Intra hippocampal injection of testosterone impaired acquisition, consolidation and retrieval of inhibitory avoidance learning and memory in adult male rats

Behavioural Brain Research

Volumn 188, Issue 1, 2008, Pages 71-77

  Harooni, Hooman Eshagh ^a,b   Naghdi, Nasser ^b   sepehri, Hoori ^a   Rohani, Ali Haeri ^a  

^a UNIVERSITY OF TEHRAN   (Iran)

^b PASTEUR INSTITUTE OF IRAN   (Iran)

Author keywords

Consolidation; Gonadectomy; Inhibitory avoidance learning; Intra hippocampal; Retrieval; Testosterone

Indexed keywords

TESTOSTERONE;

ANALYTIC METHOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; CASTRATION; COMPARATIVE STUDY; CONTROLLED STUDY; GONADECTOMY; HIPPOCAMPUS; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; RAT; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; HIPPOCAMPUS; INHIBITION (PSYCHOLOGY); MALE; MENTAL RECALL; MICROINJECTIONS; RATS; RATS, WISTAR; STATISTICS, NONPARAMETRIC; TESTOSTERONE;

EID: 38749095966     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2007.10.017     Document Type: Article

References (77)

1. Bannerman D.M., Deacon R.M., Offen S., Friswell J., Grubb M., and Rawlins J.N. Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. Behav Neurosci 116 (2002) 884-901
2. Barret-Conner E., Goodman-Gruen D., and Patay B. Endogenous sex hormones and cognitive function in older men. J Clin Endocrinol Metab 84 (1999) 3681-3685
3. Beato M., Herrlich P., and Schutz G. Steroid hormone receptors: many actors in search of a plot. Cell 83 (1995) 851-857
4. Benten W.P.M., Leiberherr M., Giese G., Wrehlke C., Stamm O., Sekeris C.E., et al. Functional testosterone receptors in plasma membranes of T cells. FASEB J 13 (1999) 123-133
5. Beyenburg S., Watzka M., Clusmann H., Blumcke I., Bidlingmaier F., Elger C.E., et al. Androgen receptor mRNA expression in the human hippocampus. Neurosci Lett 94 (2000) 25-28
6. Bimonte-Nelson H.A., Singleton R.S., Nelson M.E., Eckman C.B., Barber J., Scott T.Y., et al. Testosterone, but not nonaromatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Exp Neurol 181 (2003) 301-312
7. Castellano C., Cabib S., and Puglisi-Allegra S. Psychopharmacology of memory modulation: evidence for multiple interaction among neurotransmitters and hormones. Behav Brain Res 77 1-2 (1996) 1-21
8. Christian C.H., Rolls N.J., and Morris J.F. Nongenomic action of testosterone on a subset of lactotrophs in the male rat pituitary. Endocrinology 141 9 (2000) 3111-3119
9. Clancy A.N., Clancy A.N., Bonsall R.W., and Michael R.P. Immunohistochemical labeling of androgen receptors in the brain of rat and monkey. Life Sci 50 (1992) 409-417
10. Collins P., and Webb C. Estrogen hits the surface. Nat Med 5 (1999) 1130-1131
11. Dazzi L., Sanna A., Cagetti E., Concas A., and Biggio G. Inhibition by the neurosteroid allopregnanolone of basal and stress-induced acetylcholine release in the brain of freely moving rats. Brain Res 710 1-2 (1996) 275-280
12. Debonnel G., Bergeron R., and Montigny C.D. Potentiation by dehydroepiandrosterone of the neonatal response to N-methyl-d-aspartate in the CA3 region of the rat dorsal hippocampus: an effect mediated via sigma receptors. J Endocrinol 150 (1996) 33-42
13. Edinger K.L., and Frye C.A. Androgens' effects to enhance learning may be mediated in part through actions at estrogen receptor-beta in the hippocampus. Neurobiol Learn Mem 87 1 (2007) 78-85
14. Edinger K.L., and Frye C.A. Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5alpha-reduced metabolites in the hippocampus. Behav Neurosci 118 6 (2004) 1352-1364
