Castration differentially affects spatial working and reference memory in male rats

Archives of Sexual Behavior

Volumn 37, Issue 1, 2008, Pages 19-29

  Spritzer, Mark D ^a,b   Gill, Mandeep ^a   Weinberg, Alex ^a   Galea, Liisa A M ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b MIDDLEBURY COLLEGE   (United States)

Author keywords

Androgens; Morris water maze; Radial arm maze; Rats; Spatial memory

Indexed keywords

ANDROGEN; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AVERSIVE BEHAVIOR; BLOOD SAMPLING; CASTRATED MALE; CASTRATION; COMPARATIVE STUDY; CONFERENCE PAPER; CONTROLLED STUDY; EIGHT ARM RADIAL ARM MAZE; ERROR; LEARNING; LONG TERM MEMORY; MALE; MAZE TEST; MENTAL PERFORMANCE; MORRIS WATER MAZE; NONHUMAN; PHYSIOLOGY; RADIOIMMUNOASSAY; RAT; REFERENCE MEMORY; SPATIAL MEMORY; WORKING MEMORY;

ANIMALS; APPETITIVE BEHAVIOR; APTITUDE; ESCAPE REACTION; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; ORCHIECTOMY; ORIENTATION; RATS; RATS, SPRAGUE-DAWLEY; RETENTION (PSYCHOLOGY); TESTOSTERONE;

EID: 38349180463     PISSN: 00040002     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10508-007-9264-2     Document Type: Conference Paper

References (76)

