Zebrafish forebrain and temporal conditioning

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1637, 2014, Pages

  Cheng, Ruey Kuang ^a   Jesuthasan, Suresh J ^a,b,c   Penney, Trevor B ^c  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b DUKE NUS MEDICAL SCHOOL   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Anticipatory response; Corticostriatal circuits; Habenula; Interval timing; Two photon microscopy

Indexed keywords

ACADEMIC RESEARCH; BEHAVIORAL ECOLOGY; BRAIN; CALCIUM; CHEMICAL ANALYSIS; FISH; FRESHWATER ECOSYSTEM; HOMOLOGY; MAMMAL; NEUROLOGY; PERCEPTION;

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

ANIMAL; ANIMAL BEHAVIOR; ANIMAL MODEL; ANTICIPATORY RESPONSE; BASAL GANGLION; BIOLOGICAL MODEL; CORTICOSTRIATAL CIRCUITS; FOREBRAIN; HABENULA; HISTOLOGY; INTERVAL TIMING; LARVA; MAMMAL; METABOLISM; PHYSIOLOGY; REVIEW; SPECIES DIFFERENCE; TIME; TIME PERCEPTION; TWO-PHOTON MICROSCOPY; ZEBRA FISH;

ANTICIPATORY RESPONSE; CORTICOSTRIATAL CIRCUITS; HABENULA; INTERVAL TIMING; TWO-PHOTON MICROSCOPY;

ANIMALS; BASAL GANGLIA; BEHAVIOR, ANIMAL; HABENULA; LARVA; MAMMALS; MODELS, ANIMAL; MODELS, NEUROLOGICAL; NEUROTRANSMITTER AGENTS; PROSENCEPHALON; SPECIES SPECIFICITY; TIME FACTORS; TIME PERCEPTION; ZEBRAFISH;

EID: 84892545880     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0462     Document Type: Review

References (79)

