Testosterone modulates spatial recognition memory in male rats

Hormones and Behavior

Volumn 63, Issue 4, 2013, Pages 559-565

  Hawley, Wayne R ^a   Grissom, Elin M ^a   Martin, Ryan C ^b   Halmos, Miklos B ^b   Bart, Corrine L S ^b   Dohanich, Gary P ^a,b  

^a Tulane University   (United States)

^b TULANE UNIVERSITY   (United States)

Author keywords

Body weight; Ischiocavernosus muscle; Spatial recognition memory; Testosterone

Indexed keywords

TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; CONTROLLED STUDY; ISCHIOCAVERNOUS MUSCLE; MALE; MAZE TEST; MEMORY CONSOLIDATION; MUSCLE; NONHUMAN; ORCHIECTOMY; PRIORITY JOURNAL; RAT; RECOGNITION; SPATIAL MEMORY; TASK PERFORMANCE; WEIGHT GAIN;

ANALYSIS OF VARIANCE; ANIMALS; MALE; MAZE LEARNING; MEMORY; ORCHIECTOMY; RATS; RATS, LONG-EVANS; RECOGNITION (PSYCHOLOGY); SPACE PERCEPTION; TESTOSTERONE; WEIGHT GAIN;

EID: 84876497689     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2013.02.007     Document Type: Article

References (94)