1. Astur, R. S., Ortiz, M. L., & Sutherland, R. J. (1998). A characterization of performance by men and women in a virtual Morris water task: A large and reliable sex difference. Behavioral Brain Research, 93, 185-190.
2. Baldi, E., Efoudebe, M., Lorenzini, C. A., & Bucherelli, C. (2005). Spatial navigation in the Morris water maze: Working and long lasting reference memories. Neuroscience Letters, 378, 176-180.
3. Bimonte-Nelson, H. A., Singleton, R. S., Nelson, M. E., Eckman, C. B., Barber, J., Scott, T. Y., et al. (2003). Testosterone, but not nonarmoatizable dihydrotestosterone, improves working memory and alters nerve growth factor levels in aged male rats. Experimental Neurology, 181, 301-312.
4. Cherrier, M. M., Asthana, S., Plymate, S., Baker, L., Matsumoto, A. M., Peskind, E., et al. (2001). Testosterone supplementation improves spatial and verbal memory in healthy older men. Neurology, 57, 80-88.
5. Choi, J., & Silverman, I. (2002). The relationship between testosterone and route-learning strategies in humans. Brain and Cognition, 50, 116-120.
6. Christiansen, K., & Knussmann, R. (1987). Sex hormones and cognitive functioning in men. Neuropsychobiology, 18, 27-37.
7. Chung, B., & Hu, M.-C. (2002). Androgen biosynthesis and degradation. In C. Chang, & G. Wipple (Eds.), Androgens and andogen receptor: Mechanisms, functions, and clinical applications (pp. 1-15). Boston, MA: Kluwer.
8. Collins, D. W., & Kimura, D. (1997). A large sex difference on a two-dimensional mental rotation task. Behavioral Neuroscience, 111, 845-849.
9. Dabbs, J. M., Chang, E., & Strong, R. A. (1998). Spatial ability, navigation strategy, and geographic knowledge among men and women. Evolution and Human Behavior, 19, 89-98.
10. Daniel, J. M., Winsauer, P. J., & Moerschbaecher, J. M. (2003). Castration in rats impairs performance during acquisition of working memory task and exacerbates deficits in working memory produced by scopolamine and mecamylamine. Psychoneuroendocrinology, 170, 294-300.
11. de Bruin, J. P. C., Swinkels, W. A. M., & de Barbander, J. M. (1997). Response learning of rats in Morris water maze: Involvement of the medial prefrontal cortex. Behavioral Brain Research, 85, 47-55.
12. Driscoll, I., Hamilton, D. A., Yeo, R. A., Brooks, W. M., & Sutherland, R. J. (2005). Virtual navigation in humans: The impact of age, sex, and hormones on place learning. Hormones and Behavior, 47, 326-335.
13. Duff, S. D., & Hampson, E. (2001). A sex difference on a novel spatial working memory task in humans. Brain and Cognition, 47, 470-493.
14. Eichenbaum, H., Stewart, C., & Morris, R. G. M. (1990). Hippocampal representation in place learning. Journal of Neuroscience, 10, 3531-3542.
15. Galea, L. A. M., Kavaliers, M., & Ossenkopp, K.-P. (1996). Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. Journal of Experimental Biology, 199, 195-200.
16. Galea, L. A. M., & Kimura, D. (1993). Sex differences in route-learning. Personality and Individual Differences, 14, 53-65.
17. Gaulin, S. J. C., & FitzGerald, R. W. (1986). Sex differences in spatial ability: An evolutionary hypothesis and test. The American Naturalist, 127, 74-88.
18. Gibbs, R. B. (2005). Testosterone and estradiol produce different effects on cognitive performance in male rats. Hormones and Behavior, 48, 268-277.
19. Gouchie, C., & Kimura, D. (1991). The relationship between testosterone levels and cognitive ability patterns. Psychoneuroendocrinology, 16, 323-334.
20. Goudsmit, E., Van De Poll, N. E., & Swaab, D. F. (1990). Testosterone fails to reverse spatial memory decline in aged rats and impairs retention in young and middle-aged animals. Behavioral and Neural Biology, 53, 6-20.
21. Gresack, J. E., & Frick, K. M. (2003). Male mice exhibit better spatial working and reference memory than females in a water-escape radial arm maze task. Brain Research, 982, 98-107.
22. Gupta, D., Rager, K., Zarzycki, J., & Eichner, M. (1975). Levels of luteinizing hormones, follicle stimulating hormone, testosterone and dihydrotestosterone in the circulation of sexually maturing intact male rats and after orchidectomy and experimental bilateral cryptoorchidism. Journal of Endocrinology, 66, 183-193.
23. Hampson, E. (1990). Estrogen-related variations in human spatial and articulatory-motor skills. Psychoneuroendocrinology, 15, 97-111.
24. Hampson, E. (2000). Sexual differentiation of spatial functions in humans. In A. Matsumoto (Ed.), Sexual differentiation of the brain (pp. 279-300). Boca Raton, FL: CRC Press.
25. Harley, C. W., Malsbury, C. W., Squires, A., & Brown, R. A. M. (2000). Testosterone decreases CA1 plasticity in vivo in gonadectomized male rats. Hippocampus, 10, 693-697.
