Extreme Male Brain Theory of Autism
DOI:
https://doi.org/10.18192/riss-ijhs.v2i1.1525Keywords:
Autism spectrum disorders, extreme male brain theory, systemizing– empathizing theory, foetal testosterone TheoryAbstract
Autism spectrum conditions (ASCs) are a category of neurodevelopmental disorders with symptoms of communication and social impairment, and the exhibition of restrictive and repetitive behaviours. Their occurrence is greater in males than females and this sex difference has played an important part in hypothesizing their etiology. The Extreme Male Brain (EMB) theory is a cognitive model proposed by Simon Baron-Cohen to explain the aforementioned sex differences and potential cause of ASCs. It is based upon his Empathizing Systemizing theory, which classifies individuals into one of five cognitive profiles (Type S, Type E, Type B, Extreme Type S and Extreme Type E). These cognitive profiles determine an individual’s ability to systemize and empathize. Systemizing is the ability to understand and derive the rules of a system, and requires deductive and analytical skills. Empathizing relates to understanding human emotion and behaviour, thus requires social and communication skills. Males tend to systemize better than empathize while females have an opposite profile. Based upon the EMB theory, autistic individuals would possess an Extreme Type S profile as their impairments in social communication can be explained by a deficit in empathizing, while their preoccupation with patterns and detail-oriented behaviour can be related to their high systemizing. Together, these cognitive models have resulted in the Foetal Testosterone (fT) Theory, which implicates high prenatal testosterone as a risk factor for the associated hypermasculinized cognitive profile of individuals with ASCs. This review paper assesses the validity of the EMB and fT theories by reviewing the literature relating fT with autistic traits in the general population. The seven studies confirmed a correlation between higher fT levels and an increase in autistic traits, but limitations need to be considered when generalizing this information to an ASC sample.
References
Auyeung, B., Baron-Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, K., & Hackett, G. (2009). Fetal testosterone and autistic traits. British Journal of Psychology, 100(Pt1), 1- 22. doi: 10.1348/000712608X311731
Auyeung, B., Baron-Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, K., Hackett, G., & Hines, M. (2009). Fetal testosterone predicts sexually differentiated childhood behaviour in girls and in boys. Psychological Science, 20(2), 144-148. doi: 10.1111/j.1467-9280.2009.02279.x
Auyeung, B., Taylor, K., Hackett, G., & Baron-Cohen, S. (2010). Foetal testosterone and autistic traits in 18 to 24-month-old children. Molecular Autism, 1(1), 11-19. doi: 10.1186/2040-2392-1-11
Barbeau, E. B., Mendrek, A., & Mottron, L. (2009). Are autistic traits autistic? British Journal of Psychology, 100, 23-28. doi: 10.1348/000712608X337788
Baron-Cohen, S. (2002). The extreme male brain theory of autism. Trends in Cognitive Sciences, 6(6), 248-254.
Baron-Cohen, S. (2009). Autism: the empathizing-systemizing (E-S) theory. Annals of the New York Academy of Sciences, 1156, 68-80. doi: 10.1111/j.1749- 6632.2009.04467.x
Baron-Cohen, S., Auyeung, B., Ashwin, E., & Knickmeyer, R. (2009). Fetal testosterone and autistic traits: A response to three fascinating commentaries. British Journal of Psychology, 100(1), 39-47. doi: 10.1348/000712608X394271
Baron-Cohen, S., Knickmeyer, R. C., Belmonte, M. K. (2005). Sex differences in the brain: implications for explaining autism. Science, 310(5749), 819-823. doi: 10.1126/ science.1115455
Baron-Cohen, S., Richler, J., Bisarya, D., Gurunathan, N., & Wheelwright, S. (2003). The systemizing quotient: an investigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358(1430), 361-374. doi: 10.1098/rstb.2002.1206
