Neurogenic and neuroendocrine effects of goldfish pheromones

Journal of Neuroscience

Volumn 28, Issue 53, 2008, Pages 14492-14499

  Chung Davidson, Yu Wen ^a   Rees, Christopher Benjamin ^a,b   Bryan, Mara Beth ^a,c   Li, Weiming ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Androstenedione; Carassius auratus; 17 ,20 dihydroxy 4 pregnen 3 one; GnRH; Neurogenesis; Prostaglandin F2

Indexed keywords

17ALPHA,2BETA DIHYDROXY 4 PREGNEN 3 ONE; ANDROGEN RECEPTOR; ANDROSTENEDIONE; CHOLINE ACETYLTRANSFERASE; GONADORELIN; PHEROMONE; PROSTAGLANDIN F2 ALPHA; UNCLASSIFIED DRUG;

ANDROSTENEDIONE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BRAIN NERVE CELL; BRAIN STEM; CEREBELLUM; CONTROLLED STUDY; DIENCEPHALON; FEMALE; GENE EXPRESSION; GOLDFISH; HISTOLOGY; MALE; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SPAWNING; TELENCEPHALON;

ANALYSIS OF VARIANCE; ANDROSTENEDIONE; ANIMALS; BRAIN CHEMISTRY; CHOLINE O-ACETYLTRANSFERASE; DIENCEPHALON; DINOPROST; GENE EXPRESSION REGULATION; GLUTAMATE DECARBOXYLASE; GOLDFISH; GONADOTROPIN-RELEASING HORMONE; HYDROXYPROGESTERONES; MALE; NEUROGENESIS; NEUROTRANSMITTER AGENTS; RECEPTORS, ANDROGEN; RNA, MESSENGER;

EID: 58149381575     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3589-08.2008     Document Type: Article

References (76)

