Big ideas for small brains: What can psychiatry learn from worms, flies, bees and fish

Molecular Psychiatry

Volumn 16, Issue 1, 2011, Pages 7-16

  Burne, T ^a,b   Scott, E ^a   Van Swinderen, B ^a   Hilliard, M ^a   Reinhard, J ^a   Claudianos, C ^a   Eyles, D ^a,b   McGrath, J ^a,b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QUEENSLAND CENTRE FOR MENTAL HEALTH RESEARCH   (Australia)

Author keywords

animal model; Apis; C. elegans; Danio; Drosophila; psychiatry

Indexed keywords

BRAIN; BRAIN ELECTROPHYSIOLOGY; BRAIN SIZE; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; EXPERIMENTAL ANIMAL; HONEYBEE; NERVE CELL; NEUROPSYCHIATRY; NONHUMAN; PRIORITY JOURNAL; REVIEW; ZEBRA FISH;

ANIMALS; HIGH-THROUGHPUT SCREENING ASSAYS; MENTAL DISORDERS; MODELS, ANIMAL; NERVE TISSUE PROTEINS; NEUROPSYCHIATRY;

EID: 78650515241     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2010.35     Document Type: Review

References (106)

1. Tallman JF. Neuropsychopharmacology at the new millennium: new industry directions. Neuropsychopharmacology 1999; 20: 99-105.
2. Miczek KA, de Wit H. Challenges for translational psychophar-macology research-some basic principles. Psychopharmacology (Berl) 2008; 199: 291-301.
3. Marsden CA, Rex A. Transgenics and psychopharmacology- introduction. Rev Neurosci 2000; 11: 1-2.
4. Cryan JF, Holmes A. The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 2005; 4: 775-790.
5. German DC, Eisch AJ. Mouse models of Alzheimer's disease: insight into treatment. Rev Neurosci 2004; 15: 353-369.
6. Tecott LH. The genes and brains of mice and men. Am J Psychiatry 2003; 160: 646-656.
7. Arguello PA, Gogos JA. Modeling madness in mice: one piece at a time. Neuron 2006; 52: 179-196.
8. Crawley JN. Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol 2007; 17: 448-459.
9. White JG, Southgate E, Thomson JN, Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 1986; 314: 1-340.
10. Chatterjee N, Sinha S. Understanding the mind of a worm: hierarchical network structure underlying nervous system function in C. elegans. Progress in Brain Research 2007; Vol 168: pp 145-153.
11. Kendler KS, Greenspan RJ. The nature of genetic influences on behavior: lessons from 'simpler' organisms. Am J Psychiatry 2006; 163: 1683-1694.
12. Sawamura N, Ando T, Maruyama Y, Fujimuro M, Mochizuki H, Honjo K et al. Nuclear DISC1 regulates CRE-mediated gene transcription and sleep homeostasis in the fruit fly. Mol Psychiatry 2008; 13: 1138-1148, 1069.
13. Sawamura N, Ishida N, Tomoda T, Hai T, Furukubo-Tokunaga K, Sawa A. The fruitfly Drosophila melanogaster: a promising model to explore molecular psychiatry. Mol Psychiatry 2008; 13: 1069.
14. Sulston JE, Schierenberg E, White JG, Thomson JN. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 1983; 100: 64-119.
15. Hall DH, Russell RL. The posterior nervous system of the nematode Caenorhabditis elegans: serial reconstruction of identified neurons and complete pattern of synaptic interactions. J Neurosci 1991; 11: 1-22.
16. Takahashi K, Yoshina S, Masashi M, Ito W, Inoue T, Shiwaku H et al. Nematode homologue of PQBP1, a mental retardation causative gene, is involved in lipid metabolism. PLoS ONE 2009; 4: e4104.
17. Grigorenko AP, Moliaka YK, Soto MC, Mello CC, Rogaev EI. The Caenorhabditis elegans IMPAS gene, imp-2, is essential for development and is functionally distinct from related preseni-lins. Proc Natl Acad Sci USA 2004; 101: 14955-14960.
