Testosterone and photoperiod interact to affect spatial learning and memory in adult male white-footed mice (Peromyscus leucopus)

European Journal of Neuroscience

Volumn 23, Issue 11, 2006, Pages 3056-3062

  Pyter, Leah M ^a   Trainor, Brian C ^a   Nelson, Randy J ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Hippocampus; Seasonality; Steroid receptors; Water maze

Indexed keywords

ANDROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; SEX HORMONE; SODIUM CHLORIDE; STEROID RECEPTOR; TESTOSTERONE; WATER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CASTRATION; COMPARATIVE STUDY; CONTROLLED STUDY; EVOKED RESPONSE; GENE EXPRESSION; HIPPOCAMPUS; HORMONAL REGULATION; HORMONE ACTION; HORMONE DETERMINATION; HORMONE SUBSTITUTION; IMPLANT; INHIBITION KINETICS; LEARNING; LIGHT; MALE; MAZE TEST; MOUSE; MOUSE STRAIN; NONHUMAN; PHOTOPERIODICITY; PRIORITY JOURNAL; SPATIAL MEMORY;

ANIMALS; BEHAVIOR, ANIMAL; DRUG DELIVERY SYSTEMS; MALE; MAZE LEARNING; MEMORY; ORCHIECTOMY; PEROMYSCUS; PHOTOPERIOD; REACTION TIME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPATIAL BEHAVIOR; STATISTICS, NONPARAMETRIC; TESTOSTERONE; TIME FACTORS;

EID: 33745074105     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.04821.x     Document Type: Article

References (43)