1. Aikey J.L., Nyby J.G., Anmuth D.M., James P.J. Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Horm. Behav. 2002, 42:448-460.
2. Beatty W.W., O'Briant D.A., Vilberg T.R. Effects of ovariectomy and estradiol injections on food intake and body weight in rats with ventromedial hypothalamic lesions. Pharmacol. Biochem. Behav. 1975, 3:539-544.
3. Benice T.S., Raber J. Dihydrotestosterone modulates spatial working-memory performance in male mice. J. Neurochem. 2009, 110:902-911.
4. Benice T.S., Raber J. Castration and training in a spatial task alter the number of immature neurons in the hippocampus of male mice. Brain Res. 2010, 1329:21-29.
5. Bernardi M., Genedani S., Tagliavini S., Bertolini A. Effect of castration and testosterone in experimental models of depression in mice. Behav. Neurosci. 1989, 103:1148-1150.
6. Bonilla-Jaime H., Vazquez-Palacios G., Arteaga-Silva M., Retana-Marquez S. Hormonal responses to different sexually related conditions in male rats. Horm. Behav. 2006, 49:376-382.
7. Buddenberg T.E., Komorowski M., Ruocco L.A., Silva M.A., Topic B. Attenuating effects of testosterone on depressive-like behavior in the forced swim test in healthy male rats. Brain Res. Bull. 2009, 79:182-186.
8. Carrier N., Kabbaj M. Extracellular signal-regulated kinase 2 signaling in the hippocampal dentate gyrus mediates the antidepressant effects of testosterone. Biol. Psychiatry 2012, 71:642-651.
9. Collins W.F., Seymour A.W., Klugewicz S.W. Differential effect of castration on the somal size of pudendal motoneurons in the adult male rat. Brain Res. 1992, 577:326-330.
10. Conrad C.D., Galea L.A., Kuroda Y., McEwen B.S. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 1996, 110:1321-1334.
11. Conrad C.D., Jackson J.L., Wieczorek L., Baran S.E., Harman J.S., Wright R.L., Korol D.L. Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharmacol. Biochem. Behav. 2004, 78:569-579.
12. Daniel J.M., Fader A.J., Spencer A.L., Dohanich G.P. Estrogen enhances performance of female rats during acquisition of a radial arm maze. Horm. Behav. 1997, 32:217-225.
13. Daniel J.M., Winsauer P.J., Moerschbaecher J.M. Castration in rats impairs performance during acquisition of a working memory task and exacerbates deficits in working memory produced by scopolamine and mecamylamine. Psychopharmacology (Berl) 2003, 170:294-300.
14. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
15. Dellu F., Mayo W., Cherkaoui J., Le Moal M., Simon H. A two-trial memory task with automated recording: study in young and aged rats. Brain Res. 1992, 588:132-139.
16. Dohanich G. Gonadal steroids, learning, and memory. Hormones, Brain and Behavior 2002, 265-327. Academic Press, San Diego. D. Pfaff, A. Arnold, A. Etgen, S. Fahrback, R. Rubin (Eds.).
17. Edinger K.L., Frye C.A. Androgens' performance-enhancing effects in the inhibitory avoidance and water maze tasks may involve actions at intracellular androgen receptors in the dorsal hippocampus. Neurobiol. Learn. Mem. 2007, 87:201-208.
18. Eichenbaum H. The Cognitive Neuroscience of Memory: An Introduction 2002, Oxford University Press, New York, NY.
19. Ennaceur A., Neave N., Aggleton J.P. Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Exp. Brain Res. 1997, 113:509-519.
20. Ferguson D., Sapolsky R. Overexpression of mineralocorticoid and transdominant glucocorticoid receptor blocks the impairing effects of glucocorticoids on memory. Hippocampus 2008, 18:1103-1111.
21. Fernandez-Guasti A., Martinez-Mota L. Anxiolytic-like actions of testosterone in the burying behavior test: role of androgen and GABA-benzodiazepine receptors. Psychoneuroendocrinology 2005, 30:762-770.
22. Foilb A.R., Lui P., Romeo R.D. The transformation of hormonal stress responses throughout puberty and adolescence. J. Endocrinol. 2011, 210:391-398.
23. Foy M.R. Ovarian hormones, aging and stress on hippocampal synaptic plasticity. Neurobiol. Learn. Mem. 2011, 95:134-144.
24. Frye C.A., Seliga A.M. Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn. Affect. Behav. Neurosci. 2001, 1:371-381.
25. Frye C.A., Walf A.A. Depression-like behavior of aged male and female mice is ameliorated with administration of testosterone or its metabolites. Physiol. Behav. 2009, 97:266-269.
