Fear, anxiety, and control in the zebrafish

Developmental Neurobiology

Volumn 72, Issue 3, 2012, Pages 395-403

  Jesuthasan, Suresh ^a,b,c  

^a Agency for Science   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

Anxiety; Fear; Habenula; Interpeduncular nucleus

Indexed keywords

ANXIETY; ARTICLE; DOWN REGULATION; EMOTION; FEAR; HABENULA; INTERPEDUNCULAR NUCLEUS; LEARNING; MAMMAL; NERVOUS SYSTEM POTENTIAL; NONHUMAN; PRIORITY JOURNAL; SEPTUM NUCLEUS; ZEBRA FISH;

ANIMALS; ANXIETY; CONDITIONING, CLASSICAL; FEAR; HABENULA; HUMANS; NERVE NET; ZEBRAFISH;

EID: 84856977139     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20873     Document Type: Article

References (78)

1. Adolphs R, Tranel D, Damasio H, Damasio A. 1995. Fear and the human amygdala. J Neurosci 15: 5879-5891.
2. Agetsuma M, Aizawa H, Aoki T, Nakayama R, Takahoko M, Goto M, Sassa T, et al. 0000 The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci 13: 1354-1356.
3. Alderman SL, Bernier NJ. 2007. Localization of corticotropin-releasing factor, urotensin I, and CRF-binding protein gene expression in the brain of the zebrafish, Danio rerio. J Comp Neurol 502: 783-793.
4. 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: 365-371.
5. Amat J, Matus-Amat P, Watkins LR, Maier SF. 1998. Escapable and inescapable stress differentially and selectively alter extracellular levels of 5-HT in the ventral hippocampus and dorsal periaqueductal gray of the rat. Brain Res 797: 12-22.
6. Amo R, Aizawa H, Takahoko M, Kobayashi M, Takahashi R, Aoki T, Okamoto H. 2010. Identification of the zebrafish ventral habenula as a homolog of the mammalian lateral habenula. J Neurosci 30: 1566-1574.
7. Applegate CD, Frysinger RC, Kapp BS, Gallagher M. 1982. Multiple unit activity recorded from amygdala central nucleus during Pavlovian heart rate conditioning in rabbit. Brain Res 238: 457-462.
8. Asakawa K, Suster ML, Mizusawa K, Nagayoshi S, Kotani T, Urasaki A, Kishimoto Y, et al. 2008. Genetic dissection of neural circuits by Tol2 transposon-mediated Gal4 gene and enhancer trapping in zebrafish. Proc Natl Acad Sci USA 105: 1255-1260.
9. Bechara A, Damasio H, Damasio AR. 2000. Emotion, decision making and the orbitofrontal cortex. Cereb Cortex 10: 295-307.
10. Bencan Z, Sledge D, Levin ED. 2009. Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety. Pharmacol Biochem Behav 94: 75-80.
11. Bianco IH, Wilson SW. 2009. The habenular nuclei: A conserved asymmetric relay station in the vertebrate brain. Philos Trans R Soc Lond B Biol Sci 364: 1005-1020.
12. Blanchard DC, Blanchard RJ. 1972. Innate and conditioned reactions to threat in rats with amygdaloid lesions. J Comp Physiol Psychol 81: 281-290.
13. Blanchard RJ, Yudko EB, Rodgers RJ, Blanchard DC. 1993. Defense system psychopharmacology: An ethological approach to the pharmacology of fear and anxiety. Behav Brain Res 58: 155-165.
14. Blaser RE, Chadwick L, McGinnis GC. 2009. Behavioral measures of anxiety in zebrafish (Danio rerio). Behav Brain Res 208: 56-62.
15. Champagne DL, Hoefnagels CC, de Kloet RE, Richardson MK. 2010. Translating rodent behavioral repertoire to zebrafish (Danio rerio): Relevance for stress research. Behav Brain Res 214: 332-342.
16. Cook M, Dunning J, Wiley R, Chesler E, Johnson D, Miller D, Goldowitz D. 2007. Neurobehavioral mutants identified in an ENU-mutagenesis project. Mammalian Genome 18: 559-572.
