Serotonergic modulation of startle-escape plasticity in an African cichlid fish: A single-cell molecular and physiological analysis of a vital neural circuit

Journal of Neurophysiology

Volumn 106, Issue 1, 2011, Pages 127-137

  Whitaker, K W ^a,b   Neumeister, H ^c   Huffman, L S ^a   Kidd, C E ^a   Preuss, T ^c   Hofmann, H A ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b U S ARMY RESEARCH LABORATORY   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

5 HT receptor subtype 2; Astatotilapia burtoni; Ketanserin; Mauthner cell; Single cell polymerase chain reaction

Indexed keywords

SEROTONIN; SEROTONIN 2 RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CICHLID; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ESCAPE BEHAVIOR; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL NETWORK; NONHUMAN; PLASTICITY; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; SENSORY GATING; SEROTONINERGIC SYSTEM; STARTLE ESCAPE PLASTICITY; STARTLE REFLEX;

ANIMALS; CICHLIDS; ELECTROPHYSIOLOGICAL PHENOMENA; ESCAPE REACTION; FEMALE; MALE; NEURONAL PLASTICITY; RECEPTORS, SEROTONIN; RECEPTORS, SEROTONIN, 5-HT2; SEROTONIN; SOCIAL DOMINANCE; STARTLE REACTION;

EID: 79959931131     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01126.2010     Document Type: Article

References (94)