18. Bloom L, Horvitz HR. The Caenorhabditis elegans gene unc-76 and its human homologs define a new gene family involved in axonal outgrowth and fasciculation. Proc Natl Acad Sci USA 1997; 94: 3414-3419.
19. Miyoshi K, Honda A, Baba K, Taniguchi M, Oono K, Fujita T et al. Disrupted-In-Schizophrenia 1, a candidate gene for schizophrenia, participates in neurite outgrowth. Mol Psychiatry 2003; 8: 685-694.
20. Bord L, Wheeler J, Paek M, Saleh M, Lyons-Warren A, Ross CA et al. Primate disrupted-in-schizophrenia-1 (DISC1): high divergence of a gene for major mental illnesses in recent evolutionary history. Neurosci Res 2006; 56: 286-293.
21. Jin Y, Jorgensen E, Hartwieg E, Horvitz HR. The Caenorhabditis elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J Neurosci 1999; 19: 539-548.
22. Nass R, Miller DM, Blakely RD. C. elegans: a novel pharmaco-genetic model to study Parkinson's disease. Parkinsonism Relat Disord 2001; 7: 185-191.
23. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 2000; 403: 560-564.
24. Rugarli EI, Di Schiavi E, Hilliard MA, Arbucci S, Ghezzi C, Facciolli A et al. The Kallmann syndrome gene homolog in C. elegans is involved in epidermal morphogenesis and neurite branching. Development 2002; 129: 1283-1294.
25. De Bono M, Maricq AV. Neuronal substrates of complex behaviors in C. elegans. Annu Rev Neurosci 2005; 28: 451-501.
26. Feng Z, Li W, Ward A, Piggott BJ, Larkspur ER, Sternberg PW et al. A C. elegans model of nicotine-dependent behavior: regulation by TRP-family channels. Cell 2006; 127: 621-633.
27. Davies AG, Pierce-Shimomura JT, Kim H, VanHoven MK, Thiele TR, Bonci A et al. A central role of the BK potassium channel in behavioral responses to ethanol in C. elegans. Cell 2003; 115: 655-666.
28. Giles AC, Rose JK, Rankin CH. Investigations of learning and memory in Caenorhabditis elegans. Int Rev Neurobiol 2006; 69: 37-71.
29. Donohoe DR, Phan T, Weeks K, Aamodt EJ, Dwyer DS. Antipsychotic drugs up-regulate tryptophan hydroxylase in ADF neurons of Caenorhabditis elegans: role of calcium-calmo-dulin-dependent protein kinase II and transient receptor potential vanilloid channel. J Neurosci Res 2008; 86: 2553-2563.
30. Raizen DM, Zimmerman JE, Maycock MH, Ta UD, You YJ, Sundaram MV et al. Lethargus is a Caenorhabditis elegans sleep-like state. Nature 2008; 451: 569-572.
31. Suo S, Ishiura S, Van Tol HH. Dopamine receptors in C. elegans. Eur J Pharmacol 2004; 500: 159-166.
32. Wolf FW, Heberlein U. Invertebrate models of drug abuse. J Neurobiol 2003; 54: 161-178.
33. Zubenko GS, Jones ML, Estevez AO, Hughes III HB, Estevez M. Identification of a CREB-dependent serotonergic pathway and neuronal circuit regulating foraging behavior in Caenorhabditis elegans: a useful model for mental disorders and their treatments? Am J Med Genet B Neuropsychiatr Genet 2009; 150B: 12-23.
34. Benzer S. Behavioral mutants of Drosophila isolated by countercurrent distribution. Proc Natl Acad Sci USA 1967; 58: 1112-1119.
35. Tully T, Quinn WG. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 1985; 157: 263-277.
36. Davis RL. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu Rev Neurosci 2005; 28: 275-302.
37. Hardin PE. The circadian timekeeping system of Drosophila. Curr Biol 2005; 15: R714-R722.
38. Greenspan RJ, Ferveur JF. Courtship in Drosophila. Annu Rev Genet 2000; 34: 205-232.
