Disruption of epithalamic left-right asymmetry increases anxiety in Zebrafish

Journal of Neuroscience

Volumn 35, Issue 48, 2015, Pages 15847-15859

  Facchin, Lucilla ^a   Duboué, Erik R ^a   Halpern, Marnie E ^a  

^a GEOPHYSICAL LABORATORY   (United States)

Author keywords

Buspirone; Cortisol; Habenula; Interpeduncular nucleus; Stress

Indexed keywords

BUSPIRONE; HYDROCORTISONE; ANXIOLYTIC AGENT; FORKHEAD TRANSCRIPTION FACTOR; FOXD3 PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BRAIN ASYMMETRY; CONFINED BOX TEST; CONTROLLED STUDY; EMBRYO; EPITHALAMUS; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; HABENULA; IMMUNOFLUORESCENCE; MALE; MIRROR TEST; NONHUMAN; NOVEL TANK DIVING TEST; PRIORITY JOURNAL; SCORING SYSTEM; SWIMMING; ZEBRA FISH; ADAPTATION; ANIMAL; ASSOCIATION; DISEASE MODEL; DRUG EFFECTS; DRUG THERAPY; EXPLORATORY BEHAVIOR; GENETICS; HEMISPHERIC DOMINANCE; IMITATION; LARVA; LOCOMOTION; METABOLISM; PATHOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; PINEAL BODY; SURGERY; TRANSGENIC ANIMAL;

ADAPTATION, BIOLOGICAL; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTI-ANXIETY AGENTS; ANXIETY; BUSPIRONE; CUES; DISEASE MODELS, ANIMAL; EPITHALAMUS; EXPLORATORY BEHAVIOR; FORKHEAD TRANSCRIPTION FACTORS; FUNCTIONAL LATERALITY; HYDROCORTISONE; IMITATIVE BEHAVIOR; LARVA; LOCOMOTION; PHOTIC STIMULATION; PINEAL GLAND; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84949471599     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2593-15.2015     Document Type: Article

References (61)