Casto, J. M., Ward, O. B., & Bartke, A. (2003). Play, copulation, anatomy and testosterone in gonadally intact male rates prenatally exposed to flutamide. Physiology & Behaviour, 79(4-5), 633-641. doi: 10.1016/S0031-9384(03) 00120-3
Chakrabarti, B., Dudbridge, F., Kent, L., Wheelwright, S., Hill-Cawthorne, G., Allison, C., Banjerjee-Basu, S., & Baron-Cohen, S. (2009). Genes related to sex steroids, neural growth, and social-emotional behaviour are associated with autistic traits, empathy and Asperger syndrome. Autism Research, 2(3), 157-177. doi: 10.1002/ aur.80
Chapman, E., Baron-Cohen, S., Auyeung, B., Knickmeyer, R., Taylor, K., & Hackett, G. (2006). Fetal testosterone and empathy: Evidence from the empathy quotient (EQ) and the ‘Reading the mind in the eyes’ test. Social Neuroscience, 1(2), 135-148. doi: 10.1080/17470910600992239
Chura, L. R., Lombardo, M. V., Ashwin, E., Auyeung, B., Chakrabarti, B., Bullmore, E. T., & Baron-Cohen, S. (2010). Organizational effects of fetal testosterone on human corpus callosum size and asymmetry. Psychoneuroendocrinology, 35(1), 122-132. doi: 10.1016/j.psyneuen.2009.09.009
Collins, D. W., & Kimura, D. (1997). A large sex difference on a two-dimensional mental rotation task. Behavioural Neuroscience, 111(4), 845-849. Retrieved from http:// dx.doi.org/10.1037/0735-7044.111.4.845
Faras, H., Al Ateeqi, N., & Tidmarsh, L. (2010). Autism spectrum disorders. Annals of Saudi Medicine, 30(4), 295- 300. doi: 10.4103/0256-4947.65261
Finegan, J. A., Bartleman, B., & Wong, P. Y. (1989). A window for the study of prenatal sex hormone influences on postnatal development. The Journal of Genetic Psychology, 150(1), 101-112. doi: 10.1080/00221325.1989.9914580
Geschwind, N., & Behan, P. (1982). Left-handedness: association with immune disease, migraine, and developmental learning disorder. Proceedings of the National Academy of Sciences of the United States of America, 79(16), 5097- 5100.
Geschwind, N. & Galaburda, A. M. (1985). Cerebral lateralization: Biological mechanisms, associations, and pathology. Archives of Neurology, 42(5), 428-459. doi: 10.1001/archneur.1985.04060050026008
Gitau, R., Adams, D., Fisk, N. M., & Glover, V. (2005) Fetal plasma testosterone correlates positively with cortisol. Archives of Disease in Childhood. Fetal and Neonatal Edition, 90, F166-F169. doi: 10.1136/adc.2004.049320
Goldenfeld, N., Baron-Cohen, S., & Wheelwright, S. (2005). Empathizing and systemizing in males, females and autism. Clinical Neuropsychiatry, 2(6), 338-345. doi: 10.1017/CBO9780511543753.019
Goy, R. W., Bercovitch, F. B., & McBrair, M. C. (1988). Behavioural masculinisation is independent of genital masculinisation in prenatally androgenised female rhesus macaques. Hormones and Behaviour, 22(4), 552-571. doi: 10.1016/0018-506X(88)90058-X
Goy, R. W., & McEwen, B. S. (1980). Sexual differentiation of the brain, ed., MIT Press, Cambridge, MA, reviewed in Walled, K. (2005) Hormonal influences on sexually differentiated behaviour in nonhuman primates. Frontiers in Neuroendocrinology, 26, 7-26
Hill, E.L., & Frith, U. (2003). Understanding autism: insights from mind and brain. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358(1430), 281-289. doi: 10.1098/rstb.2002.1209
Hines, M. (2006). Prenatal testosterone and gender related behaviour. European Journal of Endocrinology, 155 (Suppl. 1), S115-121. doi: 10.1530/eje.1.02236
Hines, M., Fane, B. A., Pasterski, V. L., Matthews, G. A., Conway, G. S., & Brook C. (2003). Spatial abilities follow- ing prenatal androgen abnormality: targeting and mental rotations performance in individuals with congenital adrenal hyperplasia. Psychoneuroendocrinology, 28(8), 1010 -1026.
Hughes, J. R. (2008). A review of recent reports on autism: 1000 studies published in 2007. Epilepsy & Behaviour, 13 (3), 425-437. doi: 10.1016/j.yebeh.2008.06.015
Jones, A., Cork, C., Chowdhury, U. (2006). Autistic spectrum disorders. 1: Presentation and assessment. Community Practitioner: The Journal of the Community Practitioners’ & Health Visitors’ Association, 79 (3), 97-98.
