The anxiogenic drug yohimbine activates central viscerosensory circuits in rats

Journal of Comparative Neurology

Volumn 492, Issue 4, 2005, Pages 426-441

  Myers, Elizabeth A ^a   Banihashemi, Layla ^a   Rinaman, Linda ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Amygdala; Bed nucleus of the stria terminalis; Noradrenergic; Nucleus of the solitary tract; Parabrachial nucleus; Paraventricular nucleus of the hypothalamus; Ventrolateral medulla

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; PROTEIN FOS; YOHIMBINE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ANXIETY; ARTICLE; AVERSION; BRAIN MAPPING; BRAIN STEM; CENTRAL NERVOUS SYSTEM; CENTRAL VISCEROSENSORY SYSTEM; CONTROLLED STUDY; FLAVOR; FOOD INTAKE; FOREBRAIN; HYPOTHALAMUS; LIMBIC CORTEX; MALAISE; MALE; MEDULLA OBLONGATA; NONHUMAN; NORADRENERGIC NERVE; PEPTIDERGIC NERVOUS SYSTEM; PONS; PRIORITY JOURNAL; RAT; STRESS; STRIA TERMINALIS; VENTROLATERAL MEDULLA;

ADRENERGIC ALPHA-ANTAGONISTS; AFFERENT PATHWAYS; ANIMALS; ANOREXIA; AVOIDANCE LEARNING; BRAIN; EATING; FOOD DEPRIVATION; MALE; NEURAL PATHWAYS; NEURONS, AFFERENT; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; TASTE; VISCERA; YOHIMBINE;

EID: 27644494282     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20727     Document Type: Article

References (83)

