952621309     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.01.042     Document Type: Article

References (90)

1. Abrams J.K., Johnson P.L., Hay-Schmidt A., Mikkelsen J.D., Shekhar A., Lowry C.A. Serotonergic systems associated with arousal and vigilance behaviors following administration of anxiogenic drugs. Neuroscience 2005, 133:983-997.
2. Abrams J.K., Johnson P.L., Hollis J.H., Lowry C.A. Anatomic and functional topography of the dorsal raphe nucleus. Ann N Y Acad Sci 2004, 1018:46-57.
3. Amat J., Tamblyn J.P., Paul E.D., Bland S.T., Amat P., Foster A.C., Watkins L.R., Maier S.F. Microinjection of urocortin 2 into the dorsal raphe nucleus activates serotonergic neurons and increases extracellular serotonin in the basolateral amygdala. Neuroscience 2004, 129:509-519.
4. Amilhon B., Lepicard E., Renoir T., Mongeau R., Popa D., Poirel O., Miot S., Gras C., Gardier A.M., Gallego J., Hamon M., Lanfumey L., Gasnier B., Giros B., El M.S. VGLUT3 (vesicular glutamate transporter type 3) contribution to the regulation of serotonergic transmission and anxiety. J Neurosci 2010, 30:2198-2210.
5. Bach-Mizrachi H., Underwood M.D., Kassir S.A., Bakalian M.J., Sibille E., Tamir H., Mann J.J., Arango V. Neuronal tryptophan hydroxylase mRNA expression in the human dorsal and median raphe nuclei: major depression and suicide. Neuropsychopharmacology 2006, 31:814-824.
6. Bach-Mizrachi H., Underwood M.D., Tin A., Ellis S.P., Mann J.J., Arango V. Elevated expression of tryptophan hydroxylase-2 mRNA at the neuronal level in the dorsal and median raphe nuclei of depressed suicides. Mol Psychiatry 2008, 13:507-513.
7. Bago M., Dean C. Sympathoinhibition from ventrolateral periaqueductal gray mediated by 5-HT(1A) receptors in the RVLM. Am J Physiol Regul Integr Comp Physiol 2001, 280:R976-R984.
8. Bago M., Marson L., Dean C. Serotonergic projections to the rostroventrolateral medulla from midbrain and raphe nuclei. Brain Res 2002, 945:249-258.
9. Bajic D., Commons K.G. Acute noxious stimulation modifies morphine effect in serotonergic but not dopaminergic midbrain areas. Neuroscience 2010, 166:720-729.
10. Barton D.A., Esler M.D., Dawood T., Lambert E.A., Haikerwal D., Brenchley C., Socratous F., Hastings J., Guo L., Wiesner G., Kaye D.M., Bayles R., Schlaich M.P., Lambert G.W. Elevated brain serotonin turnover in patients with depression: effect of genotype and therapy. Arch Gen Psychiatry 2008, 65:38-46.
11. Beck S.G., Pan Y.Z., Akanwa A.C., Kirby L.G. Median and dorsal raphe neurons are not electrophysiologically identical. J Neurophysiol 2004, 91:994-1005.
12. Boadle-Biber M.C. Further studies on the role of calcium in the depolarization-induced activation of tryptophan hydroxylase. Effect of verapamil, tetracaine, haloperidol and fluphenazine. Biochem Pharmacol 1982, 31:2495-2503.
13. Boadle-Biber M.C. Activation of tryptophan hydroxylase from central serotonergic neurons by calcium and depolarization. Biochem Pharmacol 1978, 27:1069-1079.
14. Boadle-Biber M.C., Corley K.C., Graves L., Phan T.H., Rosecrans J. Increase in the activity of tryptophan hydroxylase from cortex and midbrain of male Fischer 344 rats in response to acute or repeated sound stress. Brain Res 1989, 482:306-316.
15. Boadle-Biber M.C., Johannessen J.N., Narasimhachari N., Phan T.H. Activation of tryptophan hydroxylase by stimulation of central serotonergic neurons. Biochem Pharmacol 1983, 32:185-188.