26. Frye C.A., Rhodes M.E., Rosellini R., Svare B. The nucleus accumbens as a site of action for rewarding properties of testosterone and its 5alpha-reduced metabolites. Pharmacol. Biochem. Behav. 2002, 74:119-127.
27. Gentry R.T., Wade G.N. Androgenic control of food intake and body weight in male rats. J. Comp. Physiol. Psychol. 1976, 90:18-25.
28. Gibbs R.B. Testosterone and estradiol produce different effects on cognitive performance in male rats. Horm. Behav. 2005, 48:268-277.
29. Goel N., Plyler K.S., Daniels D., Bale T.L. Androgenic influence on serotonergic activation of the HPA stress axis. Endocrinology 2011, 152:2001-2010.
30. Goudsmit E., Van de Poll N.E., Swaab D.F. Testosterone fails to reverse spatial memory decline in aged rats and impairs retention in young and middle-aged animals. Behav. Neural Biol. 1990, 53:6-20.
31. Grissom E.M., Hawley W.R., Bromley-Dulfano S.S., Marino S.E., Stathopoulos N.G., Dohanich G.P. Learning strategy is influenced by trait anxiety and early rearing conditions in prepubertal male, but not prepubertal female rats. Neurobiol. Learn. Mem. 2012, 98:174-181.
32. Handa R.J., Nunley K.M., Lorens S.A., Louie J.P., McGivern R.F., Bollnow M.R. Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors. Physiol. Behav. 1994, 55:117-124.
33. Harley C.W., Malsbury C.W., Squires A., Brown R.A. Testosterone decreases CA1 plasticity in vivo in gonadectomized male rats. Hippocampus 2000, 10:693-697.
34. Harrell L.E., Goyal M., Parsons D.S., Peagler A. The effect of gonadal steroids on the behavioral and biochemical effects of hippocampal sympathetic ingrowth. Physiol. Behav. 1990, 48:507-513.
35. Hatanaka Y., Mukai H., Mitsuhashi K., Hojo Y., Murakami G., Komatsuzaki Y., Sato R., Kawato S. Androgen rapidly increases dendritic thorns of CA3 neurons in male rat hippocampus. Biochem. Biophys. Res. Commun. 2009, 381:728-732.
36. Hawley W.R., Grissom E.M., Dohanich G.P. The relationships between trait anxiety, place recognition memory, and learning strategy. Behav. Brain Res. 2011, 216:525-530.
37. Hawley W.R., Grissom E.M., Barratt H.E., Conrad T.S., Dohanich G.P. The effects of biological sex and gonadal hormones on learning strategy in adult rats. Physiol. Behav. 2012, 105:1014-1020.
38. Hawley W.R., Grissom E.M., Patel J.M., Hodges K.S., Dohanich G.P. Reactivation of an aversive memory modulates learning strategy preference in male rats. Stress 2013, 16:73-86.
39. Hojo Y., Hattori T.A., Enami T., Furukawa A., Suzuki K., Ishii H.T., Mukai H., Morrison J.H., Janssen W.G., Kominami S., Harada N., Kimoto T., Kawato S. Adult male rat hippocampus synthesizes estradiol from pregnenolone by cytochromes P45017alpha and P450 aromatase localized in neurons. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:865-870.
40. Hughes A.M., Everitt B.J., Herbert J. Comparative effects of preoptic area infusions of opioid peptides, lesions and castration on sexual behaviour in male rats: studies of instrumental behaviour, conditioned place preference and partner preference. Psychopharmacology (Berl) 1990, 102:243-256.
41. Inagaki T., Gautreaux C., Luine V. Acute estrogen treatment facilitates recognition memory consolidation and alters monoamine levels in memory-related brain areas. Horm. Behav. 2010, 58:415-426.
42. Jonasson Z. Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci. Biobehav. Rev. 2005, 28:811-825.
43. Jones B.A., Watson N.V. Spatial memory performance in androgen insensitive male rats. Physiol. Behav. 2005, 85:135-141.
44. Kerr J.E., Allore R.J., Beck S.G., Handa R.J. Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 1995, 136:3213-3221.
45. Khalil R., King M.A., Soliman M.R. Testosterone reverses ethanol-induced deficit in spatial reference memory in castrated rats. Pharmacology 2005, 75:87-92.
46. Konkle A.T., McCarthy M.M. Developmental time course of estradiol, testosterone, and dihydrotestosterone levels in discrete regions of male and female rat brain. Endocrinology 2011, 152:223-235.
47. Kus L., Handa R.J., Hautman J.M., Beitz A.J. Castration increases [125I]MK801 binding in the hippocampus of male rats. Brain Res. 1995, 683:270-274.
48. Leranth C., Petnehazy O., MacLusky N.J. Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J. Neurosci. 2003, 23:1588-1592.
49. Li M., Masugi-Tokita M., Takanami K., Yamada S., Kawata M. Testosterone has sublayer-specific effects on dendritic spine maturation mediated by BDNF and PSD-95 in pyramidal neurons in the hippocampus CA1 area. Brain Res. 2012, 1484:76-84.