1. Bittman E.L. Ehrlich D.A. Ogdahl J.L. Jetton A.E. ( 2003) Photoperiod and testosterone regulate androgen receptor immunostaining in the Siberian hamster brain. Biol. Reprod., 69, 876 884.
2. Bronson F.H. ( 1985) Mammalian reproduction: an ecological perspective. Biol. Reprod., 32, 1 26.
3. Bronson F.H. Heideman P.D. ( 1994) Seasonal regulation of reproduction in mammals. In Knobil E. Neill J.D., (Eds), Physiology of Reproduction. Raven Press, New York, pp. 541 584.
4. Cooke B.M. Hegstrom C.D. Breedlove S.M. ( 2002) Photoperiod-dependent response to androgen in the medial amygdala of the Siberian hamster, Phodopus sungorus. J. Biol. Rhythms, 17, 147 154.
5. Dawson J.L. Cheung Y.M. Lau R.T. ( 1975) Developmental effects of neonatal sex hormones on spatial and activity skills in the white rat. Biol. Psychol., 3, 213 229.
6. Demas G.E. Nelson R.J. ( 1998) Short-day enhancement of immune function is independent of steroid hormones in deer mice (Peromyscus maniculatus). J. Comp. Physiol. [B]., 168, 419 426.
7. Ellis G.B. Turek F.W. ( 1979) Time course of the photoperiod-induced change in sensitivity of the hypothalamic-pituitary axis to testosterone feedback in castrated male hamsters. Endocrinology, 104, 625 630.
8. Ellis G.B. Turek F.W. ( 1980) Photoperiod-induced change in responsiveness of the hypothalamic-pituitary axis to exogenous 5 alpha-dihydrotestosterone and 17 beta-estradiol in castrated male hamsters. Neuroendocrinology, 31, 205 209.
9. Galea L.A. Kavaliers M. Ossenkopp K.P. ( 1996) Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J. Exp. Biol., 199, 195 200.
10. Galea L.A. Kavaliers M. Ossenkopp K.P. Hampson E. ( 1995) Gonadal hormone levels and spatial learning performance in the Morris water maze in male and female meadow voles, Microtus pennsylvanicus. Horm. Behav., 29, 106 125.
11. Galea L.A. Kavaliers M. Ossenkopp K.P. Innes D. Hargreaves E.L. ( 1994a) Sexually dimorphic spatial learning varies seasonally in two populations of deer mice. Brain Res., 635, 18 26.
12. Galea L.A. Ossenkopp K.P. Kavaliers M. ( 1994b) Performance (re-acquisition) of a water-maze task by adult meadow voles: effects of age of initial task acquisition and in utero environment (litter sex-ratio). Behav. Brain Res., 63, 177 185.
13. Goto K. Koizumi K. Ohta Y. Hashi M. Fujii Y. Ohbo N. Saika O. Suzuki H. Saito K. Suzuki K. ( 2005) Evaluation of general behavior, memory, learning performance, and brain sexual differentiation in F1 offspring males of rats treated with flutamide during late gestation. J. Toxicol. Sci., 30, 249 259.
14. Gouchie C. Kimura D. ( 1991) The relationship between testosterone levels and cognitive ability patterns. Psychoneuroendocrinology, 16, 323 334.
15. Isgor C. Sengelaub D.R. ( 1998) Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats. Horm. Behav., 34, 183 198.
16. Jacobs L.F. ( 1996) The economy of winter: phenotypic plasticity in behavior and brain structure. Biol. Bull., 191, 92 100.
17. Jarrard L.E. Okaichi H. Steward O. Goldschmidt R.B. ( 1984) On the role of hippocampal connections in the performance of place and cue tasks: comparisons with damage to hippocampus. Behav. Neurosci., 98, 946 954.
18. Jones B.A. Watson N.V. ( 2005) Spatial memory performance in androgen insensitive male rats. Physiol. Behav., 85, 135 141.
19. Keppel G. Wickens T.D. ( 2004) Design and Analysis: A Researcher's Handbook, 4th Edn. Prentice Hall, Inc., Englewood Cliffs, NJ.
20. Lessov-Schlaggar C.N. Reed T. Swan G.E. Krasnow R.E. DeCarli C. Marcus R. Holloway L. Wolf P.A. Carmelli D. ( 2005) Association of sex steroid hormones with brain morphology and cognition in healthy elderly men. Neurology, 65, 1591 1596.
21. Loy R. Gerlach J.L. McEwen B.S. ( 1988) Autoradiographic localization of estradiol-binding neurons in the rat hippocampal formation and entorhinal cortex. Brain Res., 467, 245 251.
22. Mangels R.A. Powers J.B. Blaustein J.D. ( 1998) Effect of photoperiod on neural estrogen and progestin receptor immunoreactivity in female Syrian hamsters. Brain Res., 796, 63 74.
23. Morris R. ( 1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Meth., 11, 47 60.
24. Mukai H. Takata N. Ishii H.T. Tanabe N. Hojo Y. Furukawa A. Kimoto T. Kawato S. ( 2005) Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology. Neuroscience, 138, 757 764.
25. Naghdi N. Nafisy N. Majlessi N. ( 2001) The effects of intrahippocampal testosterone and flutamide on spatial localization in the Morris water maze. Brain Res., 897, 44 51.
26. Oberlander J.G. Schlinger B.A. Clayton N.S. Saldanha C.J. ( 2004) Neural aromatization accelerates the acquisition of spatial memory via an influence on the songbird hippocampus. Horm. Behav., 45, 250 258.
27. Perrot-Sinal T.S. Kavaliers M. Ossenkopp K.P. ( 1998) Spatial learning and hippocampal volume in male deer mice: relations to age, testosterone and adrenal gland weight. Neuroscience, 86, 1089 1099.
28. Prendergast B.J. Kriegsfeld L.J. Nelson R.J. ( 2001) Photoperiodic polyphenisms in rodents: neuroendocrine mechanisms, costs, and functions. Q. Rev. Biol., 76, 293 325.
29. Prendergast B.J. Nelson R.J. Zucker I. ( 2002) Mammalian seasonal rhythms: behavior and neuroendocrine substrates. Hormones, Brain Behav., 2, 93 156.
30. Pyter L.M. Hotchkiss A.K. Nelson R.J. ( 2005a) Photoperiod-induced differential expression of angiogenesis genes in testes of adult Peromyscus leucopus. Reproduction, 129, 201 209.
31. Pyter L.M. Neigh G.N. Nelson R.J. ( 2005b) Social environment modulates photoperiodic immune and reproductive responses in adult male white-footed mice (Peromyscus leucopus). Am. J. Physiol. Regul. Integr. Comp. Physiol., 288, R891 R896.
32. Pyter L.M. Reader B.F. Nelson R.J. ( 2005c) Short photoperiods impair spatial learning and alter hippocampal dendritic morphology in adult male white-footed mice (Peromyscus leucopus). J. Neurosci., 25, 4521 4526.
33. Roselli C.E. Resko J.A. ( 1993) Aromatase activity in the rat brain: hormonal regulation and sex differences. J. Steroid Biochem. Mol. Biol., 44, 499 508.
34. Sherry D.F. Jacobs L.F. Gaulin S.J. ( 1992) Spatial memory and adaptive specialization of the hippocampus. TINS, 15, 298 303.
35. Smulders T.V. Sasson A.D. DeVoogd T.J. ( 1995) Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee. J. Neurobiol., 27, 15 25.
36. Tetel M.J. Ungar T.C. Hassan B. Bittman E.L. ( 2004) Photoperiodic regulation of androgen receptor and steroid receptor coactivator-1 in Siberian hamster brain. Brain Res. Mol. Brain Res., 131, 79 87.
37. Thompson D.C. Thompson P.S. ( 1980) Food habits and caching behavior of urban gray squirrels. Can. J. Zool., 58, 701 710.
38. Trainor B.C. Nelson R.J. ( 2005) Differential photoperiodic regulation of reproduction and aggression in two species of Peromyscus. Horm. Behav., 48, 132.
39. Turek F.W. ( 1977) The interaction of the photoperiod and testosterone in regulating serum gonadotropin levels in castrated male hamsters. Endocrinology, 101, 1210 1215.
40. Vazquez-Pereyra F. Rivas-Arancibia S. Loaeza-Del Castillo A. Schneider-Rivas S. ( 1995) Modulation of short term and long term memory by steroid sexual hormones. Life Sci., 56, PL255 PL260.
41. Weiler H.T. Hasenohrl R.U. van Landeghem A.A. van Landeghem M. Brankack J. Huston J.P. Haas H.L. ( 1998) Differential modulation of hippocampal signal transfer by tuberomammillary nucleus stimulation in freely moving rats dependent on behavioral state. Synapse, 28, 294 301.
42. Wood R.I. Newman S.W. ( 1993) Intracellular partitioning of androgen receptor immunoreactivity in the brain of the male Syrian hamster: effects of castration and steroid replacement. J. Neurobiol., 24, 925 938.
43. Xiao L. Jordan C.L. ( 2002) Sex differences, laterality, and hormonal regulation of androgen receptor immunoreactivity in rat hippocampus. Horm. Behav., 42, 327 336.