1. Agetsuma M, Aizawa H, Aoki T, Nakayama R, Takahoko M, Goto M, Sassa T, Amo R, Shiraki T, Kawakami K, Hosoya T, Higashijima S, Okamoto H (2010) The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat Neurosci 13:1354-1356. CrossRef Medline
2. Aizawa H, Bianco IH, Hamaoka T, Miyashita T, Uemura O, Concha ML, Russell C, Wilson SW, Okamoto H (2005) Laterotopic representation of left-right information onto the dorso-ventral axis of a zebrafish midbrain target nucleus. Curr Biol 15:238-243. CrossRef Medline
3. Aizawa H, Goto M, Sato T, Okamoto H (2007) Temporally regulated asymmetric neurogenesis causes left-right difference in the zebrafish habenular structures. Dev Cell 12:87-98. CrossRef Medline
4. Bandler R, Keay KA, Floyd N, Price J (2000) Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain Res Bull 53:95-104. CrossRef Medline
5. Barcellos L, Ritter F, Kreutz L, Quevedo R, Bolognesi da Silva L, Bedin A, Finco J, Cericato L (2007) Whole-body cortisol increases after direct and visual contact with a predator in zebrafish, Danio rerio. Aquaculture 272:774. CrossRef
6. Barry TP, Malison JA, Held JA, Parrish JJ (1995) Ontogeny of the cortisol stress response in larval rainbow trout. Gen Comp Endocrinol 97:57-65. CrossRef Medline
7. Barth KA, Miklosi A, Watkins J, Bianco IH, Wilson SW, Andrew RJ (2005) fsi zebrafish show concordant reversal of laterality of viscera, neuroanatomy, and a subset of behavioral responses. Curr Biol 15:844-850. CrossRef Medline
8. Bencan Z, Sledge D, Levin ED (2009) Buspirone, chlordiazepoxide and diazepam effects in a zebrafish model of anxiety. Pharmacol Biochem Behav 94:75-80. CrossRef Medline
9. Blaser RE, Chadwick L, McGinnis GC (2010) Behavioral measures of anxiety in zebrafish (Danio rerio). Behav Brain Res 208:56-62. CrossRef Medline
10. Cachat J, Stewart A, Grossman L, Gaikwad S, Kadri F, Chung KM, Wu N, Wong K, Roy S, Suciu C, Goodspeed J, Elegante M, Bartels B, Elkhayat S, Tien D, Tan J, Denmark A, Gilder T, Kyzar E, Dileo J, et al. (2010) Measuring behavioral and endocrine responses to novelty stress in adult zebrafish. Nat Protoc 5:1786-1799. CrossRef Medline
11. Cachat J, Canavello P, Elegante M, Bartels B, Elkhayat S, Hart P, Tien A, Tien D, Beeson E, Mohnot S, Laffoon A, Stewart A, Gaikwad S, Wong K, Haymore W, Kalueff A (2011) Modeling stress and anxiety in zebrafish. In: Zebrafish models in neurobehavioral research (Kalueff AV, Cachat JM, eds), pp 73-88. New York: Humana.
12. Cochella L, Tursun B, Hsieh YW, Galindo S, Johnston RJ, Chuang CF, Hobert O (2014) Two distinct types of neuronal asymmetries are controlled by the Caenorhabditis elegans zinc finger transcription factor die-1. Genes Dev 28:34-43. CrossRef Medline
13. Concha ML, Wilson SW (2001) Asymmetry in the epithalamus of verte-brates. J Anat 199:63-84. CrossRef Medline
14. Concha ML, Burdine RD, Russell C, Schier AF, Wilson SW (2000) A nodal signaling pathway regulates the laterality of neuroanatomical asymmetries in the zebrafish forebrain. Neuron 28:399-409. CrossRef Medline
15. Concha ML, Russell C, Regan JC, Tawk M, Sidi S, Gilmour DT, Kapsimali M, Sumoy L, Goldstone K, Amaya E, Kimelman D, Nicolson T, Grunder S, Gomperts M, Clarke JD, Wilson SW (2003) Local tissue interactions across the dorsal midline of the forebrain establish CNS laterality. Neuron 39:423-438. CrossRef Medline
16. Dadda M, Domenichini A, Piffer L, Argenton F, Bisazza A (2010) Early differences in epithalamic left-right asymmetry influence lateralization and personality of adult zebrafish. Behav Brain Res 206:208-215. CrossRef Medline
17. Davidson RJ (1984) Affect, cognition, and hemispheric specialization. In: Emotions, cognition, and behavior (Izard CE, Kagan J, Zajonc RB, eds), pp 46. New York: Cambridge UP.
18. Deng C, Rogers LJ (1997) Differential contributions of the two visual pathways to functional lateralization in chicks. Behav Brain Res 87:173-182. CrossRef Medline