17. Davis M, Walker DL, Miles L, Grillon C. 2010. Phasic vs. sustained fear in rats and humans: role of the extended amygdala in fear vs. anxiety. Neuropsychopharmacology 35: 105-135.
18. Dieterich DC, Hodas JJL, Gouzer G, Shadrin IY, Ngo JT, Triller A, Tirrell DA, et al. 2010. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat Neurosci 13: 897-905.
19. Dunn AJ, Berridge CW. 1990. Physiological and behavioral responses to corticotropin-releasing factor administration: Is CRF a mediator of anxiety or stress responses? Brain Res Brain Res Rev 15: 71-100.
20. Egan R, Bergner C, Hart P, Cachat J, Canavello P, Elegante M, Elkhayat S, et al. 2009. Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 38-44.
21. Fanselow MS. 1994. Neural organization of the defensive behavior system responsible for fear. Psychonomic Bull Rev 1: 429-438.
22. Flik G, Klaren PH, Van den Burg EH, Metz JR, Huising MO. 2006. CRF and stress in fish. Gen Comp Endocrinol 146: 36-44.
23. Gerlai R. 2010. High-throughput behavioral screens: The first step towards finding genes involved in vertebrate brain function using zebrafish. Molecules 15: 2609-2622.
24. Grewe BF, Helmchen F. 2009. Optical probing of neuronal ensemble activity. Curr Opin Neurobiol 19: 520-529.
25. Grillon C, Chavis C, Covington MF, Pine DS. 2009. Two-week treatment with the selective serotonin reuptake inhibitor citalopram reduces contextual anxiety but not cued fear in healthy volunteers: A fear-potentiated startle study. Neuropsychopharmacology 34: 964-971.
26. Guo S. 2009. Using zebrafish to assess the impact of drugs on neural development and function. Expert Opin Drug Discov 4: 715-726.
27. Hammack SE, Richey KJ, Schmid MJ, LoPresti ML, Watkins LR, Maier SF. 2002. The role of corticotropin-releasing hormone in the dorsal raphe nucleus in mediating the behavioral consequences of uncontrollable stress. J Neurosci 22: 1020-1026.
28. Herkenham M, Nauta WJ. 1977. Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173: 123-146.
29. Herkenham M, Nauta WJ. 1979. Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187: 19-47.
30. Hitchcock JM, Davis M. 1991. Efferent pathway of the amygdala involved in conditioned fear as measured with the fear-potentiated startle paradigm. Behav Neurosci 105: 826-842.
31. Hong S, Hikosaka O. 2008. The globus pallidus sends reward-related signals to the lateral habenula. Neuron 60: 720-729.
32. Jesuthasan S, Mathuru A. 2008. The alarm response in zebrafish: innate fear in a vertebrate genetic model. J Neurogenetics 22: 211-228.
33. Jhou TC, Fields HL, Baxter MG, Saper CB, Holland PC. 2009. The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61: 786-800.
34. Johansen JP, Hamanaka H, Monfils MH, Behnia R, Deisseroth K, Blair HT, LeDoux JE. 2010. Optical activation of lateral amygdala pyramidal cells instructs associative fear learning. Proc Natl Acad Sci 107: 12692-12697.
35. Kapp BS, Frysinger RC, Gallagher M, Haselton JR. 1979. Amygdala central nucleus lesions: Effect on heart rate conditioning in the rabbit. Physiol Behav 23: 1109-1117.
36. Klemm WR. 2004. Habenular and interpeduncularis nuclei: Shared components in multiple-function networks. Med Sci Monit 10: RA261-RA273.
37. Kokel D, Peterson RT. 2008. Chemobehavioural phenomics and behaviour-based psychiatric drug discovery in the zebrafish. Brief Funct Genomics Proteomics 7: 483-490.
38. LeDoux JE. 2000. Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