1. Alaux C, Robinson GE (2007) Alarm pheromone induces immediate-early gene expression and slow behavioral response in honey bees. J Chem Ecol 33:1346-1350.
2. Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319-335.
3. Alvarez-Buylla A, Kirn JR (1997) Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurosci 33:585-601.
4. Ambrogini P, Cuppini R, Cuppini C, Ciaroni S, Cecchini T, Ferri P, Sartini S, Del Grande P (2000) Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci Lett 286:21-24.
5. Atema J, Holl K, Ikehara W (1980) Olfactory responses of yellowfin tuna (Thunnus albacares) to prey odors: chemical search image. J Chem Ecol 6:457-465.
6. Barnea A, Nottebohm F (1994) Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc Natl Acad Sci U S A 91:11217-11221.
7. Barnea A, Nottebohm F (1996) Recruitment and replacement of hippocampal neurons in young and adult chickadees: an addition to the theory of hippocampal learning. Proc Natl Acad Sci U S A 93:714-718.
8. Beggs KT, Glendining KA, Marechal NM, Vergoz V, Nakamura I, Slessor KN, Mercer AR (2007) Queen pheromone modulates brain dopamine function in worker honey bees. Proc Natl Acad Sci U S A 104:2460-2464.
9. Carr WE (1982) Chemical stimulation of feeding behavior. In: Chemoreception in fishes (Hara TJ, ed), pp 259-273. Amsterdam: Elsevier.
10. Cayre M, Malaterre J, Scotto-Lomassese S, Strambi C, Strambi A (2002) The common properties of neurogenesis in the adult brain: from invertebrates to vertebrates. Comp Biochem Physiol B Biochem Mol Biol 132:1-15.
11. Chetverukhin VK, Polenov AL (1993) Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. I. Ventricular zone cell proliferation. Cell Tissue Res 271:341-350.
12. Chung-Davidson YW, Bryan MB, Teeter J, Bedore CN, Li W (2008) Neuroendocrine and behavioral responses to weak electric fields in adult sea lampreys (Petromyzon marinus). Horm Behav 54:34-40.
13. Conover JC, Doetsch F, Garcia-Verdugo JM, Gale NW, Yancopoulos GD, Alvarez-Buylla A (2000) Disruption of Eph/ephrin signaling affects migration and proliferation in the adult subventricular zone. Nat Neurosci 3:1091-1097.
14. Dulka JG, Stacey NE, Sorensen PW, van der Kraak GJ (1987) A steroid sex pheromone synchronizes male-female spawning readiness in goldfish. Nature 325:251-253.
15. Fahrbach SE, Strande JL, Robinson GE (1995) Neurogenesis is absent in the brains of adult honey bees and does not explain behavioral neuroplasticity. Neurosci Lett 197:145-148.
16. Font E, Desfilis E, Pérez-Cañellas M, Alca ntara S, García-Verdugo JM (1997) 3-Acetylpyridine-induced degeneration and regeneration in the adult lizard brain: a qualitative and quantitative analysis. Brain Res 754:245-259.
17. Fraser EJ, Stacey NE (2002) Isolation increases milt production in goldfish. J Exp Zool 293:511-524.
18. García-Verdugo JM, Doetsch F, Wichterle H, Lim DA, Alvarez-Buylla A (1998) Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 36:234-248.
19. Goldman SA (1997) Comparative strategies of subependymal neurogenesis in the adult forebrain. In: Isolation, characterization and utilization of CNS stem cells (Gage FH, Christen Y, eds), pp 43-66. Berlin: Springer.
20. Goldman SA (1998) Adult neurogenesis: from canaries to the clinic. J Neurobiol 36:267-286.
21. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
22. Gronenberg W, Heeren S, Hölldobler B (1996) Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199:2011-2019.
23. Grozinger CM, Robinson GE (2007) Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:461-470.
24. Grozinger CM, Sharabash NM, Whitfield CW, Robinson GE (2003) Pheromone-mediated gene expression in the honey bee brain. Proc Natl Acad Sci U S A 100:14519-14525.
25. Grozinger CM, Fischer P, Hampton JE (2007) Uncoupling primer and releaser responses to pheromone in honey bees. Naturwissenschaften 94:375-379.
26. Hara TJ, MacDonald S, Evans RE, Marui T, Arai S (1984) Morpholin, bile acids and skin mucus as possible chemical cues in salmonid homing: electrophysiological re-evaluation. In: Mechanisms of migration in fishes (McCleave JD, Arnold GP, Dodson JJ, Neill WH, eds), pp 363-378. New York: Plenum.
27. Harzsch S, Miller J, Benton J, Beltz B (1999) From embryo to adult: persistent neurogenesis and apoptotic cell death shape the lobster deutocerebrum. J Neurosci 19:3472-3485.
28. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495.
29. Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18:3206-3212.
30. Kobayashi M, Aida K, Hanyu I (1986) Pheromone from ovulatory female goldfish induces gonadotropin surge in males. Gen Comp Endocrinol 63:451-455.
31. Kobayashi M, Aida K, Hanyu I (1989) Induction of gonadotropin surge by steroid hormone implantation in ovariectomized and sexually regressed female goldfish. Gen Comp Endocrinol 73:469-476.
32. Kobayashi M, Sorensen PW, Stacey NE (2002) Hormonal and pheromonal control of spawning behavior in the goldfish. Fish Physiol Biochem 26:71-84.
33. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, García-Verdugo JM, Alvarez-Buylla A (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28:713-726.
34. Ló pez-García C, Molowny A, García-Verdugo JM, Ferrer I (1988) Delayed postnatal neurogenesis in the cerebral cortex of lizards. Dev Brain Res 43:167-174.
35. Ló pez-García C, Molowny A, García-Verdugo JM, Pérez-Sánchez F, Martínez-Guijarro FJ (1990) Postnatal neurogenesis in the brain of the lizard Podarcis hispanica. In: The forebrain in nonmammals: new aspects of structure and development (Schwerdtfeger WK, Germroth P, eds), pp 103-117. Berlin: Springer.
36. Luskin MB (1998) Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate. J Neurobiol 36:221-233.
37. Mak GK, Enwere EK, Gregg C, Pakarainen T, Poutanen M, Huhtaniemi I, Weiss S (2007) Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat Neurosci 10:1003-1011.
38. Nottebohm F (1985) Neuronal replacement in adulthood. Ann N Y Acad Sci 457:143-161.
39. Nottebohm F (1989) From bird song to neurogenesis. Sci Am 260:74-79.