39. Vosshall LB. Into the mind of a fly. Nature 2007; 450: 193-197.
40. Van Swinderen B. Attention-like processes in Drosophila require short-term memory genes. Science 2007; 315: 1590-1593.
41. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G. Correlates of sleep and waking in Drosophila melanogaster. Science 2000; 287: 1834-1837.
42. Dudai Y, Jan YN, Byers D, Quinn WG, Benzer S. dunce, a mutant of Drosophila deficient in learning. Proc Natl Acad Sci USA 1976; 73: 1684-1688.
43. Davis RL, Cherry J, Dauwalder B, Han PL, Skoulakis E. The cyclic AMP system and Drosophila learning. Mol Cell Biochem 1995; 149-150: 271-278.
44. Davis RL, Dauwalder B. The Drosophila dunce locus: learning and memory genes in the fly. Trends Genet 1991; 7: 224-229.
45. Anderton BH. Alzheimer's disease: clues from flies and worms. Curr Biol 1999; 9: R106-R109.
46. Gotz J, Streffer JR, David D, Schild A, Hoerndli F, Pennanen L et al. Transgenic animal models of Alzheimer's disease and related disorders: histopathology, behavior and therapy. Mol Psychiatry 2004; 9: 664-683.
47. Simon AF, Liang DT, Krantz DE. Differential decline in behavioral performance of Drosophila melanogaster with age. Mech Ageing Dev 2006; 127: 647-651.
48. Apostol BL, Kazantsev A, Raffioni S, Illes K, Pallos J, Bodai L et al. A cell-based assay for aggregation inhibitors as therapeutics of polyglutamine-repeat disease and validation in Drosophila. Proc Natl Acad Sci USA 2003; 100: 5950-5955.
49. Cooper RL, Neckameyer WS. Dopaminergic modulation of motor neuron activity and neuromuscular function in Drosophila melanogaster. Comp Biochem Physiol B Biochem Mol Biol 1999; 122: 199-210.
50. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, Apostol BL et al. Histone deacetylase inhibitors arrest poly-glutamine-dependent neurodegeneration in Drosophila. Nature 2001; 413: 739-743.
51. Li J, Ashley J, Budnik V, Bhat MA. Crucial role of Drosophila neurexin in proper active zone apposition to postsynaptic densities, synaptic growth, and synaptic transmission. Neuron 2007; 55: 741-755.
52. Zeng X, Sun M, Liu L, Chen F, Wei L, Xie W. Neurexin-1 is required for synapse formation and larvae associative learning in Drosophila. FEBS Lett 2007; 581: 2509-2516.
53. Bolduc FV, Bell K, Cox H, Broadie KS, Tully T. Excess protein synthesis in Drosophila fragile X mutants impairs long-term memory. Nat Neurosci 2008; 11: 1143-1145.
54. De Luca V, Muglia P, Jain U, Basile VS, Sokolowski MB, Kennedy JL. A drosophila model for attention deficit hyperactiv-ity disorder (ADHD): no evidence of association with PRKG1 gene. Neuromolecular Med 2002; 2: 281-287.
55. Guarnieri DJ, Heberlein U. Drosophila melanogaster, a genetic model system for alcohol research. Int Rev Neurobiol 2003; 54: 199-228.
56. Scholz H. Intoxicated fly brains: neurons mediating ethanol-induced behaviors. J Neurogenet 2009; 23: 111-119.
57. Corl AB, Berger KH, Ophir-Shohat G, Gesch J, Simms JA, Bartlett SE et al. Happyhour, a Ste20 family kinase, implicates EGFR signaling in ethanol-induced behaviors. Cell 2009; 137: 949-960.
58. Dierick HA. A method for quantifying aggression in male Drosophila melanogaster. Nat Protoc 2007; 2: 2712-2718.
59. Hoyer SC, Eckart A, Herrel A, Zars T, Fischer SA, Hardie SL et al. Octopamine in male aggression of Drosophila. Curr Biol 2008; 18: 159-167.