50. Luine V.N. Sex steroids and cognitive function. J. Neuroendocrinol. 2008, 20:866-872.
51. Luine V., Dohanich G. Sex differences in cognitive function in rodents. Sex Differences in the Brain 2008, 227-251. Oxford University Press, New York. J. Becker, K. Berkley, N. Geary, E. Hampson, J. Herman, E. Young (Eds.).
52. Luine V., Rodriguez M. Effects of estradiol on radial arm maze performance of young and aged rats. Behav. Neural Biol. 1994, 62:230-236.
53. Lund T.D., Hinds L.R., Handa R.J. The androgen 5alpha-dihydrotestosterone and its metabolite 5alpha-androstan-3beta, 17beta-diol inhibit the hypothalamo-pituitary-adrenal response to stress by acting through estrogen receptor beta-expressing neurons in the hypothalamus. J. Neurosci. 2006, 26:1448-1456.
54. Markham J.A., Pych J.C., Juraska J.M. Ovarian hormone replacement to aged ovariectomized female rats benefits acquisition of the morris water maze. Horm. Behav. 2002, 42:284-293.
55. McConnell S.E., Alla J., Wheat E., Romeo R.D., McEwen B., Thornton J.E. The role of testicular hormones and luteinizing hormone in spatial memory in adult male rats. Horm. Behav. 2012, 61:479-486.
56. McCormick C.M., Linkroum W., Sallinen B.J., Miller N.W. Peripheral and central sex steroids have differential effects on the HPA axis of male and female rats. Stress 2002, 5:235-247.
57. McLaughlin K.J., Bimonte-Nelson H., Neisewander J.L., Conrad C.D. Assessment of estradiol influence on spatial tasks and hippocampal CA1 spines: evidence that the duration of hormone deprivation after ovariectomy compromises 17beta-estradiol effectiveness in altering CA1 spines. Horm. Behav. 2008, 54:386-395.
58. Minerly A.E., Russo S.J., Kemen L.M., Nazarian A., Wu H.B., Weierstall K.M., Akhavan A., Jenab S., Quinones-Jenab V. Testosterone plays a limited role in cocaine-induced conditioned place preference and locomotor activity in male rats. Ethn. Dis. 2008, 18:S2-200-204.
59. Mitsushima D., Takase K., Funabashi T., Kimura F. Gonadal steroids maintain 24h acetylcholine release in the hippocampus: organizational and activational effects in behaving rats. J. Neurosci. 2009, 29:3808-3815.
60. Naghdi N., Nafisy N., Majlessi N. The effects of intrahippocampal testosterone and flutamide on spatial localization in the Morris water maze. Brain Res. 2001, 897:44-51.
61. Nelson R.J. An Introduction to Behavioral Endocrinology 2005, Sinauer Associates, Inc., Sunderland, MA. Third edition.
62. Nguyen T.V., Yao M., Pike C.J. Androgens activate mitogen-activated protein kinase signaling: role in neuroprotection. J. Neurochem. 2005, 94:1639-1651.
63. Nguyen T.V., Yao M., Pike C.J. Dihydrotestosterone activates CREB signaling in cultured hippocampal neurons. Brain Res. 2009, 1298:1-12.
64. Okamoto M., Hojo Y., Inoue K., Matsui T., Kawato S., McEwen B.S., Soya H. Mild exercise increases dihydrotestosterone in hippocampus providing evidence for androgenic mediation of neurogenesis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:13100-13105.
65. Olton D.S. Spatial memory. Sci. Am. 1977, 236:82-84. (89-94, 96, 98).
66. Olton D.S., Papas B.C. Spatial memory and hippocampal function. Neuropsychologia 1979, 17:669-682.
67. Ota H., Akishita M., Akiyoshi T., Kahyo T., Setou M., Ogawa S., Iijima K., Eto M., Ouchi Y. Testosterone deficiency accelerates neuronal and vascular aging of SAMP8 mice: protective role of eNOS and SIRT1. PLoS One 2012, 7:e29598.
68. Packard M.G., Teather L.A. Posttraining estradiol injections enhance memory in ovariectomized rats: cholinergic blockade and synergism. Neurobiol. Learn. Mem. 1997, 68:172-188.
69. Packard M.G., Schroeder J.P., Alexander G.M. Expression of testosterone conditioned place preference is blocked by peripheral or intra-accumbens injection of alpha-flupenthixol. Horm. Behav. 1998, 34:39-47.
70. Pouliot W.A., Handa R.J., Beck S.G. Androgen modulates N-methyl-d-aspartate-mediated depolarization in CA1 hippocampal pyramidal cells. Synapse 1996, 23:10-19.
71. Rodgers S.P., Bohacek J., Daniel J.M. Transient estradiol exposure during middle age in ovariectomized rats exerts lasting effects on cognitive function and the hippocampus. Endocrinology 2010, 151:1194-1203.
