The effects of biological sex and gonadal hormones on learning strategy in adult rats

Physiology and Behavior

Volumn 105, Issue 4, 2012, Pages 1014-1020

  Hawley, Wayne R ^a   Grissom, Elin M ^a   Barratt, Harriet E ^b   Conrad, Taylor S ^a   Dohanich, Gary P ^a,b  

^a Tulane University   (United States)

^b TULANE UNIVERSITY   (United States)

Author keywords

Estrous cycle; Learning strategy; Sex differences; Testosterone

Indexed keywords

SEX HORMONE; TESTIS PEPTIDE HORMONE;

ACCURACY; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DECISION MAKING; ESTRUS CYCLE; FEMALE; HIPPOCAMPUS; LATENT PERIOD; LEARNING STYLE; MALE; NONHUMAN; ORCHIECTOMY; PLACE PREFERENCE; PRIORITY JOURNAL; PROESTRUS; RAT; SEX DIFFERENCE;

ANIMALS; CHOICE BEHAVIOR; ESTROUS CYCLE; FEMALE; GONADAL HORMONES; MALE; MAZE LEARNING; ORCHIECTOMY; RATS; RATS, LONG-EVANS; SEX CHARACTERISTICS; SPATIAL BEHAVIOR;

EID: 83455260389     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2011.11.021     Document Type: Article

References (96)