1. Ahrens MB, Orger MB, Robson DN, Li JM, Keller BJ. 2013 Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 10, 413-420. (doi:10.1038/nmeth.2434)
2. Panier T, Romano SA, Olive R, Pietri T, Sumbre G, Candelier R, Debregeas G. 2013 Fast functional imaging of multiple brain regions in intact zebrafish larvae using Selective Plane Illumination Microscopy. Front. Neural Circuits 7, 65.
3. Coull JT, Cheng RK, Meck WH. 2011 Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology 36, 3-25. (doi:10.1038/npp.2010.113)
4. Vargas R, Thorsteinsson H, Karlsson KA. 2012 Spontaneous neural activity of the anterodorsal lobe and entopeduncular nucleus in adult zebrafish: a putative homologue of hippocampal sharp waves. Behav. Brain Res. 229, 10-20. (doi:10.1016/ j.bbr.2011.12.025)
5. Mueller T, Guo S. 2009 The distribution of GAD67-mRNA in the adult zebrafish (Teleost) forebrain reveals a prosomeric pattern and suggests previously unidentified homologies to tetrapods. J. Comp. Neurol. 516, 553-568. (doi:10.1002/cne.22122)
6. Maximino C, Lima MG, Oliveira KRM, Batista EDJO, Herculano AM. 2013 'Limbic associative' and 'autonomic' amygdala in teleosts: a review of the evidence. J. Chem. Neuroanat. 48-49, 1-13. (doi:10.1016/j.jchemneu.2012.10.001)
7. Scott E. 2009 The Gal4/UAS toolbox in zebrafish: new approaches for defining behavioral circuits. J. Neurochem. 110, 441-456. (doi:10.1111/ j.1471-4159.2009.06161.x)
8. Mueller T, Wullimann MF. 2009 An evolutionary interpretation of teleostean forebrain anatomy. Brain Behav. Evol. 74, 30-42. (doi:10.1159/ 000229011)
9. Aoki T et al. 2013 Imaging of neural ensemble for the retrieval of a learned behavioral program. Neuron 78, 1-14. (doi:10.1016/j.neuron.2013. 04.009)
10. Mueller T, Wullimann MF, Guo S. 2008 Early teleostean basal ganglia development visualized by zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (ecomesa), and GAD67 gene expression. J. Comp. Neurol. 507, 1245-1257. (doi:10.1002/cne.21604)
11. Hong S, Hikosaka O. 2008 The globus pallidus sends reward-related signals to the lateral habenula. Neuron 60, 720-729. (doi:10.1016/j.neuron.2008. 09.035)
12. Meck WH. 2006 Neuroanatomical localization of an internal clock: a functional link between mesolimbic, nigrostriatal, and mesocortical dopaminergic systems. Brain Res. 1109, 93-107. (doi:10.1016/j.brainres.2006.06.031)
13. Jin DZ, Fujii N, Graybiel AM. 2009 Neural representation of time in cortico-basal ganglia circuits. Proc. Natl Acad. Sci. USA 106, 19 156-19 161. (doi:10.1073/pnas.0909881106)
14. Coull JT, Vidal F, Nazarian B, Macar F. 2004 Functional anatomy of the attentional modulation of time estimation. Science 503, 1506-1508. (doi:10.1126/science.1091573)
15. Matell MS, Meck WH. 2000 Neuropsychological mechanisms of interval timing behavior. Bioassays 22, 94-103. (doi:10.1002/(SICI)1521-1878(200001) 22:1,94::AID-BIES14.3.0.CO;2-E)
16. Matell MS, Meck WH, Nicolelis MAL. 2003 Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons. Behav. Neurosci. 117, 760-773. (doi:10.1037/0735-7044. 117.4.760)
17. Meck WH, Penney TB, Pouthas V. 2008 Corticostriatal representation of time in animals and humans. Curr. Opinion Neurobiol. 18, 145-152. (doi:10.1016/j.conb.2008.08.002)
18. Wilson CJ. 1995 The contribution of cortical neurons to the firing pattern of striatal spiny neurons. In Models of information processing in the basal ganglia (eds JC Houk, JL Davis, DG Beiser), pp. 29-50. Cambridge, MA: MIT Press.
19. Portavella M, Torres B, Salas C. 2004 Avoidance response in Goldfish: emotional and temporal involvement of medial and lateral telencephalic pallium. J. Neurosci. 24, 2335-2342. (doi:10.1523/ JNEUROSCI.4930-03.2004)