16. Boadle-Biber M.C., Phan T.H. Involvement of calmodulin-dependent phosphorylation in the activation of brainstem tryptophan hydroxylase induced by depolarization of slices or other treatments that raise intracellular free calcium levels. Biochem Pharmacol 1987, 36:1174-1176.
17. Boadle-Biber M.C., Singh V.B., Corley K.C., Phan T.H., Dilts R.P. Evidence that corticotropin-releasing factor within the extended amygdala mediates the activation of tryptophan hydroxylase produced by sound stress in the rat. Brain Res 1993, 628:105-114.
18. Boldrini M., Underwood M.D., Mann J.J., Arango V. More tryptophan hydroxylase in the brainstem dorsal raphe nucleus in depressed suicides. Brain Res 2005, 1041:19-28.
19. Bonkale W.L., Turecki G., Austin M.C. Increased tryptophan hydroxylase immunoreactivity in the dorsal raphe nucleus of alcohol-dependent, depressed suicide subjects is restricted to the dorsal subnucleus. Synapse 2006, 60:81-85.
20. Braz J.M., Enquist L.W., Basbaum A.I. Inputs to serotonergic neurons revealed by conditional viral transneuronal tracing. J Comp Neurol 2009, 514:145-160.
21. Campeau S., Davis M. Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci 1995, 15:2301-2311.
22. Campeau S., Falls W.A., Cullinan W.E., Helmreich D.L., Davis M., Watson S.J. Elicitation and reduction of fear: behavioural and neuroendocrine indices and brain induction of the immediate-early gene c-fos. Neuroscience 1997, 78:1087-1104.
23. Christianson J.P., Ragole T., Amat J., Greenwood B.N., Strong P.V., Paul E.D., Fleshner M., Watkins L.R., Maier S.F. 5-hydroxytryptamine 2C receptors in the basolateral amygdala are involved in the expression of anxiety after uncontrollable traumatic stress. Biol Psychiatry 2010, 67:339-345.
24. Commons K.G. Evidence for topographically organized endogenous 5-HT-1A receptor-dependent feedback inhibition of the ascending serotonin system. Eur J Neurosci 2008, 27:2611-2618.
25. Commons K.G., Connolley K.R., Valentino R.J. A neurochemically distinct dorsal raphe-limbic circuit with a potential role in affective disorders. Neuropsychopharmacology 2003, 28:206-215.
26. Cox G.E., Jordan D., Paton J.F., Spyer K.M., Wood L.M. Cardiovascular and phrenic nerve responses to stimulation of the amygdala central nucleus in the anaesthetized rabbit. J Physiol 1987, 389:541-556.
27. Crawford L.K., Craige C.P., Beck S.G. Increased intrinsic excitability of lateral wing serotonin neurons of the dorsal raphe: a mechanism for selective activation in stress circuits. J Neurophysiol 2010, 103:2652-2663.
28. Davis M., Falls W.A., Campeau S., Kim M. Fear-potentiated startle: a neural and pharmacological analysis. Behav Brain Res 1993, 58:175-198.
29. Day H.E., Greenwood B.N., Hammack S.E., Watkins L.R., Fleshner M., Maier S.F., Campeau S. Differential expression of 5HT-1A, alpha(1b) adrenergic, CRF-R1, and CRF-R2 receptor mRNA in serotonergic, gamma-aminobutyric acidergic, and catecholaminergic cells of the rat dorsal raphe nucleus. J Comp Neurol 2004, 474:364-378.
30. 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. Increased brain serotonin turnover in panic disorder patients in the absence of a panic attack: reduction by a selective serotonin reuptake inhibitor. Stress 2007, 10:295-304.
31. Evans A.K., Heerkens J.L., Lowry C.A. Acoustic stimulation in vivo and corticotropin-releasing factor in vitro increase tryptophan hydroxylase activity in the rat caudal dorsal raphe nucleus. Neurosci Lett 2009, 455:36-41.
32. Forster G.L., Pringle R.B., Mouw N.J., Vuong S.M., Watt M.J., Burke A.R., Lowry C.A., Summers C.H., Renner K.J. 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 2008, 28:299-310.