1. Packard M., Hirsh R., White N. Differential effects of fornix and caudate nucleus lesions on two radial arm maze tasks: evidence for multiple memory systems. J Neurosci 1989, 9:1465-1472.
2. McDonald R., White N. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci 1993, 107:3-22.
3. Packard M., McGaugh J. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place response learning. Neurobiol Learn Mem 1996, 65:65-72.
4. White N., McDonald R. Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 2002, 77:125-184.
5. Compton D. Behavior strategy learning in the rat: effects of lesions of the dorsal striatum or dorsal hippocampus. Behav Processes 2004, 67:335-342.
6. Kesner R., Rogers J. An analysis of independence and interactions of brain substrates that subserve multiple attributes, memory systems, and underlying processes. Neurobiol Learn Mem 2004, 82:199-215.
7. Gold P. Coordination of multiple memory systems. Neurobiol Learn Mem 2004, 82:230-242.
8. Squire L. Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 2004, 82:171-177.
9. Lee A., Duman R., Pittenger C. A double dissociation revealing bidirectional competition between striatum and hippocampus during learning. Proc Natl Acad Sci 2008, 105:17163-17168.
10. McDonald R., White N. Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol 1994, 61:260-270.
11. Devan B., White N. Parallel information processing in the dorsal striatum: relation to hippocampal function. J Neurosci 1999, 19:2789-2798.
12. Packard M. Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. Proc Natl Acad Sci 1999, 96:12881-12886.
13. Cahill J., Baxter M. Cholinergic and noncholinergic septal neurons modulate strategy selection in spatial learning. Eur J Neurosci 2001, 14:1856-1864.
14. Chang Q., Gold P. Switching memory systems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. J Neurosci 2003, 23:3001-3005.
15. Lex B., Sommer S., Hauber W. The role of dopamine in the dorsomedial striatum in place and response learning. Neuroscience 2011, 172:212-218.
16. Kim J., Lee H., Han J., Packard M. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 2001, 21:5222-5228.
17. Packard M., Wingard J. Amygdala and "emotional" modulation of the relative use of multiple memory systems. Neurobiol Learn Mem 2004, 82:243-252.
18. Elliott A., Packard M. Intra-amygdala anxiogenic drug infusion prior to retrieval biases rats towards the use of habit memory. Neurobiol Learn Mem 2008, 90:616-623.
19. Schwabe L., Dalm S., Schachinger H., Oitzl M. Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and men. Neurobiol Learn Mem 2008, 90:495-503.
20. Sadowski R., Jackson G., Wieczorek L., Gold P. Effects of stress, corticosterone, and epinephrine administration on learning in place and response tasks. Behav Brain Res 2009, 205:19-25.
21. Schwabe L., Schachinger H., de Kloet E., Oitzl M. Stress impairs spatial but not early stimulus-response learning. Behav Brain Res 2010, 213:50-55.
22. Hawley W., Grissom E., Dohanich G. The relationships between trait anxiety, place recognition memory, and learning strategy. Behav Brain Res 2011, 216:525-530.
23. McIntyre C., Marriott L., Gold P. Patterns of brain acetylcholine release predict individual differences in preferred learning strategies in rats. Neurobiol Learn Mem 2003, 79:177-183.
24. Gastambide F., Viollet C., Lepousez G., Epelbaum J., Guillou J. Hippocampal SSTR4 somatostatin receptors control the selection of memory strategies. Psychopharmacology (Berl) 2009, 202:153-163.
25. Colombo P., Brightwell J., Countryman R. Cognitive strategy-specific increases in phosphorylated cAMP response element-binding protein and c-Fos in the hippocampus and dorsal striatum. J Neurosci 2003, 23:3547-3554.
26. Brightwell J., Smith C., Neve R., Colombo P. Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learn Mem 2007, 14:195-199.
27. Martel G., Blanchard J., Mons N., Gastambide F., Micheau J., Guillou J. Dynamic interplays between memory systems depend on practice: the hippocampus is not always the first to provide solution. Neuroscience 2007, 150:743-753.
28. Brightwell J., Smith C., Neve R., Colombo P. Transfection of mutant CREB in the striatum, but not the hippocampus, impairs long-term memory for response learning. Neurobiol Learn Mem 2008, 89:27-35.
29. Sung J., Goo J., Lee D., Jin D., Bizon J., Gallagher M., et al. Learning strategy selection in the water maze and hippocampal CREB phosphorylation differ in two inbred strains of mice. Learn Mem 2008, 15:183-188.
30. Hagewoud R., Havekes R., Tiba P., Novati A., Hogenelst K., Weinreder P., et al. Coping with sleep deprivation: shifts in regional brain activity and learning strategy. Sleep 2010, 33:1465-1473.
31. Passino E., Middei S., Restivo L., Bertaina-Anglade V., Ammassari-Teule M. Genetic approach to variability of memory systems: analysis of place vs. response learning and fos-related expression in hippocampal and striatal areas of C57BL/6 and DBA/2 mice. Hippocampus 2002, 12:63-75.
32. Teather L., Packard M., Smith D., Ellis-Behnke R., Bazan N. Differential induction of c-Jun and Fos-like proteins in rat hippocampus and dorsal striatum after training in two water maze tasks. Neurobiol Learn Mem 2005, 84:75-84.
