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. 1999 Nov 22;266(1435):2303–2308. doi: 10.1098/rspb.1999.0923

Spatial working memory in rats: no differences between the sexes.

S D Healy 1, S R Braham 1, V A Braithwaite 1
PMCID: PMC1690445  PMID: 10629980

Abstract

In a number of mammalian species, males appear to have superior spatial abilities to females. The favoured explanations for this cognitive difference are hormonal, with higher testosterone levels in males than females leading to better spatial performance, and evolutionary, where sexual selection has favoured males with increased spatial abilities for either better navigational skills in hunting or to enable an increased territory size. However, an alternative explanation for this sex difference focuses on the role of varying levels of oestrogen in females in spatial cognition (the 'fertility and parental care' hypothesis). One possibility is that varying oestrogen levels result in variation in spatial learning and memory so that, when tested across the oestrous cycle, females perform as well as males on days of low oestrogen but more poorly on days of high oestrogen. If day in the oestrous cycle is not taken into account then, across an experiment, any sex differences found would always produce male superiority. We used a spatial working memory task in a Morris water maze to test the spatial learning and memory abilities of male and female rats. The rats were tested across a number of consecutive days during which the females went through four oestrous cycles. We found no overall sex differences in latencies to reach a submerged platform in a Morris water maze but, on the day of oestrus (low oestrogen), females took an extra swim to learn the platform's location (a 100% increase over the other days in the cycle). Female swim speed also varied across the oestrous cycle but females were no less active on the day of oestrus. These results oppose the predictions of the fertility and parental care hypothesis.