26. Hines, M., Fane, B. A., Pasterski, V. L., Mathews, G. A., Conway, G. S., & Brook, C. (2003). Spatial abilities following prenatal androgen abnormality: Targeting and mental rotations performance in individuals with congenital adrenal hyperplasia. Psychoneuroendocrinology, 28, 1010-1026.
27. Hodges, H. (1996). Maze procedures: The radial-arm and water maze compared. Cognitive Brain Research, 3, 167-181.
28. Holding, C. S., & Holding, D. H. (1988). Acquisition of route network knowledge by males and females. Journal of General Psychology, 116, 29-41.
29. Holmes, M. M., Wide, J. K., & Galea, L. A. M. (2002). Low levels of estradiol facilitate, whereas high levels of estradiol impair, working memory performance on the radial arm maze. Behavioral Neuroscience, 116, 928-934.
30. Hooven, C. K., Chabris, C. F., Ellison, P. T., & Kosslyn, S. M. (2004). The relationship of male testosterone to components of mental rotation. Neuropsychologia, 43, 782-790.
31. Isgor, C., & Sengelaub, D. R. (1998). Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats. Hormones and Behavior, 34, 183-198.
32. Janowky, J. S., Oviatt, S. K., & Orwoll, E. S. (1994). Testosterone influences spatial cognition in older men. Behavioral Neuroscience, 108, 325-332.
33. Jonasson, Z. (2005). Meta-analysis of sex differences in rodent models of learning and memory: A review of behavioral and biological data. Neuroscience and Biobehavioral Reviews, 28, 811-825.
34. Jones, B. A., & Watson, N. V. (2005). Spatial memory performance in androgen insensitive male rats. Physiology and Behavior, 85, 135-141.
35. Kerr, J. E., Allore, R. J., Beck, S. G., & Handa, R. J. (1995). Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology, 136, 3213-3221.
36. Kesner, R. P., Hunt, M. E., Williams, J. M., & Long, J. M. (1996). Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cerebral Cortex, 6, 311-318.
37. Khalil, R., King, M. A., & Soliman, M. R. I. (2005). Testosterone reverses ethanol-induced deficit in spatial reference memory in castrated rats. Pharmacology, 75, 87-92.
38. Kritzer, M. (2004). The distribution of immunoreactivity for intracellular androgen receptors in the cerebral cortex of hormonally intact adult male and female rats: Localization in pyramidal neurons making corticocortical connections. Cerebral Cortex, 14, 268-280.
39. Kritzer, M. F., McLaughlin, P. J., & Smirlis, T. (2001). Gonadectomy impairs T-maze acquisition in adult male rats. Hormones and Behavior, 39, 167-174.
40. Lee, I., & Kesner, R. P. (2003). Time-dependent relationship between dorsal hippocampus and the prefrontal cortex in spatial memory. Journal of Neuroscience, 223, 1517-1523.
41. Leranth, C., Petnehazy, O., & MacLusky, N. J. (2003). Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. Journal of Neuroscience, 23, 1588-1592.
42. Linn, M. C., & Petersen, A. C. (1985). Emergence and characterization of sex differences in spatial ability: A meta-analysis. Child Development, 56, 1479-1498.
43. Luine, V. N., Richards, S. T., Wu, V. Y., & Beck, K. D. (1998). Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Hormones and Behavior, 34, 149-162.
44. Luine, V., & Rodriguez, M. (1994). Effects of estradiol on radial arm maze performance of young and aged rats. Behavioral and Neural Biology, 62, 230-236.
45. Martin, S., Jones, M., Simpson, E., & van den Buuse, M. (2003). Impaired spatial reference memory in aromatse-deficient (ArKO) mice. Neuroreport, 14, 1979-1982.
46. McKeever, W. F., & Deyo, R. A. (1990). Testosterone, dihydrotestosterone, and spatial task performance of males. Bulletin of the Psychonomic Society, 28, 305-308.
47. McKeever, W. F., Rich, D. A., Deyo, R. A., & Conner, R. L. (1987). Androgens and spatial ability: Failure to find a relationship between testosterone and ability measures. Bulletin of the Psychonomic Society, 25, 438-440.
48. Moffat, S. D., & Hampson, E. (1996). A curvilinear relationship between testosterone and spatial cognition in humans: Possible influence of hand preference. Psychoneuroendocrinology, 21, 323-337.
49. Moffat, S. D., Hampson, E., & Hatzipantelis, M. (1998). Navigation in a "virtual" maze: Sex differences and correlation with psychometric measures of spatial ability in humans. Evolution and Human Behavior, 19, 73-87.
50. Naghdi, N., Majlessi, N., & Bozorgmehr, T. (2005). The effect of intrahippocampal injection of testosterone enanthate (an androgen receptor agonist) and anisomycin (protein synthesis inhibitor) on spatial learning and memory in adult male rats. Behavioral Brain Research, 156, 263-268.
51. Naghdi, N., Nafisy, N., & Majlessi, N. (2001). The effects of intrahippocampal testosterone and flutamide on spatial localization in the Morris water maze. Brain Research, 897, 44-51.