33. Pittenger C., Fassano S., Mazzocchi-Jones D., Dunnett S., Kandel E., Brambilla R. Impaired bidirectional synaptic plasticity and procedural memory formation in striatum-specific cAMP response element-binding protein-deficient mice. J Neurosci 2006, 26:2808-2813.
34. Clements K., Saunders A., Robertson B., Wainwright P. Spontaneously hypertensive, Wistar Kyoto and Sprague-Dawley rats differ in their use of place and response strategies in the water radial arm maze. Neurobiol Learn Mem 2007, 87:285-294.
35. Gill K., Bernstein I., Mizumori S. Immediate early gene activation in hippocampus and dorsal striatum: effects of explicit place and response training. Neurobiol Learn Mem 2007, 87:583-596.
36. Espina-Marchant P., Pinto-Hamuy T., Bustamante D., Morales P., Herrera-Marschitz M. Rat strain influences the use of egocentric learning strategies mediated by neostriatum. Exp Brain Res 2009, 193:205-212.
37. Wells A., Janes A., Liu X., Deschepper C., Kaufman M., Kantak K. Medial temporal lobe functioning and structure in the spontaneously hypertensive rat: comparison with Wistar-Kyoto normotensive and Wistar-Kyoto hypertensive strains. Hippocampus 2010, 20:787-797.
38. Korol D. Role of estrogen in balancing contributions from multiple memory systems. Neurobiol Learn Mem 2004, 82:309-323.
39. Korol D., Kolo L. Estrogen-induced changes in place and response learning in young adult female rats. Behav Neurosci 2002, 116:411-420.
40. Korol D., Malin E., Borden K., Busby R., Couper-Leo J. Shifts in preferred learning strategy across the estrous cycle in female rats. Horm Behav 2004, 45:330-338.
41. Davis D., Jacobson T., Aliakbari S., Mizumori S. Differential effects of estrogen on hippocampal- and striatal-dependent learning. Neurobiol Learn Mem 2005, 84:132-137.
42. McElroy M., Korol D. Intrahippocampal muscimol shifts learning strategy in gonadally intact young adult female rats. Learn Mem 2005, 12:150-158.
43. Quinlan M., Hussain D., Brake W. Use of cognitive strategies in rats: the role of estradiol and its interaction with dopamine. Horm Behav 2008, 53:185-191.
44. Zurkovsky L., Brown S., Korol D. Estrogen modulates place learning through estrogen receptors in the hippocampus. Neurobiol Learn Mem 2006, 86:336-343.
45. Zurkovsky L., Brown S., Boyd S., Fell J., Korol D. Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscience 2007, 144:26-37.
46. Daniel J., Lee C. Estrogen replacement in ovariectomized rats affects strategy selection in the Morris water maze. Neurobiol Learn Mem 2004, 82:142-149.
47. Pleil K., Glenn M., Williams C. Estradiol alters Fos-immunoreactivity in the hippocampus and dorsal striatum during place and response learning in middle-aged but not young adult female rats. Endocrinology 2011, 152:946-956.
48. Tunur T., Dohanich G., Schrader L. Pre-exposure to context affects learning strategy selection in mice. Learn Mem 2010, 17:328-331.
49. Pleil K., Williams C. The development and stability of estrogen-modulated spatial navigation strategies in female rats. Horm Behav 2010, 57:360-367.
50. Kanit L., Taskiran D., Furedy J., Kulali B., McDonald R., Pogun S. Nicotine interacts with sex in affecting rat choice between "look-out" and "navigational" cognitive styles in the Morris water maze place learning task. Brain Res Bull 1998, 46:441-445.
51. Lehmann J., Pryce C., Bettschen D., Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav 1999, 64:705-715.
52. Kanit L., Yilmaz O., Taskiran D., Kulali B., Furedy J., Demirgoren S., et al. Sexually dimorphic cognitive style, female sex hormones, and cortical nitric oxide. Physiol Behav 2000, 71:277-287.
53. Kanit L., Taskiran D., Yilmaz O., Balkan B., Demirgoren S., Furedy J., et al. Sexually dimorphic cognitive style in rats emerges after puberty. Brain Res Bull 2000, 52:243-248.
54. Jonasson Z., Cahill J., Tobey R., Baxter M. Sexually dimorphic effects of hippocampal cholinergic deafferentation in rats. Eur J Neurosci 2004, 20:3041-3053.
55. Blokland A., Rutten K., Prickaerts J. Analysis of spatial orientation strategies of male and female Wistar rats in a Morris water escape task. Behav Brain Res 2006, 171:216-224.
56. Schmidt B., Jacobson T., Markus E. Hippocampal and striatal dependent navigation: sex difference are limited to acquisition. Horm Behav 2009, 56:199-205.
57. 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.
58. 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.).
59. Luine V., Rodriguez M. Effects of estradiol on radial arm maze performance of young and aged rats. Behav Neural Biol 1994, 62:230-236.
60. Markowska A. Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J Neurosci 1999, 19:8122-8133.
61. Beck K., Luine V. Sex differences in behavioral and neurochemical profiles after chronic stress: role of housing conditions. Physiol Behav 2000, 75:661-673.
62. 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.).
63. Harrell L., Goyal M., Parsons D., Peagler A. The effect of gonadal steroids on the behavioral and biochemical effects of hippocampal sympathetic ingrowth. Physiol Behav 1990, 48:507-513.
64. Daniel J., Winsauer P., Moerschbaecher J. 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.
65. Edinger K., Lee B., Frye C. Mnemonic effects of testosterone and its 5alpha-reduced metabolites in the conditioned fear and inhibitory avoidance tasks. Pharmacol Biochem Behav 2004, 78:559-568.