1. Allee SJ, Markham MR, Salazar VL, Stoddard PK. Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus. Horm Behav 53: 481-488, 2008.
2. Antonsen BL, Edwards DH. Mechanisms of serotonergic facilitation of a command neuron. J Neurophysiol 98: 3494-3504, 2007.
3. Arias B, Collier DA, Gastó C, Pintor L, Gutiérrez B, Vallès V, Fañanás L. Genetic variation in the 5-HT5A receptor gene in patients with bipolar disorder and major depression. Neurosci Lett 303: 111-114, 2001.
4. Baugh LR, Hill AA, Brown EL, Hunter CP. Quantitative analysis of mRNA amplification by in vitro transcription. Nucleic Acids Res 29: E29, 2001.
5. Benjamini Y, Hochberg Y. On the adaptive control of the false discovery rate in multiple testing with independent statistics. J Educ Behav Stat 25: 60-83, 2000.
6. Bierman HS, Zottoli SJ, Hale ME. Evolution of the Mauthner axon cap. Brain Behav Evol 73: 174-187, 2009.
7. Brustein E, Chong M, Holmqvist B, Drapeau P. Serotonin patterns locomotor network activity in the developing zebrafish by modulating quiescent periods. J Neurobiol 57: 303-322, 2003.
8. Canfield JG. Temporal constraints on visually directed C-start responses: behavioral and physiological correlates. Brain Behav Evol 61: 148-158, 2003.
9. Canfield JG, Rose GJ. Hierarchical sensory guidance of Mauthner-mediated escape responses in goldfish (Carassius auratus) and cichlids (Haplochromis burtoni). Brain Behav Evol 48: 137-156, 1996.
10. Churchill GA. Fundamentals of experimental design for cDNA microarrays. Nat Genet 32: 490-495, 2002.
11. Crews D. The development of phenotypic plasticity: where biology and psychology meet. Dev Psychobiol 43: 1-10, 2003.
12. Deco G, Rolls ET. Attention, short-term memory, and action selection: a unifying theory. Prog Neurobiol 76: 236-256, 2005.
13. Dickson BJ. Wired for sex: the neurobiology of Drosophila mating decisions. Science 322: 904-909, 2008.
14. Doly S, Fischer J, Brisorgueil MJ, Vergé D, Conrath M. 5-HT5A receptor localization in the rat spinal cord suggests a role in nociception and control of pelvic floor musculature. J Comp Neurol 476: 316-329, 2004.
15. Dubertret C, Hanoun N, Adès J, Hamon M, Gorwood P. Family-based association studies between 5-HT5A receptor gene and schizophrenia. J Psychiatr Res 38: 371-376, 2004.
16. Duftner N, Larkins-Ford J, Legendre M, Hofmann HA. Efficacy of RNA amplification is dependent on sequence characteristics: implications for gene expression profiling using a cDNA microarray. Genomics 91: 108-117, 2008.
17. Eaton RC, DiDomenico R, Nissanov J. Role of the Mauthner cell in sensorimotor integration by the brain stem escape network. Brain Behav Evol 37: 272-285, 1991.
18. Eberwine J. Single-cell molecular biology. Nat Neurosci 4 Suppl: 1155-1156, 2001.
19. Edwards DH, Kravitz EA. Serotonin, social status and aggression. Curr Opin Neurobiol 7: 812-819, 1997.
20. Edwards DH, Yeh SR, Musolf BE, Antonsen BL, Krasne FB. Metamodulation of the crayfish escape circuit. Brain Behav Evol 60: 360-369, 2002.
21. Edwards DH, Heitler WJ, Krasne FB. Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci 22: 153-161, 1999.
22. Edwards DH, Issa FA, Herberholz J. The neural basis of dominance hierarchy formation in crayfish. Microsc Res Tech 60: 369-376, 2003.
23. Esumi S, Wu SX, Yanagawa Y, Obata K, Sugimoto Y, Tamamaki N. Method for single-cell microarray analysis and application to gene-expression profiling of GABAergic neuron progenitors. Neurosci Res 60: 439-451, 2008.
24. Faber DS, Korn H. Neurobiology of the Mauthner Cell. New York: Raven, 1978.
25. Faber DS, Korn H, Lin JW. Role of medullary networks and postsynaptic membrane properties in regulating Mauthner cell responsiveness to sensory excitation. Brain Behav Evol 37: 286-297, 1991.
26. Feder A, Nestler EJ, Charney DS. Psychobiology and molecular genetics of resilience. Nat Rev Neurosci 10: 446-457, 2009.
27. Fernald RD. Social regulation of the brain: sex, size and status. Novartis Found Symp 244: 169-184, 2002.
28. Fernald RD, Hirata NR. Field study of Haplochromis burtoni: habitats and co-habitants. Environ Biol Fishes 2: 299-308, 1977.
29. Flores CE, Ene S, Pereda AE. An immunochemical marker for goldfish Mauthner cells. J Neurosci Methods 175: 64-69, 2008.
30. Furukawa T, Furshpan EJ. Two inhibitory mechanisms in the Mauthner neurons of goldfish. J Neurophysiol 26: 140-176, 1963.
31. Goodson JL, Evans AK, Soma KK. Neural responses to aggressive challenge correlate with behavior in nonbreeding sparrows. Neuroreport 16: 1719-1723, 2005.
32. Gotow T, Triller A, Korn H. Differential distribution of serotonergic inputs on the goldfish Mauthner cell. J Comp Neurol 299: 255-268, 1990.
33. Hinkle D, Glanzer J, Sarabi A, Pajunen T, Zielinski J, Belt B, Miyashiro K, McIntosh T, Eberwine J. Single neurons as experimental systems in molecular biology. Prog Neurobiol 72: 129-142, 2004.