72. Romeo R.D., Staub D., Jasnow A.M., Karatsoreos I.N., Thornton J.E., McEwen B.S. Dihydrotestosterone increases hippocampal N-methyl-d-aspartate binding but does not affect choline acetyltransferase cell number in the forebrain or choline transporter levels in the CA1 region of adult male rats. Endocrinology 2005, 146:2091-2097.
73. Rossbach U.L., Steensland P., Nyberg F., Le Greves P. Nandrolone-induced hippocampal phosphorylation of NMDA receptor subunits and ERKs. Biochem. Biophys. Res. Commun. 2007, 357:1028-1033.
74. Sakata K., Tokue A., Kawai N. Altered synaptic transmission in the hippocampus of the castrated male mouse is reversed by testosterone replacement. J. Urol. 2000, 163:1333-1338.
75. Sandstrom N.J., Kim J.H., Wasserman M.A. Testosterone modulates performance on a spatial working memory task in male rats. Horm. Behav. 2006, 50:18-26.
76. Seale J.V., Wood S.A., Atkinson H.C., Harbuz M.S., Lightman S.L. Gonadal steroid replacement reverses gonadectomy-induced changes in the corticosterone pulse profile and stress-induced hypothalamic-pituitary-adrenal axis activity of male and female rats. J. Neuroendocrinol. 2004, 16:989-998.
77. Simerly R.B., Chang C., Muramatsu M., Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp. Neurol. 1990, 294:76-95.
78. Smith S.T., Stackman R.W., Clark A.S. Spatial working memory is preserved in rats treated with anabolic-androgenic steroids. Brain Res. 1996, 737:313-316.
79. Smith M.D., Jones L.S., Wilson M.A. Sex differences in hippocampal slice excitability: role of testosterone. Neuroscience 2002, 109:517-530.
80. Spritzer M.D., Galea L.A. Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev. Neurobiol. 2007, 67:1321-1333.
81. Spritzer M.D., Gill M., Weinberg A., Galea L.A. Castration differentially affects spatial working and reference memory in male rats. Arch. Sex. Behav. 2008, 37:19-29.
82. Spritzer M.D., Daviau E.D., Coneeny M.K., Engelman S.M., Prince W.T., Rodriguez-Wisdom K.N. Effects of testosterone on spatial learning and memory in adult male rats. Horm. Behav. 2011, 59:484-496.
83. Toufexis D., Davis C., Hammond A., Davis M. Sex differences in hormonal modulation of anxiety measured with light-enhanced startle: possible role for arginine vasopressin in the male. J. Neurosci. 2005, 25:9010-9016.
84. Viau V., Meaney M.J. The inhibitory effect of testosterone on hypothalamic-pituitary-adrenal responses to stress is mediated by the medial preoptic area. J. Neurosci. 1996, 16:1866-1876.
85. Viau V., Lee P., Sampson J., Wu J. A testicular influence on restraint-induced activation of medial parvocellular neurons in the paraventricular nucleus in the male rat. Endocrinology 2003, 144:3067-3075.
86. Wade G.N. Gonadal hormones and behavioral regulation of body weight. Physiol. Behav. 1972, 8:523-534.
87. Wainwright S.R., Lieblich S.E., Galea L.A. Hypogonadism predisposes males to the development of behavioural and neuroplastic depressive phenotypes. Psychoneuroendocrinology 2011, 36:1327-1341.
88. Woolley C.S., Gould E., Frankfurt M., McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 1990, 10:4035-4039.
89. Wright R.L., Conrad C.D. Chronic stress leaves novelty-seeking behavior intact while impairing spatial recognition memory in the Y-maze. Stress 2005, 8:151-154.
90. Wright R.L., Conrad C.D. Enriched environment prevents chronic stress-induced spatial learning and memory deficits. Behav. Brain Res. 2008, 187:41-47.
91. Wright R.L., Lightner E.N., Harman J.S., Meijer O.C., Conrad C.D. Attenuating corticosterone levels on the day of memory assessment prevents chronic stress-induced impairments in spatial memory. Eur. J. Neurosci. 2006, 24:595-605.
92. Xiao L., Jordan C.L. Sex differences, laterality, and hormonal regulation of androgen receptor immunoreactivity in rat hippocampus. Horm. Behav. 2002, 42:327-336.
93. Ziehn M.O., Avedisian A.A., Dervin S.M., Umeda E.A., O'Dell T.J., Voskuhl R.R. Therapeutic testosterone administration preserves excitatory synaptic transmission in the hippocampus during autoimmune demyelinating disease. J. Neurosci. 2012, 32:12312-12324.
94. Zuloaga D.G., Poort J.E., Jordan C.L., Breedlove S.M. Male rats with the testicular feminization mutation of the androgen receptor display elevated anxiety-related behavior and corticosterone response to mild stress. Horm. Behav. 2011, 60:380-388.