15. Edinger K.L., Lee B., and Frye C.A. Mnemonic effects of testosterone and its 5alpha-reduced metabolites in the conditioned fear and inhibitory avoidance tasks. Pharmacol Biochem Behav 78 3 (2004) 559-568
16. Evans R.M. The steroid and thyroid hormone receptor superfamily. Science 240 4854 (1988) 889-895
17. Flood L.F., Farr S.A., Kaiser F.E., La Regina M., and Morley J.E. Age-related decrease of plasma testosterone in SAMP8 mice: replacement improves age-related impairment of learning and memory. Phisiol Behav 57 (1995) 669-673
18. Foy M.R., and Teyler T.J. 17-alpha-Estradiol and 17-beta-estradiol in hippocampus. Brain Res Bull 10 6 (1983) 735-739
19. Frye C.A., Edinger K.L., Seliga A.M., and Wawrzycki J.M. 5alpha-reduced androgens may have actions in the hippocampus to enhance cognitive performance of male rats. Psychoneuroendocrinology 29 8 (2004) 1019-1027
20. Frye C.A., and Seliga A.M. Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn Affective Behav Neurosci 1 (2001) 371-381
21. Frye C.A., Van Keuren K.R., and Erskine M.S. Behavioral effects of 3alpha-androstanediol. I. Modulation of sexual receptivity and promotion of GABA-stimulated chloride flux. Behav Brain Res 79 1-2 (1996) 109-118
22. Gouchie C., and Kimura D. The relationship between testosterone levels and cognitive ability patterns. Psychoneuroendocrinology 16 4 (1991) 323-334
23. Goudsmith E., Van De Poll N.E., and 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 53 (1990) 6-20
24. Hampson E. Spatial cognition in humans: possible modulation by androgens and estrogens. J Psychol Neurosci 20 (1995) 397-404
25. Isgor C., and Sengelaub D.R. Effects of neonatal gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats. J Neurobiol 55 2 (2003) 179-190
26. Izquierdo I., and McGaugh J.L. Behavioral pharmacology and its contribution to the molecular basis of memory consolidation. Behav Pharmacol 11 (2000) 517-534
27. Izquierdo I., and Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem 68 (1997) 285-316
28. Izquierdo I., Quillfeldt J.A., Zanatta M.S., Quevedo J., Schaeffer E., Schmitz P.K., et al. Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. Eur J Neurosci 9 (1997) 786-793
29. Izquierdo L.A., Barros D.M., Vianna M.R., Coitinho A., deDavid e Silva T., Choi H., et al. Molecular pharmacological dissection of short- and long-term memory. Cell Mol Neurobiol 22 (2002) 269-288
30. Jafari-Sabet M. NMDA receptor blockers prevents the facilitatory effects of post-training intra-dorsal hippocampal NMDA and physostigmine on memory retention of passive avoidance learning in rats. Behav Brain Res 169 1 (2006) 120-127
31. Janowsky J.S., Oviatt S.K., and Orwoll E.S. Testosterone influences spatial cognition in older men. Behav Neurosci 108 2 (1994) 325-332
32. Kaut K.P., and Bunsey M.D. The effects of lesions to the rat hippocampus or rhinal cortex on olfactory and spatial memory: retrograde and anterograde findings. Cogn Affect Behav Neurosci 1 3 (2001) 270-286
33. Kerr J.E., Allore R.J., Beck S.G., and Handa R.J. Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 136 8 (1995) 3213-3221
34. Kritzer M.F., McLaughlin P.J., Smirlis T., and Robinson J.K. Gonadectomy impairs T-maze acquisition in adult male rats. Horm Behav 39 2 (2001) 167-174
35. Kudriashova I.V. Reaction of hippocampal neurons at different stages of rat avoidance conditioning. Zh Vyssh Nerv Deiat Im I P Pavolva 51 2 (2001) 182-189
