Abstract
Reports of morphological differences between the brains of humans with different sexual orientation1 or gender identity2 have furthered speculation that such behaviours may result from hormonal or genetic influences on the developing brain. However, the causal chain may be reversed; sexual behaviour in adulthood may have caused the morphological differences. I report how adult sexual experience alters the appearance of rat motor neurons as revealed by Nissl staining, the same technique used in post-mortem human studies.
Main
Male Sprague-Dawley rats were castrated at 117-123 days of age and I implanted 5-mm-long testosterone-filled Silastic capsules subcutaneously, to produce a much lower than normal concentration of circulating androgen while sustaining continued male copulatory behaviour3. One week later I gave each rat as a cage-mate an ovariectomized female that had been subcutaneously implanted with either a 5-mm capsule containing 10% oestradiol to induce constant behavioural receptivity4, or an empty capsule.
Male rats provided with oestrogen-treated cage-mates began copulating shortly after the introduction of the receptive female and were therefore labelled ‘copulators’. The males caged with untreated (and therefore unreceptive) females were never observed to copulate and are designated ‘non-copulators’. Females were replaced from a reserve pool every 3 days (with confirmation that only the oestrogen-treated females were receptive) for 27 days.
I stained the spinal cords from the males with thionin to reveal motor neurons in the spinal nucleus of the bulbocavernosus (SNB)5. These motor neurons and their striated target muscles are active during male copulatory behaviour6, and shrink after castration unless replacement testosterone is provided7. Changes in the size of SNB somata and nuclei are accompanied by changes in the number and size of synaptic inputs to the motor neurons8. An observer, blind to group membership, determined the number and cross-sectional area of SNB somata and nuclei7.
As expected, SNB somata and nuclei were smaller than in gonadally intact males7 (Fig. 1), and there was no difference between the groups in the number of SNB motor neurons. The number of neurons, which is reported in only a few human studies9, appears stable. The ten copulator males had significantly smaller SNB somata (P<0.04, two-tailed t-test) and nuclei (P<0.02) than the nine non-copulators. the bulbocavernosus muscles innervated by the snb were also lighter in copulators (711±37 mg; mean±s.e.m.) than in non-copulators (868±50; P<0.02). the animals received equivalent androgen exposure as shown by the lack of difference in either body mass (P>0.20) or themass of the highly androgen-sensitive seminal vesicles (168.5±12.9 mg, copulators; 177.8±11.9 mg, non-copulators).
Copulatory experience can therefore alter the size of neurons, as revealed by Nissl staining. Whether the sensory experience or motor activity of copulation induced these morphological changes, interpretations of correlations between human behaviour and neural morphology must acknowledge that the two are reciprocally related10,11. It is possible that differences in sexual behaviour cause, rather than are caused by, differences in brain structure.
References
LeVay, S. Science 253, 1034–1037 (1991).
Zhou, J.-N., Hofman, M. A., Gooren, L. J. G. & Swaab, D. F. Nature 378, 68–70 (1995).
Damassa, D. A., Smith, E. R., Tennent, B. & Davidson, J. M. Hormones Behav. 8, 275–286 (1977).
Blaustein, J. D., Brown, T. J. & Reading, D. S. Physiol. Behav. 29, 475–481 (1982).
Breedlove, S. M. & Arnold, A. P. Science 210, 564–566 (1980).
Holmes, G. M., Chapple, W. D., Leipheimer, R. E. & Sachs, B. D. Physiol. Behav. 49, 1235–1246 (1991).
Breedlove, S. M. & Arnold, A. P. Brain Res. 225, 297–307 (1981).
Leedy, M. G., Beattie, M. S. & Bresnahan, J. C. Brain Res. 424, 386–390 (1987).
Swaab, D. F., Gooren, L. J. G. & Hofman, M. A. Prog. Brain Res. 93, 205–219 (1992).
Bennett, E. L., Diamond, M. L., Krech, D. & Rosenzweig, M. R. Science 146, 610–619 (1964).
Hubel, D. H. & Wiesel, T. N. J. Neurophysiol. 28, 1041–1059 (1965).
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Breedlove, S. Sex on the brain. Nature 389, 801 (1997). https://doi.org/10.1038/39764
Issue Date:
DOI: https://doi.org/10.1038/39764
This article is cited by
-
An anthropometric study of sexual orientation and gender identity in Thailand
Scientific Reports (2021)
-
Turning sex inside-out: Peripheral contributions to sexual differentiation of the central nervous system
Biology of Sex Differences (2012)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.