60. Van Swinderen B, Greenspan RJ. Salience modulates 20-30 Hz brain activity in Drosophila. Nat Neurosci 2003; 6: 579-586.
61. Seugnet L, Suzuki Y, Stidd R, Shaw PJ. Aversive phototaxic suppression: evaluation of a short-term memory assay in Drosophila melanogaster. Genes Brain Behav 2009; 8: 377-389.
62. Sarkar S, Krishna G, Imarisio S, Saiki S, O'Kane CJ, Rubinsztein DC. A rational mechanism for combination treatment of Hun-tington's disease using lithium and rapamycin. Human Mol Genet 2008; 17: 170-178.
63. Dokucu ME, Yu L, Taghert PH. Lithium- and valproate-induced alterations in circadian locomotor behavior in Drosophila. Neuropsychopharmacology 2005; 30: 2216-2224.
64. Gilestro GF, Tononi G, Cirelli C. Widespread changes in synaptic markers as a function of sleep and wakefulness in Drosophila. Science 2009; 324: 109-112.
65. Van Swinderen B, Flores KA. Attention-like processes underlying optomotor performance in a Drosophila choice maze. J Neurobiol 2006; 67: 129-145.
66. Swinderen B. The remote roots of consciousness in fruit-fly selective attention? Bioessays 2005; 27: 321-330.
67. Menzel R, Giurfa M. Cognition by a mini brain. Nature 1999; 400: 718-719.
68. Gould JL, Gould CG. The Honeybee. Scientific American Library: New York, 1995.
69. von Frisch K. The Dance Language and Orientation of Bees. Harvard Univ. Press.: London, 1993.
70. Reinhard J, Srinivasan MV, Zhang SW. Scent-triggered navigation in honeybees. Nature 2004; 427: 411.
71. Giurfa M. Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comparative Physiol 2007; 193: 801-824.
72. Letzkus P, Ribi WA, Wood JT, Zhu H, Zhang SW, Srinivasan MV. Lateralization of olfaction in the honeybee Apis mellifera. Curr Biol 2006; 16: 1471-1476.
73. Rogers LJ, Vallortigara G. From antenna to antenna: lateral shift of olfactory memory recall by honeybees. PLoS One 2008; 3: e2340.
74. Rujescu D, Ingason A, Cichon S, Pietilainen OP, Barnes MR, Toulopoulou T et al. Disruption of the neurexin 1 gene is associated with schizophrenia. Human Mol Genet 2009; 18: 988-996.
75. Chubykin AA, Liu X, Comoletti D, Tsigelny I, Taylor P, Sudhof TC. Dissection of synapse induction by neuroligins: effect of a neuroligin mutation associated with autism. J Biol Chem 2005; 280: 22365-22374.
76. Biswas S, Russell RJ, Jackson CJ, Vidovic M, Ganeshina O, Oakeshott JG et al. Bridging the synaptic gap: neuroligins and neurexin I in Apis mellifera. PLoS ONE 2008; 3: e3542.
77. Weinstock GM, Robinson GE, Gibbs RA, Worley KC, Evans JD, Maleszka R. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 2006; 443: 931-949.
78. Baier H, Scott EK. Genetic and optical targeting of neural circuits and behavior-zebrafish in the spotlight. Curr Opin Neurobiol 2009; 19: 553-560.
79. Baier H. Zebrafish on the move: towards a behavior-genetic analysis of vertebrate vision. Curr Opin Neurobiol 2000; 10: 451-455.
80. McLean DL, Fetcho JR. Using imaging and genetics in zebrafish to study developing spinal circuits in vivo. Dev Neurobiol 2008; 68: 817-834.
81. Debruyne J, Hurd MW, Gutiérrez L, Kaneko M, Tan Y, Wells DE et al. Isolation and phenogenetics of a novel circadian rhythm mutant in zebrafish. J Neurogenet 2004; 18: 403-428.
82. Prober DA, Rihel J, Onah AA, Sung RJ, Schier AF. Hypocretin/ orexin overexpression induces an insomnia-like phenotype in zebrafish. J Neurosci 2006; 26: 13400-13410.