Knickmeyer, R. C. & Baron-Cohen, S. (2006). Fetal testosterone and sex differences. Early Human Development, 82 (12), 755-760. doi: 10.1016/j.earlhumdev.2006.09.014
Knickmeyer, R. C., & Baron-Cohen, S. (2006). Fetal testosterone and sex differences in typical social development and in autism. Journal of Child Neurology, 21(10), 825- 845. doi: 10.1177/08830738060210101601
Knickmeyer, R., Baron-Cohen, S., Fane, B. A., Wheelwright, S., Mathews, G. A., Conway, G. C., & Hines, M. (2006a). Androgens and autistic traits: A study of individuals with congenital adrenal hyperplasia. Hormones and Behaviour, 50(1), 148-153. doi: 10.1016/ j.yhbeh.2006.02.006
Knickmeyer, R., Baron-Cohen, S., Raggatt, P., & Taylor, K. (2005). Foetal testosterone, social relationships, and restricted interests in children. Journal of Child Psychology and Psychiatry, 46(2), 198-210. doi: 10.1111/j.1469- 7610.2004.00349.x
Knickmeyer, R., Baron-Cohen, S., Raggatt, R., Taylor, K., & Hackett, G. (2006b). Fetal testosterone and empathy. Hormones and Behaviour, 49(3), 282-292. doi: 10.1016/j.yhbeh.2005.08.010
Manning, J. T., Baron-Cohen, S., Wheelwright, S., & Sanders, G. (2001). The 2nd to 4th digit ratio and autism. Developmental Medicine and Child Neurology, 43 (3), 160-164. doi: 10.1111/j.1469-8749.2001.tb00181.x
Manson, J. E. (2008). Prenatal exposure to sex steroid hormones and behavioural/cognitive outcomes. Metabolism: Clinical and Experimental, 57(Suppl. 2), S16-21. doi: 10.1016/j.metabol.2008.07.010
Marco, E.J., & Skuse, D. H. (2006). Autism – lessons from the X chromosome. Social Cognitive and Affective Neuroscience, 1(3), 183-193. doi: 10.1093/scan/nsl028
Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behaviour in the female guinea pig. Endocrinology, 65, 369- 382. Retrieved from http://dx.doi.org/10.1210/endo-65-3-369
Pomerantz, S. M., Fox, T. O., Sholl, S. A., Vito, C. C., & Goy, R. W. (1985). Androgen and estrogen receptors in fetal rhesus monkey brain and anterior pituitary. Endocrinology, 116(1), 83-89. Retrieved from http://dx.doi.org/10.1210/endo-116-1-83
Skuse, D. H. (2009). Is autism really a coherent syndrome in boys, or girls? British Journal of Psychology, 100(Pt1), 33-37. doi: 10.1348/000712608X369459
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 (2), 250-270. Retrieved from http://dx.doi.org/10.1037/0033-2909.117.2.250
Wakabayashi, A., Baron-Cohen, S., Uchiyama, T., Yoshida, Y., Kuroda, M., & Wheelwright, S. (2007). Empathizing and systemizing in adults with and without autism spectrum conditions: cross-cultural stability. Journal of Autism and Developmental Disorders, 37(10), 1823-1832. doi: 10.1007/s10803-006-0316-6
Wallen, K. (2005). Hormonal influences on sexually differentiated behaviour in nonhuman primates. Frontiers in Neuroendocrinology, 26(1), 7-26. doi: 10.1016/j.yfrne.2005.02.001
Wallen, K., Maestripieri, D., & Mann, D. R. (1995). Effects of neonatal testicular suppression with a GnRH antagonist on social behaviour in group-living juvenile rhesus monkeys. Hormones and Behaviour, 29(3), 322-337. doi: 10.1006/hbeh.1995.1023
Ward, I. L., Ward, O. B., Affuso, J. D., Long, W. D. 3rd, French, J. A., & Hendricks, S. E. (2003). Fetal testosterone surge: specific modulation induced in male rates by maternal stress and/or alcohol consumption. Hormones and Behaviour, 43, 531-539. doi: 10.1016/S0018-506X(03) 00061-8