39. LeDoux JE, Cicchetti P, Xagoraris A, Romanski L. 1990. The lateral amygdaloid nucleus: Sensory interface of the amygdala in fear conditioning. J Neurosci 10: 1062-1069.
40. 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: 2517-2529.
41. Lee A, Mathuru AS, Teh C, Kibat C, Korzh V, Penney TB, Jesuthasan S. 2010. The habenula prevents helpless behavior in larval zebrafish. Curr Biol 20: 2211-2216.
42. Liang KC, Melia KR, Miserendino MJ, Falls WA, Campeau S, Davis M. 1992. Corticotropin-releasing factor: Long-lasting facilitation of the acoustic startle reflex. J Neurosci 12: 2303-2312.
43. Lillesaar C, Stigloher C, Tannhäuser B, Wullimann MF, Bally-Cuif L. 2009. Axonal projections originating from raphe serotonergic neurons in the developing and adult zebrafish, Danio rerio, using transgenics to visualize raphe-specific pet1 expression. J Comp Neurol 512: 158-182.
44. Ma PM. 1994. Catecholaminergic systems in the zebrafish. I. Number, morphology, and histochemical characteristics of neurons in the locus coeruleus. J Comp Neurol 344: 242-255.
45. Maier SF, Seligman ME. 1976. Learned helplessness: Theory and evidence. J Exp Psychol Gen 105: 3-46.
46. Markova O, Mukhtarov M, Real E, Jacob Y, Bregestovski P. 2008. Genetically encoded chloride indicator with improved sensitivity. J Neurosci Methods 170: 67-76.
47. Marks MJ, Smith KW, Collins AC. 1998. Differential agonist inhibition identifies multiple epibatidine binding sites in mouse brain. J Pharmacol Exp Therap 285: 377-386.
48. Matsumoto M, Hikosaka O. 2007. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447: 1111-1115.
49. Matsumoto M, Hikosaka O. 2009. Representation of negative motivational value in the primate lateral habenula. Nat Neurosci 12: 77-84.
50. Maximino C, de Brito TM, Colmanetti R, Pontes AAA, de Castro HM, de Lacerda RIT, Morato S, et al. 2010a. Parametric analyses of anxiety in zebrafish scototaxis. Behav Brain Res 210: 1-7.
51. Maximino C, de Brito TM, da Silva Batista AW, Herculano AM, Morato S, Gouveia AJr. 2010b. Measuring anxiety in zebrafish: a critical review. Behav Brain Res 214: 157-171.
52. McHenry MJ, Feitl KE, Strother JA, Van Trump WJ. 2009. Larval zebrafish rapidly sense the water flow of a predator's strike. Biol Lett 5: 477-479.
53. McLean DL, Fetcho JR. 2004. Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish. J Comp Neurol 480: 38-56.
54. Meyer-Lindenberg A, Hariri AR, Munoz KE, Mervis CB, Mattay VS, Morris CA, Berman KF. 2005. Neural correlates of genetically abnormal social cognition in Williams syndrome. Nat Neurosci 8: 991-993.
55. Mobbs D, Marchant JL, Hassabis D, Seymour B, Tan G, Gray M, Petrovic P, et al. 2009. From threat to fear: The neural organization of defensive fear systems in humans. J Neurosci 29: 12236-12243.
56. Mobbs D, Petrovic P, Marchant JL, Hassabis D, Weiskopf N, Seymour B, Dolan RJ, et al. 2007. When fear is near: Threat imminence elicits prefrontal-periaqueductal gray shifts in humans. Science 317: 1079-1083.
57. Mongeau R, Miller GA, Chiang E, Anderson DJ. 2003. Neural correlates of competing fear behaviors evoked by an innately aversive stimulus. J Neurosci 23: 3855-3868.
58. Northcutt RG. 2006. Connections of the lateral and medial divisions of the goldfish telencephalic pallium. J Comp Neurol 494: 903-943.
59. Overmier JB, Seligman ME. 1967. Effects of inescapable shock upon subsequent escape and avoidance responding. J Comp Physiol Psychol 63: 28-33.