1. Aghajanian GK, VanderMaelen CP. 1982. Alpha 2-adrenoceptor-mediated hyperpolarization of locus coeruleus neurons: intracellular studies in vivo. Science 215:1394-1396.
2. Aston-Jones G, Delfs JM, Druhan J, Zhu Y. 1999. The bed nucleus of the stria terminalis: a target site for noradrenergic actions in opiate withdrawal. Ann N Y Acad Sci 877:486-498.
3. Bhattacharya SK, Satyan KS, Chakrabarti A. 1997. Anxiogenic action of caffeine: an experimental study in rats. J Psychopharmacol 11:219-224.
4. Bing C, Stone EA, Zhang Y, Filer D. 1992. Immunohistochemical studies of noradrenergic-induced expression of c-fos in the rat CNS. Brain Res 592:57-62.
5. Brambilla F. 2001. Social stress in anorexia nervosa: a review of immunoendocrine relationships. Physiol Behav 73:365-369.
6. Buller KM, Dayas CV, Day TA. 2003. Descending pathways from the paraventricular nucleus contribute to the recruitment of brainstem nuclei following a systemic immune challenge. Neuroscience 118:189-203.
7. Callahan MF, Beales M, Oltmans GA. 1984. Yohimbine and rauwolscine reduce food intake of genetically obese (ob/ob) and lean mice. Pharmacol Biochem Behav 20:591-599.
8. Charney DS, Deutch A. 1996. A functional neuroanatomy of anxiety and fear: implications for the pathophysiology and treatment of anxiety disorders. Crit Rev Neurobiol 10:419-446.
9. Charney DS, Heninger GR, Redmond J. 1983. Yohimbine induced anxiety and increased noradrenergic function in humans: effects of diazepam and clonidine. Life Sci 33:19-29.
10. Charney DS, Woods SW, Heninger GR. 1989. Noradrenergic function in generalized anxiety disorder: effects of yohimbine in healthy subjects and patients with generalized anxiety disorder. Psychiatry Res 27:173-182.
11. Clayton EC, Williams CL. 2000. Adrenergic activation of the nucleus tractus solitarius potentiates amygdala norepinephrine release and enhances retention performance in emotionally arousing and spatial memory tasks. Behav Brain Res 112:151-158.
12. Corre PL, Palmer RJ, Kailasam MT, Kennedy BP, Skaar TP, Ho H, Leverge R, Smith DW, Ziegler MG, Insel PA, Schork NJ, Flockhart DA, O'Connor DT. 2004. Human sympathetic activation by alpha2-adrenergic blockade with yohimbine: bimodal, epistatic influence of cytochrome P450-mediated drug metabolism. Clin Pharmacol Ther 76:139-153.
13. Dayas CV, Day TA. 2001. Opposing roles for medial and central amygdala in the initiation of noradrenergic cell responses to a psychological stressor. Eur J Neurosci 15:1712-1718.
14. Dayas CV, Buller KM, Day TA. 2004. Hypothalamic paraventricular nucleus neurons regulate medullary catecholamine cell responses to restraint stress. J Comp Neurol 478:22-34.
15. Delfs JM, Zhu Y, Druhan JP, Aston-Jones G. 2000. Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion. Nature 403:430-434.
16. Deutsch JA, Hardy WT. 1977. Cholecystokinin produces bait shyness in rats. Nature 266:196.
17. Elmquist JK, Saper CB. 1996. Activation of neurons projecting to the paraventricular hypothalamic nucleus by intravenous lipopolysaccharide. J Comp Neurol 374:315-331.
18. Elmquist JK, Scammell TE, Jacobson CD, Saper CB. 1996. Distribution of fos-like immunoreactivity in the rat brain following intravenous lipopoysaccharide administration. J Comp Neurol 371:85-103.
19. Ericsson A, Kovacs KJ, Sawchenko PE. 1994. A functional anatomical analysis of central pathways subserving the effects of interleukin-1 on stress-related neuroendocrine neurons. J Neurosci 14:897-913.
20. File SE. 1986. Aversive and appetitive properties of anxiogenic and anxiolytic agents. Behav Brain Res 21:189-194.
21. File SE, Seth P. 2003. A review of 25 years of the social interaction test. Eur J Pharmacol 463:35-53.
22. Forray MI, Bustos G, Gysling K. 1997. Regulation of norepinephrine release from the rat bed nucleus of the stria terminalis: in vivo microdialysis studies. J Neurosci Res 50:1040-1046.
23. Gerra G, Zaimovic A, Zambelli U, Timpano M, Reali N, Bernasconi S, Brambilla F. 2000. Neuroendocrine responses to psychological stress in adolescents with anxiety disorder. Neuropsychobiology 42:82-92.
24. Gurguis GNM, Vitton BJ, Uhde TW. 1997. Behavioral, sympathetic and adrenocortical responses to yohimbine in panic disorder patients and normal controls. Psychiatry Res 71:27-39.
25. Hoffman GE, Smith MS, Verbalis JG. 1993. c-Fos and related immediate early gene products as markers of activity in neuroendocrine systems. Front Neuroendocrinol 14:173-213.
26. Hubbard JW, Pfister SL, Biediger AM, Herzig TC, Keeton TK. 1988. The pharmacokinetic properties of yohimbine in the conscious rat. Naunyn Schmiedebergs Arch Pharmacol 337:583-587.
27. Jones BE, Yang T-Z. 1985. The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242:56-92.
28. Khoshbouei H, Cecchi M, Dove S, Javors M, Morilak DA. 2002. Behavioral reactivity to stress: amplification of stress-induced noradrenergic activation elicits a galanin-mediated anxiolytic effect in central amygdala. Pharmacol Biochem Behav 71:407-417.