34. Hofmann HA. Functional genomics of neural and behavioral plasticity. J Neurobiol 54: 272-282, 2003.
35. Hofmann HA, Fernald RD. Social status controls somatostatin neuron size and growth. J Neurosci 20: 4740-4744, 2000.
36. Imboden M, Devignot V, Korn H, Goblet C. Regional distribution of glycine receptor messenger RNA in the central nervous system of zebrafish. Neuroscience 103: 811-830, 2001.
37. Koenig E. Ribosomal RNA in Mauthner axon: implications for a protein synthesizing machinery in the myelinated axon. Brain Res 174: 95-107, 1979.
38. Koenig E, Martin R. Cortical plaque-like structures identify ribosomecontaining domains in the Mauthner cell axon. J Neurosci 16: 1400-1411, 1996.
39. Kohno K, Noguchi N. Large myelinated club endings on the Mauthner cell in the goldfish: a study with thin sectioning and freeze-fracturing. Anat Embryol (Berl) 173: 361-370, 1986.
40. Korn H, Faber DS. The Mauthner cell half a century later: a neurobiological model for decision-making? Neuron 47: 13-28, 2005.
41. Koyama M, Kinkhabwala A, Satou C, Higachijima S, Fetcho J. Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain. Proc Natl Acad Sci USA 108: 1170-1175, 2011.
42. Krasne FB, Shamsian A, Kulkarni R. Altered excitability of the crayfish lateral giant escape reflex during agonistic encounters. J Neurosci 17: 709-716, 1997.
43. Krishnan V, Nestler EJ. The molecular neurobiology of depression. Nature 455: 894-902, 2008.
44. Kurimoto K, Saitou M. Single-cell cDNA microarray profiling of complex biological processes of differentiation. Curr Opin Genet Dev 20: 470-477, 2010.
45. Landolt HP, Wehrle R. Antagonism of serotonergic 5-HT2A/2C receptors: mutual improvement of sleep, cognition and mood? Eur J Neurosci 29: 1795-1809, 2009.
46. Maan ME, Eshuis B, Haesler MP, Schneider MV, van Alphen JJM, Seehausen O. Color polymorphism and predation in a Lake Victoria cichlid fish. Copeia 3: 621-629, 2008.
47. Maier W, Mössner R, Quednow BB, Wagner M, Hurlemann R. From genes to psychoses and back: the role of the 5HT2alpha-receptor and prepulse inhibition in schizophrenia. Eur Arch Psychiatry Clin Neurosci 258, Suppl 5: 40-43, 2008.
48. Martin KC. Local protein synthesis during axon guidance and synaptic plasticity. Curr Opin Neurobiol 14: 305-310, 2004.
49. McClung CA, Nestler EJ. Neuroplasticity mediated by altered gene expression. Neuropsychopharmacology 33: 3-17, 2008.
50. McLean DL, Fetcho JR. Relationship of tyrosine hydroxylase and serotonin immunoreactivity to sensorimotor circuitry in larval zebrafish. J Comp Neurol 29: 57-71, 2004.
51. Meyer A, Schartl M. Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions. Curr Opin Cell Biol 11: 699-704, 1999.
52. Mintz I, Korn H. Serotonergic facilitation of quantal release at central inhibitory synapses. J Neurosci 11: 3359-3370, 1991.
53. Mintz I, Gotow T, Triller A, Korn H. Effect of serotonergic afferents on quantal release at central inhibitory synapses. Science 245: 190-200, 1989.
54. Munro AD. Effects of melatonin, serotonin, and naloxone on aggression in isolated cichlid fish, Aequidens pulcher. J Pineal Res 3: 257-262, 1986.
55. Neumeister H, Szabo TM, Preuss T. Behavioral and physiological characterization of sensorimotor gating in the goldfish startle response. J Neurophysiol 99: 1493-1502, 2008.
56. Neumeister HK, Whitaker KW, Hofmann HA, Preuss T. Social and ecological regulation of a decision-making circuit. J Neurophysiol 104: 3180-3188, 2010.
57. Newman SW. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann NY Acad Sci 877: 242-257, 1999.
58. O'Connell LA, Hofmann HA. Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. Front Neuroendocrinol (December 14, 2010). doi: 10.1016/j.yfrne.2010.12.004.
59. O'Connell LA, Hofmann HA. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol. In press.
60. Pereda A, O'Brien J, Nagy JI, Bukauskas F, Davidson KG, Kamasawa N, Yasumura T, Rash JE. Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci 23: 7489-7503, 2003.
61. Pereda AE, Nairn AC, Wolszon LR, Faber DS. Postsynaptic modulation of synaptic efficacy at mixed synapses on the Mauthner cell. J Neurosci 14: 3704-3712, 1994.
62. Pereda A, Reisine T, Faber DS, Korn H. Somatostatin enhances excitatory synaptic transmission at mixed synapses on the Mauthner (M-) cell. Neurosci Soc Abstr 23: 1180, 1997.
63. Pereda A, Triller A, Korn H, Faber DS. Dopamine enhances both electrotonic coupling and chemical excitatory postsynaptic potentials at mixed synapses. Proc Natl Acad Sci USA 89: 12088-12092, 1992.
64. Petrov T, Seitanidou T, Triller A, Korn H. Differential distribution of GABA- and serotonin-containing afferents on an identified central neuron. Brain Res 559: 75-81, 1991.