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Selected References

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  1. Bannerman D. M., Good M. A., Butcher S. P., Ramsay M., Morris R. G. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature. 1995 Nov 9;378(6553):182–186. doi: 10.1038/378182a0. [DOI] [PubMed] [Google Scholar]
  2. Berry B., McMahan R., Gallagher M. Spatial learning and memory at defined points of the estrous cycle: effects on performance of a hippocampal-dependent task. Behav Neurosci. 1997 Apr;111(2):267–274. doi: 10.1037//0735-7044.111.2.267. [DOI] [PubMed] [Google Scholar]
  3. Birke L. I. Object Investigation by the oestrous rat and guinea-pig: the oestrous cycle and the effects of oestrogen and progesterone. Anim Behav. 1979 May;27(Pt 2):350–358. doi: 10.1016/0003-3472(79)90168-4. [DOI] [PubMed] [Google Scholar]
  4. Bucci D. J., Chiba A. A., Gallagher M. Spatial learning in male and female Long-Evans rats. Behav Neurosci. 1995 Feb;109(1):180–183. doi: 10.1037//0735-7044.109.1.180. [DOI] [PubMed] [Google Scholar]
  5. 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 Dec;32(3):217–225. doi: 10.1006/hbeh.1997.1433. [DOI] [PubMed] [Google Scholar]
  6. Finger F. W. Estrus and general activity in the rat. J Comp Physiol Psychol. 1969 Jul;68(3):461–466. doi: 10.1037/h0027490. [DOI] [PubMed] [Google Scholar]
  7. Frye C. A. Estrus-associated decrements in a water maze task are limited to acquisition. Physiol Behav. 1995 Jan;57(1):5–14. doi: 10.1016/0031-9384(94)00197-d. [DOI] [PubMed] [Google Scholar]
  8. Galea L. A., Kavaliers M., Ossenkopp K. P., Hampson E. Gonadal hormone levels and spatial learning performance in the Morris water maze in male and female meadow voles, Microtus pennsylvanicus. Horm Behav. 1995 Mar;29(1):106–125. doi: 10.1006/hbeh.1995.1008. [DOI] [PubMed] [Google Scholar]
  9. Galea L. A., Kavaliers M., Ossenkopp K. P. Sexually dimorphic spatial learning in meadow voles Microtus pennsylvanicus and deer mice Peromyscus maniculatus. J Exp Biol. 1996 Jan;199(Pt 1):195–200. doi: 10.1242/jeb.199.1.195. [DOI] [PubMed] [Google Scholar]
  10. Galea L. A., Saksida L., Kavaliers M., Ossenkopp K. P. Naloxone facilitates spatial learning in a water-maze task in female, but not male, adult nonbreeding meadow voles. Pharmacol Biochem Behav. 1994 Feb;47(2):265–271. doi: 10.1016/0091-3057(94)90009-4. [DOI] [PubMed] [Google Scholar]
  11. Gould E., Woolley C. S., Frankfurt M., McEwen B. S. Gonadal steroids regulate dendritic spine density in hippocampal pyramidal cells in adulthood. J Neurosci. 1990 Apr;10(4):1286–1291. doi: 10.1523/JNEUROSCI.10-04-01286.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gray J. A., Buffery A. W. Sex differences in emotional and cognitive behaviour in mammals including man: adaptive and neural bases. Acta Psychol (Amst) 1971 Mar;35(2):89–111. doi: 10.1016/0001-6918(71)90014-x. [DOI] [PubMed] [Google Scholar]
  13. Grimshaw G. M., Sitarenios G., Finegan J. A. Mental rotation at 7 years: relations with prenatal testosterone levels and spatial play experiences. Brain Cogn. 1995 Oct;29(1):85–100. doi: 10.1006/brcg.1995.1269. [DOI] [PubMed] [Google Scholar]
  14. Jacobs L. F., Gaulin S. J., Sherry D. F., Hoffman G. E. Evolution of spatial cognition: sex-specific patterns of spatial behavior predict hippocampal size. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6349–6352. doi: 10.1073/pnas.87.16.6349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kolakowski D., Malina R. M. Spatial ability, throwing accuracy and man's hunting heritage. Nature. 1974 Oct 4;251(5474):410–412. doi: 10.1038/251410a0. [DOI] [PubMed] [Google Scholar]
  16. Luine V. N., Richards S. T., Wu V. Y., Beck K. D. Estradiol enhances learning and memory in a spatial memory task and effects levels of monoaminergic neurotransmitters. Horm Behav. 1998 Oct;34(2):149–162. doi: 10.1006/hbeh.1998.1473. [DOI] [PubMed] [Google Scholar]
  17. Morris R. G., Garrud P., Rawlins J. N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 1982 Jun 24;297(5868):681–683. doi: 10.1038/297681a0. [DOI] [PubMed] [Google Scholar]
  18. Perrot-Sinal T. S., Heale V. R., Ossenkopp K. P., Kavaliers M. Sexually dimorphic aspects of spontaneous activity in meadow voles (Microtus pennsylvanicus): effects of exposure to fox odor. Behav Neurosci. 1996 Oct;110(5):1126–1132. doi: 10.1037//0735-7044.110.5.1126. [DOI] [PubMed] [Google Scholar]
  19. Perrot-Sinal T. S., Kostenuik M. A., Ossenkopp K. P., Kavaliers M. Sex differences in performance in the Morris water maze and the effects of initial nonstationary hidden platform training. Behav Neurosci. 1996 Dec;110(6):1309–1320. doi: 10.1037//0735-7044.110.6.1309. [DOI] [PubMed] [Google Scholar]
  20. Rissanen A., Puoliväli J., van Groen T., Riekkinen P., Jr In mice tonic estrogen replacement therapy improves non-spatial and spatial memory in a water maze task. Neuroreport. 1999 Apr 26;10(6):1369–1372. doi: 10.1097/00001756-199904260-00039. [DOI] [PubMed] [Google Scholar]
  21. Roof R. L., Havens M. D. Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Res. 1992 Feb 14;572(1-2):310–313. doi: 10.1016/0006-8993(92)90491-q. [DOI] [PubMed] [Google Scholar]
  22. Roof R. L. Neonatal exogenous testosterone modifies sex difference in radial arm and Morris water maze performance in prepubescent and adult rats. Behav Brain Res. 1993 Feb 26;53(1-2):1–10. doi: 10.1016/s0166-4328(05)80261-x. [DOI] [PubMed] [Google Scholar]
  23. Saucier D., Cain D. P. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature. 1995 Nov 9;378(6553):186–189. doi: 10.1038/378186a0. [DOI] [PubMed] [Google Scholar]
  24. Voyer D., Voyer S., Bryden M. P. Magnitude of sex differences in spatial abilities: a meta-analysis and consideration of critical variables. Psychol Bull. 1995 Mar;117(2):250–270. doi: 10.1037/0033-2909.117.2.250. [DOI] [PubMed] [Google Scholar]
  25. Warren S. G., Humphreys A. G., Juraska J. M., Greenough W. T. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res. 1995 Dec 12;703(1-2):26–30. doi: 10.1016/0006-8993(95)01059-9. [DOI] [PubMed] [Google Scholar]
  26. Warren S. G., Juraska J. M. Spatial and nonspatial learning across the rat estrous cycle. Behav Neurosci. 1997 Apr;111(2):259–266. doi: 10.1037//0735-7044.111.2.259. [DOI] [PubMed] [Google Scholar]
  27. Williams C. L., Barnett A. M., Meck W. H. Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci. 1990 Feb;104(1):84–97. doi: 10.1037//0735-7044.104.1.84. [DOI] [PubMed] [Google Scholar]
  28. Williams C. L., Meck W. H. The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology. 1991;16(1-3):155–176. doi: 10.1016/0306-4530(91)90076-6. [DOI] [PubMed] [Google Scholar]
  29. Woolley C. S., McEwen B. S. Estradiol mediates fluctuation in hippocampal synapse density during the estrous cycle in the adult rat. J Neurosci. 1992 Jul;12(7):2549–2554. doi: 10.1523/JNEUROSCI.12-07-02549.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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