20. Olton DS, Meck WH, Church RM. 1987 Separation of hippocampal and amygdaloid involvement in temporal memory dysfunctions. Brain Res. 404, 180-188. (doi:10.1016/0006-8993(87)91369-2)
21. Balci F, Meck WH, Moore H, Brunner D. 2009 Timing deficits in aging and neuropathology. In Animal models of human cognitive aging (eds JL Bizon, A Wood), pp. 161-201. Totowa, NJ: Humana Press.
22. Lewis PA, Couch TJ, Walker MP. 2011 Keeping time in your sleep: overnight consolidation of temporal rhythm. Neuropsychologia 49, 115-123. (doi:10. 1016/j.neuropsychologia.2010.10.025)
23. MacDoland CJ, Lepage KQ, Eden UT, Eichenbaum H. 2011 Hippocampal 'time cells' bridge the gap in memory for discontinuous events. Neuron 71, 737-749. (doi:10.1016/j.neuron.2011.07.012)
24. MacDonald CJ, Carrow S, Place R, Eichenbaum H. 2013 Distinct hippocampal time cell sequences represent odor memories in immobilized rats. J. Neurosci. 33, 14 607-14 616. (doi:10.1523/ JNEUROSCI.1537-13.2013)
25. Phelps EA, LeDoux JE. 2005 Contribution of the amygdala to emotion processing: from animal models to human behavior. Neuron 48, 175-187. (doi:10.1016/j.neuron.2005.09.025)
26. Bermudez MA, Gobel C, Schultz W. 2012 Sensitivity to temporal reward structure in amygdala neurons. Curr. Biol. 22, 1839-1844. (doi:10.1016/j.cub.2012. 07.062)
27. Meck WH, MacDonald CJ. 2007 Amygdala inactivation reverses fear's ability to impair divided attention and make time stand still. Behav. Neurosci. 121, 707-720. (doi:10.1037/0735-7044.121.4.707)
28. Mella N, Conty L, Pouthas V. 2011 The role of physiological arousal in time perception: psychophysiological evidence from an emotion regulation paradigm. Brain Cogn. 75, 18-28. (doi:10.1016/j.bandc.2010.10.005)
29. Stephenson-Jones M, Floros O, Robertson B, Grillner S. 2011 Evolutionary conservation of the habenula nuclei and their circuitry controlling the dopamine and 5-hydroxytryptophan (5-HT) systems. Proc. Natl Acad. Sci. USA 109, E164-E173.
30. Hendricks M, Jesuthasan S. 2007 Asymmetric innervation of the habenula in zebrafish. J. Comp. Neurol. 502, 611-619. (doi:10.1002/cne.21339)
31. Aizawa H, Amo R, Okamoto H. 2011 Phylogeny and ontogeny of the habenula structure. Front. Neurosci. 5, 138. (doi:10.3389/fnins.2011.00138)
32. Bianco IH, Wilson SW. 2009 The habenula nuclei: a conserved asymmetric relay station in the vertebrate brain. Phil. Trans. R. Soc. B 364, 1005-1020. (doi:10.1098/rstb.2008.0213)
33. Hong S, Jhou TC, Smith M, Saleem KS, Hikosaka O. 2011 Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates. J. Neurosci. 31, 11 457-11 471. (doi:10.1523/ JNEUROSCI.1384-11.2011)
34. Hikosaka O. 2010 The habenula: from stress evasion to value-based decision-making. Nat. Rev. Neurosci. 11, 503-513. (doi:10.1038/nrn2866)
35. Bromgerg-Martin ES, Matsumoto M, Hikosaka O. 2010 Distinct tonic and phasic anticipatory activity in lateral habenula and dopamine neurons. Neuron 67, 144-155. (doi:10.1016/j.neuron.2010.06.016)
36. Jesuthasan S. 2012 Fear, anxiety and control in the zebrafish. Dev. Neurobiol. 72, 395-403. (doi:10. 1002/dneu.20873)
37. Okamoto H, Agetsuma M, Aizawa H. 2012 Genetic dissection of the zebrafish habenula, a possible switching board for selection of behavioral strategy to cope with fear and anxiety. Dev. Neurobiol. 72, 386-394. (doi:10.1002/dneu.20913)
38. Yamaguchi T, Danjo T, Pastan I, Hikida T, Nakanishi S. 2013 Distinct roles of segregated transmission of the septo-habenula pathway in anxiety and fear. Neuron 78, 537-544. (doi:10.1016/j.neuron. 2013.02.035)
39. Meck WH. 1996 Neuropharmacology of timing and time perception. Cogn. Brain Res. 3, 227-242. (doi:10.1016/0926-6410(96)00009-2)