40. Olson AK, Eadie BD, Ernst C, Christie BR (2006) Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus 16:250-260.
41. Parhar IS (2002) Cell migration and evolutionary significance of GnRH subtypes. Prog Brain Res 141:3-17.
42. Partridge BL, Liley NR, Stacey NE (1976) The role of pheromones in the sexual behavior of the goldfish. Anim Behav 24:291-299.
43. Patel SN, Clayton NS, Krebs JR (1997) Spatial learning induces neurogenesis in the avian brain. Behav Brain Res 89:115-128.
44. 3H]thymidine autoradiographic and bromodeoxyuridine immunocytochemical study. Brain Res Dev Brain Res 93:49-61.
45. Pérez-Cañellas MM, Font E, García-Verdugo JM (1997) Postnatal neurogenesis in the telencephalon of turtles: evidence for nonradial migration of new neurons from distant proliferative ventricular zones to the olfactory bulbs. Brain Res Dev Brain Res 101:125-137.
46. Polenov AL, Chetverukhin VK (1993) Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. II. Types of neuronal cells produced. Cell Tissue Res 271:351-362.
47. Poling KR, Fraser EJ, Sorensen PW (2001) The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comp Biochem Physiol B Biochem Mol Biol 129:645-651.
48. Ramirez C, Nacher J, Molowny A, Sanchez-Sanchez F, Irurzun A, Lopez-Garcia C (1997) Photoperiod-temperature and neuroblast proliferation-migration in the adult lizard cortex. Neuroreport 8:2337-2442.
49. Rees CB, Li W (2004) Development and application of a real-time quantitative PCR assay for determining CYP1A transcripts in three genera of salmonids. Aquat Toxicol 66:357-368.
50. Saglio P, Fauconneau B (1985) Free amino acid content in the skin mucus of goldfish, Carassius auratus L.: influence of feeding. Comp Biochem Physiol A Comp Physiol 82:67-70.
51. Sandeman R, Sandeman D (2000) Impoverished and enriched living conditions influence the proliferation and survival of neurons in crayfish brain. J Neurobiol 45:215-226.
52. Scherwood NM, Von Schalburg K, Lescheid DW (1997) Origin and evolution of GnRH in vertebrates. In: GnRH neurons: gene to behavior (Parhar IS, Sakuma Y, eds), pp 3-25. Tokyo: Brain Shuppan.
53. Scott AP, Sorensen PW (1994) Time-course of release of pheromonally active gonadal steroids and their conjugates by ovulatory goldfish. Gen Comp Endocrinol 96:309-323.
54. Scott AP, Bye VJ, Baynes SM (1980) Seasonal variations in sex steroids of female rainbow trout (Salmo gairdnerii Richardson). J Fish Biol 17:587-592.
55. Scotto Lomassese S, Strambi C, Strambi A, Charpin P, Augier R, Aouane A, Cayre M (2000) Influence of environmental stimulation on neurogenesis in the adult insect brain. J Neurobiol 45:162-171.
56. Sorensen PW, Goetz FW (1993) Pheromonal and reproductive function of F prostaglandins and their metabolites in teleost fish. J Lipid Med 6:385-393.
57. Sorensen PW, Hara TJ, Stacey NE, Goetz FW (1988) F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol Reprod 39:1039-1050.
58. Sorensen PW, Stacey NE, Chamberlain KJ (1989) Differing behavioral and endocrionological effects of two female sex pheromones on male goldfish. Horm Behav 23:317-332.
59. Sorensen PW, Hara TJ, Stacey NE, Dulka JG (1990) Extreme olfactory specificity of the male goldfish to the preovulatory steroidal pheromone 17α,20β-dihydroxy-4-pregnen-3-one. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 166:373-384.
60. Sorensen PW, Pinillos M, Scott AP (2005) Sexually mature male goldfish release large quantities of androstenedione into the water where it functions as a pheromone. Gen Comp Endocrinol 140:164-175.
61. Stacey NE (1987) Roles of hormones and pheromones in fish reproductive behavior. In: Psychobiology of reproductive behavior, an evolutionary perspective (Crews D, ed), pp 28-60. Englewood Cliffs, NJ: Prentice Hall.
62. Stacey NE (1991) Hormonal pheromones in fish: status and prospects. In: Proceedings of the Fourth International Symposium on the Reproductive Physiology of Fish (Scott AP, Sumpter JP, Kime DS, Rolfe MS, eds), pp 177-181. Sheffield, UK: Fish Symposium 91.
63. Stacey NE (2003) Hormones, pheromones and reproductive behavior. Fish Physiol Biochem 28:229-235.
64. Stacey NE, Peter RE (1979) Central action of prostaglandins in spawning behavior of female goldfish. Physiol Behav 22:1191-1196.
65. Stacey NE, Sorensen PW (1986) 17α,20β-Dihydroxy-4-pregnen-3- one: a steroidal primer pheromone which increases milt volume in the goldfish, Carassius auratus. Can J Zool 64:2412-2417.
66. Stacey NE, Sorensen PW (2002) Fish hormonal pheromones. In: Hormones, brain, and behavior, Vol 2 (Pfaff D, Arnold D, Ategen A, Farbach S, Rubin R, eds), pp 375-435. New York: Academic.
67. Stacey NE, Fraser EJ, Sorensen PW, Van Der Kraak GJ (2001) Milt production in goldfish: regulation by multiple social stimuli. Comp Biochem Physiol C Toxicol Pharmacol 130:467-476.
68. Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23:251-258.
69. van Praag H, Kempermann G, Gage FH (1999a) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
70. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999b) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A 96:13427-13431.
71. Vergoz V, Schreurs HA, Mercer AR (2007) Queen pheromone blocks aversive learning in young worker bees. Science 317:384-386.
72. Volkoff H, Peter RE (1999) Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish (Carassius auratus). Gen Comp Endocrinol 116:347-355.
73. Yu KL, Lin X-W, Bastos JC, Peter RE (1997) Neural regulation of GnRH in teleost fishes. In: GnRH neurons: gene to behavior (Parhar IS, Sakuma Y, eds), pp 277-312. Tokyo: Brain Shuppan.
74. Zheng W, Stacey NE (1996) Two mechanisms for increasing milt volume in male goldfish. J Exp Zool 276:287-295.
75. Zheng W, Stacey NE (1997) A steroidal pheromone and spawning stimuli act via different neuroendocrine mechanisms to increase gonadotropin and milt volume in male goldfish (Carassius auratus). Gen Comp Endocrinol 105:228-238.
76. Zupanc GKH (2006) Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192:649-670.