29. Kiem DT, Barna I, Koenig JI, Makara GB. 1995. Adrenocorticotropin, prolactin and beta-endorphin stimulatory actions of alpha-2-adrenoceptor antagonists. Neuroendocrinology 61:152-158.
30. Kusnecov AW, Goldfarb Y. 2005. Neural and behavioral responses to systemic immunologic stimuli: a consideration of bacterial T cell superantigens. Curr Pharm Design 11:1039-1046.
31. Lacosta S, Merali Z, Anisman H. 1999. Behavioral and neurochemical consequences of lipopolysaccharide in mice: anxiogenic-like effects. Brain Res 818:291-303.
32. Lasiter PS, Glanzman DL. 1985. Cortical substrates of taste aversion learning: involvement of dorsolateral amygdaloid nuclei and temporal neocortex in taste aversion learning. Behav Neurosci 99:257-276.
33. Li H-Y, Ericsson A, Sawchenko PE. 1996. Distinct mechanisms underlie activation of hypothalamic neurosecretory neurons and their medullary catecholaminergic afferents in categorically different stress paradigms. Proc Natl Acad Sci U S A 93:2359-2364.
34. Linden CH, Vellman WP, Rumack B. 1985. Yohimbine: a new street drug. Ann Emerg Med 14:1002-1004.
35. Malcolm A, Camilleri M, Kost L, Burton DD, Fett SL, Zinsmeister AR. 2000. Toward identifying optimal doses for alpha-2 adrenergic modulation of colonic and rectal motor and sensory function. Aliment Pharmacol Ther 14:783-793.
36. Mattila M, Seppala T, Mattila MJ. 1988. Anxiogenic effect of yohimbine in healthy subjections: comparison with caffeine and antagonism by clonidine and diazepam. Int Clin Psychopharmacol 3:215-229.
37. McGaugh JL. 2000. Memory-a century of consolidation. Science 287:248-251.
38. McLean IW, Nakane PK. 1974. Periodate-lysine-paraformldehyde fixative. A new fixative for immunoelectron microscopy. J Histochem Cytochem 22:1077-1083.
39. Morgan JI, Curran T. 1991. Stimulus-transcription coupling in the nervous system: involvement of the inducible protooncogenes fos and jun. Annu Rev Neurosci 14:421-451.
40. Myers EA, Rinaman L. 2005. Trimethylthiazoline (TMT) supports conditioned flavor avoidance and activates viscerosensory, hypothalamic, and limbic circuits in rats. Am J Physiol Regul Integr Comp Physiol 288:R1716-R1726.
41. Nandi J, Meguid MM, Inui A, Xu Y, Makarenko IG, Tada T, Chen C. 2002. Central mechanisms involved with catabolism. Curr Opin Clin Nutr Metab Care 5:407-418.
42. Nava F, Carta G. 2001. Melatonin reduces anxiety induced by lipopolysaccharide in the rat. Neurosci Lett 307:57-60.
43. Nutt DJ. 1990. The pharmacology of human anxiety. Pharmacol Ther 47:233-266.
44. Pacak K, Armando I, Komoly S, Fukuhara K, Weise VK, Holmes C, Kopin IJ, Goldstein DS. 1992. Hypercortisolemia inhibits yohimbine-induced release of norepinephrine in the posterolateral hypothalamus of conscious rats. Endocrinology 131:1369-1376.
45. Pacak K, McCarty R, Palkovits M, Kopin IJ, Goldstein DS. 1995. Effects of immobilization on in vivo release of norepinephrine in the bed nucleus of the stria terminalis in conscious rats. Brain Res 688:242-246.
46. Parker LA. 2003. Taste avoidance and taste aversion: evidence for two different processes. Learn Behav 31:165-172.
47. Paxinos G, Watson C. 1997. The rat brain in stereotaxic coordinates. San Diego: Academic Press.
48. Pellow S, Chopin P, File SE, Briley M. 1985. Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149-167.
49. Petrov T, Krukoff TL, Jhamandas JH. 1993. Branching projections of catecholaminergic brainstem neurons to the paraventricular hypothalamic nucleus and the central nucleus of the amygdala in the rat. Brain Res 609:81-92.
50. Petrov T, Krukoff TL, Jhamandas JH. 1995. Convergent influence of the central nucleus of the amygdala and the paraventricular hypothalamic nucleus upon brainstem autonomic neurons as revealed by c-fos expression and anatomical tracing. J Neurosci Res 42:835-845.
51. Reilly S. 1999. The parabrachial nucleus and conditioned taste aversion. Brain Res Bull 48:239-254.
52. Riche D, Pommery JD, Menetrey D. 1990. Neuropeptides and catecholamines in efferent projections of the nuclei of the solitary tract in the rat. J Comp Neurol 293:399-424.
53. Rinaman L, Stricker EM, Hoffman GE, Verbalis JG. 1997. Central c-fos expression in neonatal and adult rats after subcutaneous injection of hypertonic saline. Neuroscience 79:1165-1175.
54. Roder S, Ciriello J. 1993. Innervation of the amygdaloid complex by catecholaminergic cell groups of the ventrolateral medulla. J Comp Neurol 332:105-122.
55. Roder S, Ciriello J. 1994. Collateral axonal projections to limbic structures from ventrolateral medullary A1 noradrenergic neurons. Brain Res 638:182-188.
56. Sakai N, Yamamoto T. 1999. Possible routes of visceral information in the rat brain in formation of conditioned taste aversion. Neurosci Res 35:53-61.
57. Sawchenko PE, Swanson LW. 1982. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res Rev 4:275-325.