52. Neave, N., Menaged, M., & Weightman, D. R. (1999). Sex differences in cognition: The role of testosterone and sexual orientation. Brain and Cognition, 41, 245-262.
53. Nyborg, H. (1983). Spatial ability in men and women: Review and new theory. Advances in Behavior Research and Theory, 5, 89-140.
54. Olton, D. S., & Papas, B. C. (1979). Spatial memory and hippocampal function. Neuropsychologia, 17, 669-682.
55. Packard, M. G., Kohlmaier, J. R., & Alexander, G. M. (1996). Posttraining intrahippocampal estradiol injections enhance spatial memory in male rats: Interaction with cholinergic systems. Behavioral Neuroscience, 110, 626-632.
56. Parsons, T. D., Larson, P., Kratz, K., Thiebaux, M., Bluestein, B., Buckwalter, J. G., et al. (2004). Sex differences in mental rotation and spatial rotation in a virtual environment. Neuropsychologia, 42, 555-562.
57. Perrot-Sinal, T. S., Kostenuik, M. A., Ossenkopp, K.-P., & Kavaliers, M. (1996). Sex differences in performance in the Morris water maze and the effect of initial nonstationary hidden platform training. Behavioral Neuroscience, 110, 1309-1320.
58. Postma, A., Jager, G., Kessels, R. P. C., Koppeschaar, H. P. F., & van Honk, J. (2004). Sex differences for selective forms of spatial memory. Brain and Cognition, 54, 24-34.
59. Postma, A., Winkel, J., Tuiten, A., & van Honk, J. (1999). Sex differences and menstrual cycle effects in human spatial ability. Psychoneuroendocrinology, 24, 175-192.
60. Pothuizen, H. H., Zhang, W.-N., Jongen-Rêlo, A. L., Feldon, J., & Yee, B. K. (2004). Dissociation of function between the dorsal and the ventral hippocampus in spatial learning abilities of the rat: A within-subject, within-task comparison of reference and working memory. European Journal of Neuroscience, 19, 705-712.
61. Roof, R. L. (1993). Neonatal exogenous testosterone modifies sex difference in radial arm and Morris water maze performance in prepubescent and adult rats. Behavioural Brain Research, 53, 1-10.
62. Roof, R. L., & Havens, M. D. (1992). Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Research, 572, 310-313.
63. Sandstrom, N. J., Kim, J. H., & Wasserman, M. A. (2005). Testosterone modulates performance on spatial working memory task in male rats. Hormones and Behavior, 50, 18-26.
64. Seamans, J. K., Floresco, S. B., & Phillips, A. G. (1995). Functional differences between the prelimbic and anterior cingulated regions of the rat prefrontal cortex. Behavioral Neuroscience, 109, 1063-1073.
65. Seamans, J. K., & Phillips, A. G. (1994). Selective memory impairments produced by transient lidocaine-induced lesions of the nucleus acumens in rats. Behavioral Neuroscience, 108, 456-468.
66. Seymore, P., Dou, H., & Juraska, J. M. (1996). Sex differences in radial maze performance: Influence of rearing environment and room cues. Psychobiology, 24, 33-37.
67. Silverman, I., & Eals, M. (1992). Sex difference n spatial abilities: Evolutionary theory and data. In J. Barkow, L. Cosmides, & J. Tooby (Eds.), The adapted mind: Evolutionary psychology and the generation of culture (pp. 533-549). Oxford, UK: Oxford University Press.
68. Silverman, I., Kastuk, D., Choi, J., & Phillips, K. (1999). Testosterone levels and spatial ability in men. Psychoneuroendocrinology, 24, 813-822.
69. Smith, M. D., Jones, L. S., & Wilson, M. A. (2002). Sex differences in hippocampal slice excitability: Role of testosterone. Neuroscience, 109, 517-530.
70. Spritzer, M. D., & Galea, L. A. M. (2007). Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Developmental Neurobiology, 67, 1321-1333.
71. Stefani, M. R., & Moghaddam, B. (2005). Systemic and prefrontal cortical NMDA receptor blockade differentially affect discrimination learning and set-shift ability in rats. Behavioral Neuroscience, 119, 420-428.
72. van Haaren, R., van Hiest, A., & Heinsbroek, R. P. W. (1990). Behavioral differences between male and female rats: Effects of gonadal hormones on learning and memory. Neuroscience and Biobehavioral Reviews, 14, 23-33.
73. van Hest, A., van Haaren, F., & van de Poll, N. E. (1989). Perseverative responding in male and female Wistar rats: Effects of gonadal hormones. Hormones and Behavior, 23, 57-67.
74. Voyer, D., Voyer, S., & Bryden, M. P. (1995). Magnitude of sex differences in spatial abilities: A meta-analysis and consideration of critical variables. Psychological Bulletin, 117, 250-270.
75. Wang, C., Leung, A., & Sinha-Hikim, A. P. (1993). Reproductive aging in the male brown-Norway rat: A model for the human. Endocrinology, 133, 2773-2781.
76. Williams, C. L., Barnett, A. M., & Meck, W. H. (1990). Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behavioral Neuroscience, 104, 84-97.