36. 125I] MK801 binding in the hippocampus of male rats. Brain Res 683 (1995) 270-274
37. Lauber A.H., and Whalen R.E. Muscarinic cholinergic modulation of hypothalamic estrogen binding site. Brain Res 443 (1998) 21-26
38. Leiberherr M., and Grosse B. Androgen increases intracellular calcium concentration and inositol 1,4,5-triphosphate and diacylglycerol formation via a pertusis toxin-sensitive G protein. J Biol Chem 269 10 (1994) 7217-7223
39. Lorenzini C.A., Baldi E., Bucherelli C., Sacchetti B., and Tassoni G. Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response: a tetrodotoxin functional inactivation study. Brain Res 730 (1996) 32-39
40. Lund B.C., Bever-Stille K.A., and Perry P.J. Testosterone and andropause: the feasibility of testosterone replacement therapy in older men. Pharmacotherapy 8 (1999) 951-956
41. MacLusky N.J., Hajszan T., Prange-Kiel J., and Leranth C. Androgen modulation of hippocampal synaptic plasticity. Neuroscience 138 3 (2006) 957-965
42. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., and Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232 4753 (1986) 1004-1007
43. Martinez G.L., Quirarte S., Diaz-Cintra C., Quiroz M.L., and Prado-Alcala R.A. Effects of lesions of hippocampal fields CA1 and CA on acquisition of inhibitory avoidance. Neuropsychobiology 46 (2002) 97-103
44. McAbee M.D., and DonCarlos L.L. Ontogeny of regionspecific sex differences in androgen messenger ribonucleic acid expression in the rat forebrain. Endocrinology 139 4 (1998) 1738-1745
45. McCarthy M.M. Functional significance of steroid modulation of GABAergic neurotransmission analysis at the behavioral, cellular and molecular levels. Horm Behav 29 (1995) 131-140
46. McGaugh J.L. Memory-a century of consolidation. Science 287 (2000) 248-251
47. Mienville J.M., and Vicini S. Pregnenolone sulfate antagonizes GABAA receptor-mediated currents via a reduction of channel opening frequency. Brain Res 489 1 (1989) 190-194
48. Moor E., DeBoer P., and Westerink B.H. GABA receptors and benzodiazepine binding sites modulate hippocampal acetylcholine release in vivo. Eur J Pharmacol 359 2-3 (1998) 119-126
49. Moradpour F., Naghdi N., and Fathollahi Y. Anastrozole improved testosterone-induced impairment acquisition of spatial learning and memory in the hippocampal CA1 region in adult male rats. Behav Brain Res 175 2 (2006) 223-232
50. Mukai H., Takata N., Ishii H.T., Tanabe N., Hojo Y., Furukawa A., et al. Hippocampal synthesis of estrogens and androgens which are paracrine modulators of synaptic plasticity: synaptocrinology. Neuroscience 138 3 (2006) 757-764
51. Naghdi N., and Asadollahi A. Genomic and nongenomic effects of intrahippocampal microinjection of testosterone on long-term memory in male adult rats. Behav Brain Res 153 1 (2004) 1-6
52. Naghdi N., Mohaddess G., Khamnei S., and Arjomand M. No significant differences between intact and testosterone depleted or administered male rats in spatial learning and memory. Iran J Pharmaceut Res 1 (2005) 29-32
53. Naghdi N., Nafisy N., and Majlesi N. The effects of intrahippocampal testosterone and flutamide on spatial localization in the Morris water maze. Brain Res 897 (2001) 44-51
54. Naghdi N., Oryan S., and Etemadi R. The study of spatial memory in adult male rats with injection of testosterone enanthate and flutamide into the basolateral nucleus of the amygdala in Morris water maze. Brain Res 972 1-2 (2003) 1-8