58. Schroeder BE, Schiltz CA, Kelley AE. 2003. Neural activation profile elicited by cues associated with the anxiogenic drug yohimbine differs from that observed for reward-paired cues. Neuropsychopharmacology 28:14-21.
59. Schroeter S, Apparsundaram S, Wiley RG, Miner LH, Sesack SR, Blakely RD. 2000. Immunolocalization of the cocaine- and antidepressant-sensitive 1-norepinephrine transporter. J Comp Neurol 420:211-232.
60. Shaham Y, Erb S, Stewart J. 2000a. Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Rev 33:13-33.
61. Shaham Y, Highfield D, Delfs J, Leung S, Stewart J. 2000b. Clonidine blocks stress-induced reinstatement of heroin seeking in rats: an effect independent of locus coeruleus noradrenergic neurons. Eur J Neurosci 12:292-302.
62. Shepard JD, Bossert JM, Liu SY, Shaham Y. 2004. The anxiogenic drug yohimbine reinstates methamphetamine seeking in a rat model of drug relapse. Biol Psychiatry 55:1082-1089.
63. Singewald N, Sharp T. 2000. Neuroanatomical targets of anxiogenic drugs in the hindbrain as revealed by Fos immunocytochemistry. Neuroscience 98:759-770.
64. Singewald N, Salchner P, Sharp T. 2003. Induction of c-Fos expression in specific areas of the fear circuitry in rat forebrain by anxiogenic drugs. Biol Psychiatry 53:275-283.
65. Smith MA, Kling MA, Whitfield HJ, Brandt HA, Demitrack MA, Geracioti TD, Chrousos GP, Gold PW. 1989. Corticotropin-releasing hormone: from endocrinology to psychobiology. Horm Res 31:66-71.
66. Southwick SM, Bremner JD, Rasmusson A, Morgan CA, Arnsten A, Charney DS. 1999. Role of norepinephrine in the pathophysiology and treatment of posttraumatic stress disorder. Biol Psychiatry 46:1192-1204.
67. Stine SM, Grillon CG, Morgan CA, Kosten TR, Charney DS, Krystal JH. 2001. Methadone patients exhibit increased startle and cortisol response after intravenous yohimbine. Psychopharmacology 154:274-281.
68. Stine SM, Southwick SM, Petrakis IL, Kosten TR, Charney DS, Krystal JH. 2002. Yohimbine-induced withdrawal and anxiety symptoms in opioid-dependent patients. Biol Psychiatry 51:642-651.
69. Stone EA, Zhang Y, John S, Filer D, Bing G. 1993. Effect of locus coeruleus lesion on c-fos expression in the cerebral cortex caused by yohimbine injection or stress. Brain Res 603:181-185.
70. Szemeredi K, Komoly S, Kopin IJ, Bagdy G, Keiser HR, Goldstein DS. 1991. Simultaneous measurement of plasma and brain extracellular fluid concentrations of catechols after yohimbine administration in rats. Brain Res 542:8-14.
71. Tanaka M, Yoshida M, Emoto H, Ishii H. 2000. Noradrenaline systems in the hypothalamus, amygdala and locus coeruleus are involved in the provocation of anxiety: basic studies. Eur J Pharmacol 405:397-406.
72. Terenzi MG, Ingram CD. 1995. A combined immunocytochemical and retrograde tracing study of noradrenergic connections between the caudal medulla and bed nucleus of the stria terminalis. Brain Res 672:289-297.
73. Tsujino T, Sano H, Kubota Y, Hsieh S-T, Miyajima T, Saito K, Nakajima M, Saito N, Yokoyama M. 1992. Expression of Fos-like immunoreactivity by yohimbine and clonidine in the rat brain. Eur J Pharmacol 226:69-78.
74. Wada T, Fukada N. 1991. Effects of DN-2327, a new anxiolytic, diazepam and buspirone on exploratory activity of the rat in an elevated plus-maze. Psychopharmacology 104:444-450.
75. Watson RE, Wiegand ST, Clough RW, Hoffman GE. 1986. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7:155-159.
76. White DA, Birkle DL. 2001. The differential effects of prenatal stress in rats on the acoustic startle reflex under baseline conditions and in response to anxiogenic drugs. Psychopharmacology 154:169-176.
77. Williams CL, Men D, Clayton EC. 2000. The effects of noradrenergic activation of the nucleus tractus solitarius on memory and potentiating norepinephrine release in the amygdala. Behav Neurosci 114:1131-1144.
78. Woulfe JM, Hrycyshyn AW, Flumerfelt BA. 1988. Collateral axonal projections from the A1 noradrenergic cell group to the paraventricular nucleus and bed nucleus of the stria terminalis in the rat. Exp Neurol 102:121-124.
79. Woulfe JM, Flumerfelt BA, Hrycyshyn AW. 1990. Efferent connections of the A1 noradrenergic cell group: a DBH immunohistochemical and PHA-L anterograde tracing study. Exp Neurol 109:308-322.
80. Yamamoto T, Shimura T, Sako N, Yasoshima Y, Sakai N. 1994. Neurol substrates for conditioned taste aversion in the rat. Behav Brain Res 65:123-137.
81. Yirmiya R, Pollak Y, Morag M, Reichenberg A, Barak O, Avitsur R, Shavit Y, Ovadia H, Weidenfeld J, Morag A, Mahal A. 2000. Illness, cytokines, and depression. Ann N Y Acad Sci 917:478-487.
82. Zardetto-Smith AM, Gray TS. 1990. Organization of peptidergic and catecholaminergic efferents from the nucleus of the solitary tract to the rat amygdala. Brain Res Bull 25:875-887.
83. Zardetto-Smith AM, Gray TS. 1995. Catecholamine and NPY efferents from the ventrolateral medulla to the amygdala in the rat. Brain Res Bull 38:253-260.