33. Gardner K.L., Thrivikraman K.V., Lightman S.L., Plotsky P.M., Lowry C.A. Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience 2005, 136:181-191.
34. Grahn R.E., Will M.J., Hammack S.E., Maswood S., McQueen M.B., Watkins L.R., Maier S.F. Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res 1999, 826:35-43.
35. Gray T.S. Amygdaloid CRF pathways. Role in autonomic, neuroendocrine, and behavioral responses to stress. Ann N Y Acad Sci 1993, 697:53-60.
36. Gray T.S., Magnuson D.J. Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat. Peptides 1992, 13:451-460.
37. Grillon C., Pellowski M., Merikangas K.R., Davis M. Darkness facilitates the acoustic startle reflex in humans. Biol Psychiatry 1997, 42:453-460.
38. Grubbs F.E. Procedures for detecting outlying observations in samples. Technometrics 1969, 11:1-21.
39. Hale M.W., Hay-Schmidt A., Mikkelsen J.D., Poulsen B., Bouwknecht J.A., Evans A.K., Stamper C.E., Shekhar A., Lowry C.A. 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 2008, 157:733-748.
40. Hioki H., Nakamura H., Ma Y.F., Konno M., Hayakawa T., Nakamura K.C., Fujiyama F., Kaneko T. Vesicular glutamate transporter 3-expressing nonserotonergic projection neurons constitute a subregion in the rat midbrain raphe nuclei. J Comp Neurol 2010, 518:668-686.
41. Imai H., Steindler D.A., Kitai S.T. The organization of divergent axonal projections from the midbrain raphe nuclei in the rat. J Comp Neurol 1986, 243:363-380.
42. Johnson P.L., Lowry C.A., Truitt W., Shekhar A. Disruption of GABAergic tone in the dorsomedial hypothalamus attenuates responses in a subset of serotonergic neurons in the dorsal raphe nucleus following lactate-induced panic. J Psychopharmacol 2008, 22:642-645.
43. Kapp B.S., Gallagher M., Underwood M.D., McNall C.L., Whitehorn D. Cardiovascular responses elicited by electrical stimulation of the amygdala central nucleus in the rabbit. Brain Res 1982, 234:251-262.
44. Keay K.A., Bandler R. Parallel circuits mediating distinct emotional coping reactions to different types of stress. Neurosci Biobehav Rev 2001, 25:669-678.
45. Kerman I.A., Shabrang C., Taylor L., Akil H., Watson S.J. Relationship of presympathetic-premotor neurons to the serotonergic transmitter system in the rat brainstem. J Comp Neurol 2006, 499:882-896.
46. Kirby L.G., Rice K.C., Valentino R.J. Effects of corticotropin-releasing factor on neuronal activity in the serotonergic dorsal raphe nucleus. Neuropsychopharmacology 2000, 22:148-162.
47. Koch M., Schnitzler H.U. The acoustic startle response in rats-circuits mediating evocation, inhibition and potentiation. Behav Brain Res 1997, 89:35-49.
48. Kohler C., Steinbusch H. Identification of serotonin and non-serotonin-containing neurons of the mid-brain raphe projecting to the entorhinal area and the hippocampal formation. A combined immunohistochemical and fluorescent retrograde tracing study in the rat brain. Neuroscience 1982, 7:951-975.
49. Kovacs K.J. c-Fos as a transcription factor: a stressful (re)view from a functional map. Neurochem Int 1998, 33:287-297.
50. Lee H.S., Kim M.A., Valentino R.J., Waterhouse B.D. Glutamatergic afferent projections to the dorsal raphe nucleus of the rat. Brain Res 2003, 963:57-71.
51. Lee Y., Davis M. Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. J Neurosci 1997, 17:6434-6446.
52. Li Y.-Q., Jai H.-G., Rao Z.-R., Shi J.-W. Serotonin-, substance P- or leucine-enkephalin-containing neurons in the midbrain periaqueductal gray and nucleus raphe dorsalis send projection fibers to the central amygdaloid nucleus in the rat. Neurosci Lett 1990, 120:124-127.
53. Liu Y, Dwork AJ, Bakalian MJ, Ilievski G, Arango V (2009) Distribution of calbindin-immunoreactive neurons in the amygdala and its subnuclei: a post mortem study of depressed suicides. In: Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, Online. Program No. 156.5. 2009.