40. Cheng RK, MacDonald CJ, Meck WH. 2006 Differential effects of cocaine and ketamine on time estimation: implications for neurobiological models of interval timing. Pharmacol. Biochem. Behav. 85, 114-122. (doi:10.1016/j.pbb.2006.07.019)
41. Lake JI, Meck WH. 2013 Differential effects of amphetamine and haloperidol on temporal reproduction: dopaminergic regulation of attention and clock speed. Neuropsychogia 51, 284-292. (doi:10.1016/j.neuropsychologia.2012.09.014)
42. Kastenhuber E, Kratochwil CF, Ryu S, Schweitzer J, Driever W. 2010 Genetic dissection of dopaminergic and noradrenergic contributions to catecholaminergic tracts in early larval zebrafish. J. Comp. Neurol. 518, 439-458. (doi:10.1002/cne.22214)
43. Filippi A, Mahler J, Schweitzer J, Driever W. 2010 Expression of the paralogous tyrosine hydroxylase encoding genes th1 and th2 reveals the full complement of dopaminergic and noradrenergic neurons in zebrafish larval and juvenile brain. J. Comp. Neurol. 518, 423-438. (doi:10.1002/ cne.22213)
44. Yamamoto K, Ruuskanen JO, Wullimann MF, Vernier P. 2010 Two tyrosine hydroxylase genes in vertebrates: new dopaminergic territories revealed in the zebrafish brain. Mol. Cell Neurosci. 43, 394-402. (doi:10.1016/j.mcn.2010.01.006)
45. Mueller T, Vernier P, Wullimann MF. 2004 The adult central nervous cholinergic system of a neurogenetic model animal, the zebrafish Danio rerio. Brain Res. 1011, 156-169. (doi:10.1016/j.brainres.2004. 02.073)
46. Lillesaar C. 2011 The serotonergic system in fish. J. Chem. Neuroanat. 41, 294-308. (doi:10.1016/ j.jchemneu.2011.05.009)
47. Mahler J, Filippi A, Driever W. 2010 DeltaA/DeltaD regulate multiple and temporally distinct phases of notch signaling during dopaminergic neurogenesis in zebrafish. J. Neurosci. 30, 16 621-16 635. (doi:10.1523/JNEUROSCI.4769-10.2010)
48. Souza BR, Romano-Silva MA, Tropepe V. 2011 Dopamine D2 receptor activity modulates Akt signaling and alters GABAergic neuron development and motor behavior in zebrafish larvae. J. Neurosci. 31, 5512-5525. (doi:10.1523/JNEUROSCI.5548-10.2011)
49. Meck WH, Church RM. 1987 Cholinergic modulation of the content of temporal memory. Behav. Neurosci. 101, 457-464. (doi:10.1037/0735-7044.101.4.457)
50. Meck WH. 2006 Temporal memory in matured and aged rate is sensitive to choline acetyltransferase inhibition. Brain Res. 1108, 168-175. (doi:10.1016/ j.brainres.2006.06.047)
51. Jacobs SE, Fine A, Juliano SL. 1994 Cholinergic basal forebrain transplants restore diminished metabolic activity in the somatosensory cortex of rats with acetylcholine depletion. J. Neurosci. 14, 697-711.
52. Meck WH, Church RM, Wenk GL, Olton DS. 1987 Nucleus basalis magnocellularis and medial septal area lesions differentially impair temporal memory. J. Neurosci. 7, 3505-3511.
53. Hinton SC, Meck WH. 1996 Increasing the speed of an internal clock: the effects of nicotine on interval timing. Drug Dev. Res. 38, 204-211. (doi:10.1002/ (SICI)1098-2299(199607/08)38:3/4,204::AIDDDR9.3.0. CO;2-Q)
54. Eddins D, Petro A, Williams P, Cerutti DT, Levin ED. 2009 Nicotine effects on learning in zebrafish: the role of dopaminergic systems. Psychopharmacology 202, 103-109. (doi:10.1007/s00213-008-1287-4)
55. Gorlich A, Antolin-Fontes B, Ables JL, Frahm S, Slimak MA, Dougherty JD, Tallon I-I. 2013 Reexposure to nicotine during withdrawal increases the pacemaking activity of cholinergic habenula neurons. Proc. Natl Acad. Sci. USA 110, 17 077-17 082. (doi:10.1073/pnas.1313103110)
56. McLean DL, Fetcho JR. 2004 Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish. J. Comp. Neurol. 480, 38-56. (doi:10. 1002/cne.20280)
57. Rammsayer TH, Hennig J, Haag A, Lange N. 2001 Effects of noradrenergic activity on temporal processing in humans. Q. J. Exp. Psychol. B. 54, 247-258. (doi:10.1080/02724990143000036)