19. Desjardins JK, Fernald RD (2010) What do fish make of mirror images? Biol Lett 6:744-747. CrossRef Medline
20. Dreosti E, Vendrell Llopis N, Carl M, Yaksi E, Wilson SW (2014) Left-right asymmetry is required for the habenulae to respond to both visual and olfactory stimuli. Curr Biol 24:440-445. CrossRef Medline
21. Egan RJ, Bergner CL, Hart PC, Cachat JM, Canavello PR, Elegante MF, Elkhayat SI, Bartels BK, Tien AK, Tien DH, Mohnot S, Beeson E, Glasgow E, Amri H, Zukowska Z, Kalueff AV (2009) Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish. Behav Brain Res 205:38-44. CrossRef Medline
22. Facchin L, Argenton F, Bisazza A (2009a) Lines of Danio rerio selected for opposite behavioural lateralization show differences in anatomical left-right asymmetries. Behav Brain Res 197:157-165. CrossRef Medline
23. Facchin L, Burgess HA, Siddiqi M, Granato M, Halpern ME (2009b) Determining the function of zebrafish epithalamic asymmetry. Philos Trans R Soc Lond B Biol Sci 364:1021-1032. CrossRef Medline
24. Gamse JT, Thisse C, Thisse B, Halpern ME (2003) The parapineal mediates left-right asymmetry in the zebrafish diencephalon. Development 130: 1059-1068. CrossRef Medline
25. Gamse JT, Kuan YS, Macurak M, Brösamle C, Thisse B, Thisse C, Halpern ME (2005) Directional asymmetry of the zebrafish epithalamus guides dorsoventral innervation of the midbrain target. Development 132:4869-4881. CrossRef Medline
26. Gilmour DT, Maischein HM, Nusslein-Volhard C (2002) Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron 34:577-588. CrossRef Medline
27. Gorelick DA, Watson W, Halpern ME (2008) Androgen receptor gene ex- pression in the developing and adult zebrafish brain. Dev Dyn 237: 2987-2995. CrossRef Medline
28. Goto K, Kurashima R, Gokan H, Inoue N, Ito I, Watanabe S (2010) Left-right asymmetry defect in the hippocampal circuitry impairs spatial learning and working memory in iv mice. PLoS One 5:e15468. CrossRef Medline
29. Gunturkun O, Hellmann B, Melsbach G, Prior H (1998) Asymmetries of representation in the visual system of pigeons. Neuroreport 9:4127-4130. CrossRef Medline
30. Gutiérrez-Ibáñez C, Reddon AR, Kreuzer MB, Wylie DR, Hurd PL (2011) Variation in asymmetry of the habenular nucleus correlates with behavioural asymmetry in a cichlid fish. Behav Brain Res 221:189-196. CrossRef Medline
31. Jetti SK, Vendrell-Llopis N, Yaksi E (2014) Spontaneous activity governs olfactory representations in spatially organized habenular microcircuits. Curr Biol 24:434-439. CrossRef Medline
32. Kawakami R, Dobi A, Shigemoto R, Ito I (2008) Right isomerism of the brain in inversus viscerum mutant mice. PLoS One 3:e1945. CrossRef Medline
33. Kuan YS, Gamse JT, Schreiber AM, Halpern ME (2007a) Selective asymmetry in a conserved forebrain to midbrain projection. J Exp Zool B Mol Dev Evol 308:669-678. CrossRef Medline
34. Kuan YS, Yu HH, Moens CB, Halpern ME (2007b) Neuropilin asymmetry mediates a left-right difference in habenular connectivity. Development 134:857-865. CrossRef Medline
35. Lau BY, Mathur P, Gould GG, Guo S (2011) Identification of a brain center whose activity discriminates a choice behavior in zebrafish. Proc Natl Acad Sci U S A 108:2581-2586. CrossRef Medline
36. 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. CrossRef Medline
37. Lesch BJ, Gehrke AR, Bulyk ML, Bargmann CI (2009) Transcriptional regulation and stabilization of left-right neuronal identity in C. elegans. Genes Dev 23:345-358. CrossRef Medline
38. Levin ED, Bencan Z, Cerutti DT (2007) Anxiolytic effects of nicotine in zebrafish. Physiol Behav 90:54-58. CrossRef Medline
39. Liang JO, Etheridge A, Hantsoo L, Rubinstein AL, Nowak SJ, Izpisúa Bel-monte JC, Halpern ME (2000) Asymmetric nodal signaling in the zebrafish diencephalon positions the pineal organ. Development 127: 5101-5112. Medline
40. Long S, Ahmad N, Rebagliati M (2003) The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 130:2303-2316. CrossRef Medline