54. Lowry C.A., Evans A.K., Gasser P.J., Hale M.W., Staub D.R., Shekhar A. Topographical organization and chemoarchitecture of the dorsal raphe nucleus and the median raphe nucleus. Serotonin and Sleep: Molecular, Functional and Clinical Aspects 2008, 25-68. Birkhauser, Basel. J.M. Monti, B.L. Pandi-Perumal, B.L. Jacobs, D.L. Nutt (Eds.).
55. Lowry C.A., Hale M.W. Serotonin and the neurobiology of anxious states. The Behavioural Neurobiology of Serotonin 2010, Elsevier, Amsterdam. C.P. 'ller, B.L. Jacobs (Eds.).
56. Lowry C.A., Hale M.W., Evans A.K., Heerkens J., Staub D.R., Gasser P.J., Shekhar A. Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 2008, 1148:86-94.
57. Lowry C.A., Johnson P.L., Hay-Schmidt A., Mikkelsen J., Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 2005, 8:233-246.
58. Lowry C.A., Rodda J.E., Lightman S.L., Ingram C.D. Corticotropin-releasing factor increases in vitro firing rates of serotonergic neurons in the rat dorsal raphe nucleus: evidence for activation of a topographically organized mesolimbocortical serotonergic system. J Neurosci 2000, 20:7728-7736.
59. Lukkes J.L., Forster G.L., Renner K.J., Summers C.H. Corticotropin-releasing factor 1 and 2 receptors in the dorsal raphe differentially affect serotonin release in the nucleus accumbens. Eur J Pharmacol 2008, 578:185-193.
60. Masini C.V., Day H.E., Campeau S. Long-term habituation to repeated loud noise is impaired by relatively short interstressor intervals in rats. Behav Neurosci 2008, 122:210-223.
61. McEuen JG, Bale TL (2006) Chronic stress induces alterations in serotonin-related gene expression in a model of CRF dysregulation. In: 2006 Neuroscience Meeting Planner. Atlanta, GA: Society for Neuroscience. Online. 501.1.2006.
62. Meloni E.G., Reedy C.L., Cohen B.M., Carlezon W.A. Activation of raphe efferents to the medial prefrontal cortex by corticotropin-releasing factor: correlation with anxiety-like behavior. Biol Psychiatry 2007, 63:832-839.
63. Morimoto M., Morita N., Ozawa H., Yokoyama K., Kawata M. Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: an immunohistochemical and in situ hybridization study. Neurosci Res 1996, 26:235-269.
64. Neugebauer V., Li W., Bird G.C., Han J.S. The amygdala and persistent pain. Neuroscientist 2004, 10:221-234.
65. Ottersen O.P. 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 1981, 202:335-356.
66. Paxinos G., Carrive P., Wang H., Wang P.-Y. Chemoarchitectonic atlas of the rat brainstem 1999, Academic Press, San Diego.
67. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego. 4th edition.
68. Pernar L., Curtis A.L., Vale W.W., Rivier J.E., Valentino R.J. Selective activation of corticotropin-releasing factor-2 receptors on neurochemically identified neurons in the rat dorsal raphe nucleus reveals dual actions. J Neurosci 2004, 24:1305-1311.
69. Perroud N., Neidhart E., Petit B., Vessaz M., Laforge T., Relecom C., La H.R., Malafosse A., Guipponi M. Simultaneous analysis of serotonin transporter, tryptophan hydroxylase 1 and 2 gene expression in the ventral prefrontal cortex of suicide victims. Am J Med Genet B Neuropsychiatr Genet 2010, 153B:909-918.
70. Petit J.-M., Luppi P.-H., Peyron C., Rampon C., Jouvet M. VIP-like immunoreactive projections from the dorsal raphe and caudal linear nuclei to the bed nucleus of the stria terminalis demonstrated by a double immunohistochemical method in the rat. Neurosci Lett 1995, 193:77-80.
71. Peyron C., Luppi P.H., Fort P., Rampon C., Jouvet M. Lower brainstem catecholamine afferents to the rat dorsal raphe nucleus. J Comp Neurol 1996, 364:402-413.