65. Preuss T, Faber DS. Central cellular mechanisms underlying temperaturedependent changes in the goldfish startle-escape behavior. J Neurosci 23: 5617-5626, 2003.
66. Preuss T, Osei-Bonsu PE, Weiss SA, Wang C, Faber DS. Neural representation of object approach in a decision-making motor circuit. J Neurosci 26: 3454-3464, 2006.
67. Renn SC, Aubin-Horth N, Hofmann HA. Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray. BMC Genomics 5: 42, 2004.
68. Renn SC, Aubin-Horth N, Hofmann HA. Fish and chips: functional genomics of social plasticity in an African cichlid fish. J Exp Biol 211: 3041-3056, 2008.
69. Roberts C, Price GW, Middlemiss DN. Ligands for the investigation of 5-HT autoreceptor function. Brain Res Bull 56: 463-469, 2001.
70. Robinson GE, Fernald RD, Clayton DF. Genes and social behavior. Science 322: 896-900, 2008.
71. Salzburger W, Renn SC, Steinke D, Braasch I, Hofmann HA, Meyer A. Annotation of expressed sequence tags for the East African cichlid fish Astatotilapia burtoni and evolutionary analyses of cichlid ORFs. BMC Genomics 9: 96, 2008.
72. Satou C, Kimura Y, Kohashi T, Horikawa K, Takeda H, Oda Y, Higashijima S. Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish. J Neurosci 29: 6780- 6793, 2009.
73. Schlegel T, Schuster S. Small circuits for large tasks: high-speed decisionmaking in archerfish. Science 319: 104-106, 2008.
74. Smyth GK. Limma: linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor, edited by Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W. New York: Springer, 2005, p. 397-420.
75. Smyth GK, Thorne NP, Wettenhall J. LIMMA: Linear Models for Microarray Data, Version 1.6.6, User's Guide. 2004 [http://bioinf.wehi.edu.au/limma/].
76. Sotelo-Silveira JR, Calliari A, Cárdenas M, Koenig E, Sotelo JR. Myosin Va and kinesin II motor proteins are concentrated in ribosomal domains (periaxoplasmic ribosomal plaques) of myelinated axons. J Neurobiol 60: 187-196, 2004.
77. Spitzer N, Antonsen BL, Edwards DH. Immunocytochemical mapping and quantification of expression of a putative type 1 serotonin receptor in the crayfish nervous system. J Comp Neurol 484: 261-282, 2005.
78. Sprouse J, Reynolds L, Braselton J, Schmidt A. Serotonin-induced phase advances of SCN neuronal firing in vitro: a possible role for 5-HT5A receptors? Synapse 54: 111-118, 2004.
79. Sur C, Korn H, Triller A. Colocalization of somatostatin with GABA or glutamate in distinct afferent terminals presynaptic to the Mauthner cell. J Neurosci 14: 576-589, 1994.
80. Szabo TM, Brookings T, Preuss T, Faber DS. Effects of temperature acclimation on a central neural circuit and its behavioral output. J Neurophysiol 100: 2997-3008, 2008.
81. Teshiba T, Shamsian A, Yashar B, Yeh SR, Edwards DH, Krasne FB. Dual and opposing modulatory effects of serotonin on crayfish lateral giant escape command neurons. J Neurosci 21: 4523-4529, 2001.
82. Tietjen I, Rihel JM, Cao Y, Koentges G, Zakhary L, Dulac C. Single-cell transcriptional analysis of neuronal progenitors. Neuron 24: 161-175, 2003.
83. Trainor BC, Hofmann HA. Somatostatin and somatostatin receptor gene expression in dominant and subordinate males of an African cichlid fish. Behav Brain Res 179: 314-320, 2007.
84. Trainor BC, Hofmann HA. Somatostatin regulates aggressive behavior in an African cichlid fish. Endocrinology 147: 5119-5125, 2006.
85. Triller A, Nicola MA, Coudrier E, Louvard D, Korn H. A monoclonal antibody raised against the Mauthner cell also recognizes some reticular neurons. Neuroscience 41: 277-285, 1991.
86. Turner GF, Pitcher TJ. Attack abatement: a model for group protection by combined avoidance and dilution. Am Nat 128: 228-240, 1986.
87. Veenema AH. Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: what can we learn from animal models? Front Neuroendocrinol 30: 497-518, 2009.
88. Weiss SA, Preuss T, Faber DS. A role of electrical inhibition in sensorimotor integration. Proc Natl Acad Sci USA 105: 18047-18052, 2008.
89. Weiss SA, Zottoli SJ, Do SC, Faber DS, Preuss T. Correlation of C-start behaviors with neural activity recorded from the hindbrain in free-swimming goldfish (Carassius auratus). J Exp Biol 209: 4788-4801, 2006.
90. Winberg S, Winberg Y, Fernald RD. Effect of social rank on brain monoaminergic activity in a cichlid fish. Brain Behav Evol 49: 230-236, 1997.
91. Wong RY, Hofmann HA. Behavioral genomics: an organismal perspective. In: Encyclopedia of Life Sciences. Chichester, UK: Wiley, 2010.
92. Woolley ML, Marsden CA, Fone KC. 5-ht6 receptors. Curr Drug Targets CNS Neurol Disord 3: 59-79, 2004.
93. Yeh SR, Fricke RA, Edwards DH. The effect of social experience on serotonergic modulation of the escape circuit of crayfish. Science 271: 366-369, 1996.
94. Yeh SR, Musolf BE, Edwards DH. Neuronal adaptations to changes in the social dominance status of crayfish. J Neurosci 17: 697-708, 1997.