55. O'Malley B.W. The steroid receptor superfamily: more excitement predicted for future. Mol Endocrinol 4 (1990) 363-369
56. Paden C.M., and Roselli C.E. Modulation of aromatase activity by testosterone in transplants of fetal rat hypothalamus-preoptic area. Brain Res 430 (1987) 127-133
57. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1986), Academic Press, New York
58. Pouliot W.A., Handa R.J., and Beck S.G. Androgen modulates N-methyl-d-aspartate-mediated depolarization in CA1 hippocampal pyramidal cells. Synapse 23 1 (1996) 10-19
59. Riedel G., Micheau J., Lam A.G., Roloff E.L., Martin S.J., Bridge H., et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci 2 (1999) 898-905
60. Roselli C.E., Horton L.E., and Resko J.A. Time-course and steroid specificity of aromatase induction in rat hypothalamus-preoptic area. Biol Reprod 37 3 (1987) 628-633
61. Rupprecht R., and Holsboer F. Neuroactive steroids: mechanisms of action and neuropsychopharmacological perspectives. Trends Neurosci 22 9 (1999) 410-416
62. Russell K.S., Haynes M.P., Sinha D., Clerisme E., and Bender J.R. Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci USA 97 (2000) 5930-5935
63. Sar M., Lubahn D.B., French F.S., and Wilson E.M. Immunohistochemical localization of the androgen receptor in rat and human tissues. Endocrinology 127 6 (1990) 3180-3186
64. Shibuya K., Takata N., Hojo Y., Furukawa A., Yasumatsu N., Kimoto T., et al. Hippocampal cytochrome P450s synthesize brain neurosteroids which are paracrine neuromodulators of synaptic signal transduction. Biochim Biophys Acta 1619 3 (2003) 301-316
65. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294 (1990) 76-95
66. Smith M.D., Jones L.S., and Wilson M.A. Sex differences in hippocampal slice excitability: role of testosterone. Neuroscience 109 3 (2002) 517-530
67. Sternbach H. Age-associated testosterone decline in men: clinical issues for psychiatry. Am J Psychiatry 155 10 (1998) 1310-1318
68. Tan R.S. Memory loss as a reported symptom of andropause. Arch Androl 47 3 (2001) 185-189
69. Teyler T.J., Vardaris R.M., Lewis D., and Rawitch A.B. Gonadal steroids: effects on excitability of hippocampal pyramidal cells. Science 209 4460 (1980) 1017-1018
70. Truss M., and Beato M. Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocr Rev 14 4 (1993) 459-479
71. Twyman R.E., and Macdonald R.L. Neurosteroid regulation of GABAA receptor single-channel kinetic properties of mouse spinal cord neurons in culture. J Physiol 456 (1992) 215-245
72. Vazquez-Pereyra F., Rivas-Arancibia S., Loaeza-Del Castillo A., and Schneider-Rivas S. Modulation of short term and long term memory by steroid sexual hormones. Life Sci 56 (1995) 255-260
73. Wide J.K., Hanratty K., Ting J., and Galea L.A. High level estradiol impairs and low level estradiol facilitates non-spatial working memory. Behav Brain Res 155 (2004) 45-53
74. Wong M., and Moss R.L. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J Neurosci 12 8 (1992) 3217-3225
75. Wong M., and Moss R.L. Patch-clamp analysis of direct steroidal modulation of glutamate receptor-channels. J Neuroendocrinol 6 3 (1994) 347-355
76. Xiao L., and Jordan C.L. Sex differences, laterality, and hormonal regulation of androgen receptor immunoreactivity in rat hippocampus. Horm Behav 42 3 (2002) 327-336
77. Zhang J., Chang Y.H., Fildman N.A., Ma W., Jahsousi F., Barkes J.Z., et al. The expression of GABA-A receptor α2 subunit is up regulated by testosterone in rat cerebral cortex. Neurosci Lett 265 (1999) 25-28