72. Peyron C., Petit J.-M., Rampon C., Jouvet M., Luppi P.-H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 1998, 82:443-468.
73. Porter K., Hayward L.F. Stress-induced changes in c-Fos and corticotropin releasing hormone immunoreactivity in the amygdala of the spontaneously hypertensive rat. Behav Brain Res 2011, 216:543-551.
74. Rasmussen K., Heym J., Jacobs B.L. Activity of serotonin-containing neurons in nucleus centralis superior of freely moving cats. Exp Neurol 1984, 83:302-317.
75. Rizvi T.A., Ennis M., Behbehani M.M., Shipley M.T. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol 1991, 303:121-131.
76. Sakanaka M.S.T., Lederis K. Distribution and efferent projections of corticotropin-releasing factor-like immunoreactivity in the rat amygdaloid complex. Brain Res 1986, 382:213-238.
77. Schweimer J., Fendt M., Schnitzler H.U. Effects of clonidine injections into the bed nucleus of the stria terminalis on fear and anxiety behavior in rats. Eur J Pharmacol 2005, 507:117-124.
78. Singh V.B., Hao-Phan T., Corley K.C., Boadle-Biber M.C. Increase in cortical and midbrain tryptophan hydroxylase activity by intracerebroventricular administration of corticotropin releasing factor: block by adrenalectomy, by RU 38486 and by bilateral lesions to the central nucleus of the amygdala. Neurochem Int 1992, 20:81-92.
79. Staub D.R., Evans A.K., Lowry C.A. Evidence supporting a role for corticotropin-releasing factor type 2 (CRF2) receptors in the regulation of subpopulations of serotonergic neurons. Brain Res 2006, 1070:77-89.
80. Staub D.R., Spiga F., Lowry C.A. Urocortin 2 increases c-Fos expression in topographically organized subpopulations of serotonergic neurons in the rat dorsal raphe nucleus. Brain Res 2005, 1044:176-189.
81. Steinbusch H.W., van der Kooy D., Verhofstad A.A., Pellegrino A. Serotonergic and non-serotonergic projections from the nucleus raphe dorsalis to the caudate-putamen complex in the rat, studied by a combined immunofluorescence and fluorescent retrograde axonal labeling technique. Neurosci Lett 1980, 19:137-142.
82. Takase L.F., Nogueira M.I., Baratta M., Bland S.T., Watkins L.R., Maier S.F., Fornal C.A., Jacobs B.L. Inescapable shock activates serotonergic neurons in all raphe nuclei of rat. Behav Brain Res 2004, 153:233-239.
83. Takase L.F., Nogueira M.I., Bland S.T., Baratta M., Watkins L.R., Maier S.F., Fornal C.A., Jacobs B.L. Effect of number of tailshocks on learned helplessness and activation of serotonergic and noradrenergic neurons in the rat. Behav Brain Res 2005, 162:299-306.
84. Underwood M.D., Arango V., Bakalian M.J., Ruggiero D.A., Mann J.J. Dorsal raphe nucleus serotonergic neurons innervate the rostral ventrolateral medulla in rat. Brain Res 1999, 824:45-55.
85. Underwood M.D., Khaibulina A.A., Ellis S.P., Moran A., Rice P.M., Mann J.J., Arango V. Morphometry of the dorsal raphe nucleus serotonergic neurons in suicide victims. Biol Psychiatry 1999, 46:473-483.
86. Van Bockstaele E.J., Biswas A., Pickel V.M. Topography of serotonin neurons in the dorsal raphe nucleus that send axon collaterals to the rat prefrontal cortex and nucleus accumbens. Brain Res 1993, 624:188-198.
87. Vandermaelen C.P., Aghajanian G.K. Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat brain slices. Brain Res 1983, 289:109-119.
88. Walker D.L., Davis M. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 1997, 17:9375-9383.
89. Walker D.L., Toufexis D.J., Davis M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 2003, 463:199-216.
90. Wilensky A.E., Schafe G.E., Kristensen M.P., LeDoux J.E. Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci 2006, 26:12387-12396.