58. Penney TB, Holder MD, Meck WH. 1996 Clonidineinduced antagonism of norepinephrine modulates the attentional processes involved in peak-interval timing. Exp. Clin. Psychopharm. 4, 82-92. (doi:10. 1037/1064-1297.4.1.82)
59. Yokogawa T, Hannan MC, Burgess HA. 2012 The dorsal raphe modulates sensory responsiveness during arousal in zebrafish. J. Neurosci. 32, 15 205-15 215. (doi:10.1523/JNEUROSCI.1019-12.2012)
60. Fero K, Yokogawa T, Burgess HA. 2011 The behavioral repertoire of larval zebrafish. In Zebrafish models in neurobehavioural research (eds AV Kalueff, JM Cachat), ch. 12, pp. 249-291. Berlin, Germany: Springer.
61. Drew MR, Zupan B, Cooke A, Couvillon PA, Balsam PD. 2005 Temporal control of conditioned responding in Goldfish. J. Exp. Psych. Anim. Behav. Proc. 31, 31-39. (doi:10.1037/0097-7403.31.1.31)
62. Agetsuma M et al. 2010 The habenula is crucial for experience-dependent modification of fear responses in zebrafish. Nat. Neurosci. 13, 1354-1356. (doi:10.1038/nn.2654)
63. 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. (doi:10.1016/j.cub.2010.11.025)
64. Nordgreen J, Janczak AM, Hovland AL, Ranheim B, Horsberg TE. 2010 Trace classical conditioning in rainbow trout (Oncorhynchus mykiss): what do they learn? Anim. Cogn. 13, 303-309. (doi:10.1007/ s10071-009-0267-3)
65. Cerutti D, Jozefowiez D, Staddon JER. 2013 Rapid, accurate time estimation in zebrafish (Danio rerio). Behav. Process. 99, 21-25. (doi:10.1016/j.beproc. 2013.06.007)
66. Valente A, Huang K-H, Portugues R, Engert F. 2012 Ontogeny of classical and operant learning behaviors in zebrafish. Learn. Mem. 19, 170-177. (doi:10.1101/lm.025668.112)
67. Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF, Engert F, Portugues R. 2012 Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485, 471-477. (doi:10.1038/nature11057)
68. Engert F. 2013 Fish in the matrix: motor learning in a virtual world. Front. Neural Circuits 6, 125. (doi:10.3389/fncir.2012.00125)
69. Aizenberg M, Schuman EM. 2011 Cerebellardependent learning in larval zebrafish. J. Neurosci. 31, 8708-8712. (doi:10.1523/JNEUROSCI.6565-10. 2011)
70. Sumbre G, Muto A, Baier H, Poo MM. 2008 Entrained rhythmic activities of neuronal ensembles as perceptual memory of time interval. Nature 456, 102-106. (doi:10.1038/nature07351)
71. Niell CM, Smith SJ. 2005 Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron 45, 941-951. (doi:10. 1016/j.neuron.2005.01.047)
72. Schwartz G, Harris R, Shrom D, Berry 2nd MJ. 2007 Detection and prediction of periodic patterns by the retina. Nat. Neurosci. 10, 552-554. (doi:10.1038/ nn1887)
73. Scott E, Baier H. 2009 The cellular architecture of the larval zebrafish tectum, as revealed by Gal4 enhancer trap lines. Front. Neural Circuits 3, 13.
74. Muto A, Ohkura M, Abe G, Nakai J, Kawakami K. 2013 Real-time visualization of neuronal activity during perception. Curr. Biol. 23, 307-311. (doi:10.1016/j.cub.2012.12.040)
75. Buhusi CV, Meck WH. 2005 What makes us tick? Functional and neural mechanisms of interval timing. Nat. Rev. Neurosci. 6, 755-765. (doi:10.1038/nrn1764)
76. Merchant H, Harrington DL, Meck WH. 2013 Neural basis of the perception and estimation of time. Annu. Rev. Neurosci. 36, 313-336. (doi:10.1146/ annurev-neuro-062012-170349)
77. Chen T-W et al. 2013 Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300. (doi:10.1038/ nature12354)
78. Dreosi E, Odermatt B, Morostkar MM, Ladnado L. 2009 A genetically encoded reporter of synaptic activity in vivo. Nat. Methods 6, 883-889. (doi:10.1038/nmeth.1399)
79. Leung LC, Wang GX, Mourrain P. 2013 Imaging zebrafish neural activity from whole brain to synapse. Front. Neural Circuits 7, 76. (doi:10.33389/ fncir.2013.00076)