83. Bretaud S, Li Q, Lockwood BL, Kobayashi K, Lin E, Guo S. A choice behavior for morphine reveals experience-dependent drug preference and underlying neural substrates in developing larval zebrafish. Neuroscience 2007; 146: 1109-1116.
84. Darland T, Dowling JE. Behavioral screening for cocaine sensitivity in Mutagenized Zebrafish. Proc Natl Acad Sci USA 2001; 98: 11691-11696.
85. Gerlai R, Lahav M, Guo S, Rosenthal A. Drinks like a fish: Zebra fish (Danio rerio) as a behavior genetic model to study alcohol effects. Pharmacol Biochem Behavior 2000; 67: 773-782.
86. Kily LJM, Cowe YCM, Hussain O, Patel S, McElwaine S, Cotter FE et al. Gene expression changes in a zebrafish model of drug dependency suggest conservation of neuro-adaptation pathways. J Exp Biol 2008; 211: 1623-1634.
87. Ninkovic J, Ballycuif L. The zebrafish as a model system for assessing the reinforcing properties of drugs of abuse. Methods 2006; 39: 262-274.
88. Best JD, Berghmans S, Hunt JJFG, Clarke SC, Fleming A, Goldsmith P et al. Non-associative learning in larval zebrafish. Neuropsychopharmacology 2008; 33: 1206-1215.
89. Best JD, Alderton WK. Zebrafish: an in vivo model for the study of neurological diseases. Neuropsychiatric Disease and Treatment 2008; 4: 567-576.
90. Guo S. Linking genes to brain, behavior and neurological diseases: what can we learn from zebrafish? Genes, Brain and Behavior 2004; 3: 63-74.
91. Schweitzer J, Driever W. Development of the dopamine systems in zebrafish. Adv Exp Med Biol 2009; 651: 1-14.
92. Ekker SC, Larson JD. Morphant technology in model developmental systems. Genesis 2001; 30: 89-93.
93. Elliott DA, Brand AH. The GAL4 system: a versatile system for the expression of genes. Methods Mol Biol (Clifton, NJ) 2008; 420: 79-95.
94. Lichtman JW, Smith SJ. Seeing circuits assemble. Neuron 2008; 60: 441-448.
95. Arrenberg AB, Del Bene F, Baier H. Optical control of zebrafish behavior with halorhodopsin. Proc Natl Acad Sci USA 2009; 106: 17968-17973.
96. Borue X, Cooper S, Hirsh J, Condron B, Venton BJ. Quantitative evaluation of serotonin release and clearance in Drosophila. J Neurosci Methods 2009; 179: 300-308.
97. Wyart C, Del Bene F, Warp E, Scott EK, Trauner D, Baier H et al. Optogenetic dissection of a behavioural module in the vertebrate spinal cord. Nature 2009; 461: 407-410.
98. Olsen SR, Wilson RI. Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila. Trends Neurosci 2008; 31: 512-520.
99. Wu Y, Bolduc FV, Bell K, Tully T, Fang Y, Sehgal A et al. A Drosophila model for Angelman syndrome. Proc Natl Acad Sci USA 2008; 105: 12399-12404.
100. Schnabel J. Neuroscience: standard model. Nature 2008; 454: 682-685.
101. Van der Staay FJ. Animal models of behavioral dysfunctions: basic concepts and classifications, and an evaluation strategy. Brain Res Rev 2006; 52: 131-159.
102. Meyer U, Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog Neurobiol 2009; e-pub ahead of print.
103. van der Staay FJ, Arndt SS, Nordquist RE. Evaluation of animal models of neurobehavioral disorders. Behav Brain Funct 2009; 5: 11.
104. Kandel ER. In Search of Memory: The Emergence of a New Science of Mind Norton. New York, 2006.
105. Sattelle DB, Jones AK, Buckingham SD. Insect genomes: challenges and opportunities for neuroscience. Invert Neurosci 2007; 7: 133-136.
106. McGrath JJ, Richards LJ. Why schizophrenia epidemiology needs neurobiology-and vice versa. Schizophr Bull 2009; 35: 577-581.