66. Gibbs R. Testosterone and estradiol produce different effects on cognitive performance in male rats. Horm Behav 2005, 48:268-277.
67. Sandstrom N., Kim J., Wasserman M. Testosterone modulates performance on a spatial working memory task in male rats. Horm Behav 2006, 50:18-26.
68. Gibbs R., Johnson D. Sex-specific effects of gonadectomy and hormone treatment on acquisition of a 12-arm radial maze task by Sprague Dawley rats. Endocrinology 2008, 149:3176-3183.
69. Spritzer M., Gill M., Weinberg A., Galea L. Castration differentially affects spatial working and reference memory in male rats. Arch Sex Behav 2008, 37:19-29.
70. Benice T., Raber J. Dihydrotestosterone modulates spatial working-memory performance in male mice. J Neurochem 2009, 110:902-911.
71. Hasegawa N., Mochizuki M. Improved effect of Pycnogenol on impaired spatial memory function in partial androgen deficiency rat model. Phytother Res 2009, 23:840-843.
72. Spritzer M., Daviau E., Coneeny N., Engelman S., Prince W., Rodriguez-Wisdom K. Effects of testosterone on spatial learning and memory in adult male rats. Horm Behav 2011, 59:484-496.
73. Gibbs R. Estradiol enhances DMP acquisition via a mechanism not mediated by turning strategy but which requires intact basal forebrain cholinergic projections. Horm Behav 2007, 52:352-359.
74. Menard C., Dohanich G. Scopolamine inhibition of lordosis in naturally cycling female rats. Physiol Behav 1989, 45:819-823.
75. Williams C., Barnett A., Meck W. Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 1990, 104:84-97.
76. Dawson J., Cheung Y., Lau R. Developmental effects of neonatal sex hormones on spatial and activity skills in the white rat. Biol Psychol 1975, 3:213-229.
77. Roof R. Neonatal exogenous testosterone modifies sex difference in radial and Morris water maze performance in prepubescent and adult rats. Behav Brain Res 1993, 53:1-10.
78. Isgor C., Sengelaub D. Prenatal gonadal steroids affect adult spatial behavior, CA1 and CA3 pyramidal cell morphology in rats. Horm Behav 1998, 34:183-198.
79. Isgor C., Sengelaub D. Effects of neonatal gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats. J Neurobiol 2003, 55:179-190.
80. Roof R. The dentate gyrus is sexually dimorphic in prepubescent rats: testosterone plays a significant role. Brain Res 1993, 610:148-151.
81. Mitsushima D., Takase K., Funabashi T., Kimura F. Gonadal steroids maintain 24 h acetylcholine release in the hippocampus: organizational and activational effects in behaving rats. J Neurosci 2009, 29:3808-3815.
82. Rummel J., Epp J., Galea L. Estradiol does not influence strategy choice but place strategy choice is associated with increased cell proliferation in the hippocampus of female rats. Horm Behav 2010, 58:582-590.
83. Ferragud A., Haro A., Sylvain A., Velazquez-Sanchez C., Hernandez-Rabaza V., Canales J. Enhanced habit-based learning and decreased neurogenesis in the adult hippocampus in a murine model of chronic social stress. Behav Brain Res 2010, 210:134-139.
84. Fitz N., Gibbs R., Johnson D. Aversive stimulus attenuates impairment of acquisition in a delayed match to position T-maze task caused by a selective lesion of septo-hippocampal cholinergic projections. Brain Res Bull 2006, 69:660-665.
85. Fitz N., Gibbs R., Johnson D. Selective lesion of septal cholinergic neurons in rats impairs acquisition of a delayed matching to position T-maze task by delaying the shift from a response to a place strategy. Brain Res Bull 2008, 77:356-360.
86. Romeo R., Staub B., Jasnow A., Karatsoreos I., Thornton J., McEwen B. 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.
87. Nakamura N., Fujita H., Kawata M. Effects of gonadectomy on immunoreactivity for choline acetyltransferase in the cortex, hippocampus, and basal forebrain of adult male rats. Neuroscience 2002, 109:473-485.
88. Nguyen T., Yao M., Pike C. Androgens activate mitogen-activated protein kinase signaling: role in neuroprotection. J Neurochem 2005, 94:1639-1651.
89. Nguyen T., Yao M., Pike C. Dihydrotestosterone activates CREB signaling in cultured hippocampal neurons. Brain Res 2009, 1298:1-12.
90. Lewis C., McEwen B., Frankfurt M. Estrogen-induction of dendritic spines in ventromedial hypothalamus and hippocampus: effects of neonatal aromatase blockade and adult GDX. Dev Brain Res 1995, 87:91-95.
91. Leranth C., Petnehazy O., MacLusky N. Gonadal hormones affect spine synaptic density in the CA1 hippocampal subfield of male rats. J Neurosci 2003, 23:1588-1592.
92. Hatanaka Y., Mukai H., Mitsuhashi K., Hojo Y., Murakami G., Komatsuzaki Y., et al. Androgen rapidly increases dendritic thorns of CA3 neurons in male rat hippocampus. Biochem Biophys Res Commun 2009, 381:728-732.
93. Spritzer M., Galea L. Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats. Dev Neurobiol 2007, 67:1321-1333.
94. Benice T., 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.
95. Spritzer M., Ibler E., Inglis W., Curtis M. Testosterone and social isolation influence adult neurogenesis in the dentate gyrus of male rats. Neuroscience 2011, 195:180-190.
96. Smith M., Jones L., Wilson M. Sex differences in hippocampal slice excitability: role of testosterone. Neuroscience 2002, 109:517-530.