60. Portavella M, Torres B, Salas C. 2004a. Avoidance response in goldfish: Emotional and temporal involvement of medial and lateral telencephalic pallium. J Neurosci 24: 2335-2342.
61. Portavella M, Torres B, Salas C, Papini MR. 2004b. Lesions of the medial pallium, but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish (Carassius auratus). Neurosci Lett 362: 75-78.
62. Puelles L, Kuwana E, Puelles E, Bulfone A, Shimamura K, Keleher J, Smiga S, et al. 2000. Pallial and subpallial derivatives in the embryonic chick and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1, Nkx-21, Pax-6, and Tbr-1. J Comp Neurol 424: 409-438.
63. Sackerman J, Donegan JJ, Cunningham CS, Nguyen NN, Lawless K, Long A, Benno RH, et al. 2010. Zebrafish behavior in novel environments: Effects of acute exposure to anxiolytic compounds and choice of Danio rerio line, Int J Comp Psychol 23:43-61.
64. Sahuque L, Kullberg E, McGeehan A, Kinder J, Hicks M, Blanton M, Janak P, et al. 2006. Anxiogenic and aversive effects of corticotropin-releasing factor (CRF) in the bed nucleus of the stria terminalis in the rat: Role of CRF receptor subtypes. Psychopharmacology 186: 122-132.
65. Scheer N, Campos-Ortega JA. 1999. Use of the Gal4-UAS technique for targeted gene expression in the zebrafish. Mech Dev 80: 153-158.
66. Seligman ME, Maier SF. 1967. Failure to escape traumatic shock. J Exp Psychol 74: 1-9.
67. Speedie N, Gerlai R. 2008. Alarm substance induced behavioral responses in zebrafish (Danio rerio). Behav Brain Res 188: 168-177.
68. Sutherland RJ. 1982. The dorsal diencephalic conduction system: A review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 6: 1-13.
69. Thornton EW, Bradbury GE. 1989. Effort and stress influence the effect of lesion of the habenula complex in one-way active avoidance learning. Physiol Behav 45: 929-935.
70. Walker DL, Davis M. 1997a. Anxiogenic effects of high illumination levels assessed with the acoustic startle response in rats. Biol Psychiatry 42: 461-471.
71. Walker DL, Davis M. 1997b. Double dissociation between the involvement of the bed nucleus of the stria terminalis and the central nucleus of the amygdala in startle increases produced by conditioned versus unconditioned fear. J Neurosci 17: 9375-9383.
72. Weiss JM. 1968. Effects of coping responses on stress. J Comp Physiol Psychol 65: 251-260.
73. Whalen PJ, Shin LM, McInerney SC, Fischer H, Wright CI, Rauch SL. 2001. A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion 1: 70-83.
74. Wilcox KS, Christoph GR, Double BA, Leonzio RJ. 1986. Kainate and electrolytic lesions of the lateral habenula: Effect on avoidance responses. Physiol Behav 36: 413-417.
75. Wullimann MF, Mueller T. 2004a. Identification and morphogenesis of the eminentia thalami in the zebrafish. J Comp Neurol 471: 37-48.
76. Wullimann MF, Mueller T. 2004b. Teleostean and mammalian forebrains contrasted: Evidence from genes to behavior. J Comp Neurol 475: 143-162.
77. Wullimann MF, Rink E. 2002. The teleostean forebrain: a comparative and developmental view based on early proliferation. Pax6 activity and catecholaminergic organization. Brain Res Bull 57: 363-370.
78. Yamamoto N, Ishikawa Y, Yoshimoto M, Xue HG, Bahaxar N, Sawai N, Yang CY, et al. 2007. A new interpretation on the homology of the teleostean telencephalon based on hodology and a new eversion model. Brain Behav Evol 69: 96-104.