41. Magno LD, Fontes A, Gonçalves BM, Gouveia A Jr (2015) Pharmacological study of the light/dark preference test in zebrafish (Danio rerio): Water-borne administration. Pharmacol Biochem Behav 135:169-176. CrossRef Medline
42. Manns M, Römling J (2012) The impact of asymmetrical light input on cerebral hemispheric specialization and interhemispheric cooperation. Nat Commun 3:696. CrossRef Medline
43. Maximino C, de Brito TM, da Silva Batista AW, Herculano AM, Morato S, Gouveia A Jr (2010) Measuring anxiety in zebrafish: a critical review. Behav Brain Res 214:157-171. CrossRef Medline
44. Okamoto H, Agetsuma M, Aizawa H (2012) Genetic dissection of the ze-brafish habenula, a possible switching board for selection of behavioral strategy to cope with fear and anxiety. Dev Neurobiol 72:386-394. CrossRef Medline
45. Orman R, Stewart M (2007) Hemispheric differences in protein kinase C betaII levels in the rat amygdala: baseline asymmetry and lateralized changes associated with cue and context in a classical fear conditioning paradigm. Neuroscience 144:797-807. CrossRef Medline
46. Poole RJ, Hobert O (2006) Early embryonic programming of neuronal left/ right asymmetry in C. elegans. Curr Biol 16:2279-2292. CrossRef Medline
47. Rogers LJ (2008) Development and function of lateralization in the avian brain. Brain Res Bull 76:235-244. CrossRef Medline
48. Rosemberg DB, Rico EP, Mussulini BH, Piato AL, Calcagnotto ME, Bonan CD, Dias RD, Blaser RE, Souza DO, de Oliveira DL (2011) Differences in spatio-temporal behavior of zebrafish in the open tank paradigm after a short-period confinement into dark and bright environments. PLoS One 6:e19397. CrossRef Medline
49. Sackerman J, Donegan JJ, Cunningham CS, Nguyen NN, Lawless K, Long A, Benno RH, Gould GG (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. Medline
50. Selye H (1976) Stress in health and disease. Boston: Butterworths. Serra EL, Medalha CC, Mattioli R (1999) Natural preference of zebrafish (Danio rerio) for a dark environment. Braz J Med Biol Res 32:1551-1553. Medline
51. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379-423. CrossRef
52. Signore IA, Guerrero N, Loosli F, Colombo A, Villalón A, Wittbrodt J, Con- cha ML (2009) Zebrafish and medaka: model organisms for a comparative developmental approach of brain asymmetry. Philos Trans R Soc Lond B Biol Sci 364:991-1003. CrossRef Medline
53. Sovrano VA, Andrew RJ (2006) Eye use during viewing a reflection: behavioural lateralisation in zebrafish larvae. Behav Brain Res 167:226-231. CrossRef Medline
54. Sovrano VA, Rainoldi C, Bisazza A, Vallortigara G (1999) Roots of brain specializations: preferential left-eye use during mirror-image inspection in six species of teleost fish. Behav Brain Res 106:175-180. CrossRef Medline
55. Suzuki H, Thiele TR, Faumont S, Ezcurra M, Lockery SR, Schafer WR (2008) Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 454:114-117. CrossRef Medline
56. Valencia-Alfonso CE, Verhaal J, Gunturkun O (2009) Ascending and de-scending mechanisms of visual lateralization in pigeons. Philos Trans R Soc Lond B Biol Sci 364:955-963. CrossRef Medline
57. Walker C (1999) Haploid screens and gamma-ray mutagenesis. Methods Cell Biol 60:43-70. Medline
58. Wu Y, Kawakami R, Shinohara Y, Fukaya M, Sakimura K, Mishina M, Wa- tanabe M, Ito I, Shigemoto R (2005) Target-cell-specific left-right asymmetry of NMDA receptor content in schaffer collateral synapses in epsilon1/NR2A knock-out mice. J Neurosci 25:9213-9226. CrossRef Medline
59. Yáñez J, Meissl H, Anadón R (1996) Central projections of the parapineal organ of the adult rainbow trout (Oncorhynchus mykiss). Cell Tissue Res 285:69-74. CrossRef Medline
60. Young EJ, Williams CL (2010) Valence dependent asymmetric release of norepinephrine in the basolateral amygdala. Behav Neurosci 124:633-644. CrossRef Medline
61. Young EJ, Williams CL (2013) Differential activation of amygdala Arc expression by positive and negatively valenced emotional learning conditions. Front Behav Neurosci 7:191. CrossRef Medline