Whitehouse, A. J., Mayberry, M. T., Hart, R., Mattes, E., Newnham, J. P., Sloboda, D. M., Stanley, F. J., & Hickey, M. (2010). Fetal androgen exposure and pragmatic language ability of girls in middle childhood: implications for the extreme male-brain theory of autism. Psychoneuroendocrinology, 35(8), 1259-1264. doi: 10.1016/j.psyneuen.2010.02.007
Auyeung, B., Baron-Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, K., Hackett, G., & Hines, M. (2009). Fetal testosterone predicts sexually differentiated childhood behaviour in girls and in boys. Psychological Science, 20(2), 144-148. doi: 10.1111/j.1467-9280.2009.02279.x
Auyeung, B., Taylor, K., Hackett, G., & Baron-Cohen, S. (2010). Foetal testosterone and autistic traits in 18 to 24-month-old children. Molecular Autism, 1(1), 11-19. doi: 10.1186/2040-2392-1-11
Barbeau, E. B., Mendrek, A., & Mottron, L. (2009). Are autistic traits autistic? British Journal of Psychology, 100, 23-28. doi: 10.1348/000712608X337788
Baron-Cohen, S. (2002). The extreme male brain theory of autism. Trends in Cognitive Sciences, 6(6), 248-254.
Baron-Cohen, S. (2009). Autism: the empathizing-systemizing (E-S) theory. Annals of the New York Academy of Sciences, 1156, 68-80. doi: 10.1111/j.1749- 6632.2009.04467.x
Baron-Cohen, S., Auyeung, B., Ashwin, E., & Knickmeyer, R. (2009). Fetal testosterone and autistic traits: A response to three fascinating commentaries. British Journal of Psychology, 100(1), 39-47. doi: 10.1348/000712608X394271
Baron-Cohen, S., Knickmeyer, R. C., Belmonte, M. K. (2005). Sex differences in the brain: implications for explaining autism. Science, 310(5749), 819-823. doi: 10.1126/ science.1115455
Baron-Cohen, S., Richler, J., Bisarya, D., Gurunathan, N., & Wheelwright, S. (2003). The systemizing quotient: an investigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358(1430), 361-374. doi: 10.1098/rstb.2002.1206
Casto, J. M., Ward, O. B., & Bartke, A. (2003). Play, copulation, anatomy and testosterone in gonadally intact male rates prenatally exposed to flutamide. Physiology & Behaviour, 79(4-5), 633-641. doi: 10.1016/S0031-9384(03) 00120-3
Chakrabarti, B., Dudbridge, F., Kent, L., Wheelwright, S., Hill-Cawthorne, G., Allison, C., Banjerjee-Basu, S., & Baron-Cohen, S. (2009). Genes related to sex steroids, neural growth, and social-emotional behaviour are associated with autistic traits, empathy and Asperger syndrome. Autism Research, 2(3), 157-177. doi: 10.1002/ aur.80
Chapman, E., Baron-Cohen, S., Auyeung, B., Knickmeyer, R., Taylor, K., & Hackett, G. (2006). Fetal testosterone and empathy: Evidence from the empathy quotient (EQ) and the ‘Reading the mind in the eyes’ test. Social Neuroscience, 1(2), 135-148. doi: 10.1080/17470910600992239
Chura, L. R., Lombardo, M. V., Ashwin, E., Auyeung, B., Chakrabarti, B., Bullmore, E. T., & Baron-Cohen, S. (2010). Organizational effects of fetal testosterone on human corpus callosum size and asymmetry. Psychoneuroendocrinology, 35(1), 122-132. doi: 10.1016/j.psyneuen.2009.09.009
Collins, D. W., & Kimura, D. (1997). A large sex difference on a two-dimensional mental rotation task. Behavioural Neuroscience, 111(4), 845-849. Retrieved from http:// dx.doi.org/10.1037/0735-7044.111.4.845
Faras, H., Al Ateeqi, N., & Tidmarsh, L. (2010). Autism spectrum disorders. Annals of Saudi Medicine, 30(4), 295- 300. doi: 10.4103/0256-4947.65261
Finegan, J. A., Bartleman, B., & Wong, P. Y. (1989). A window for the study of prenatal sex hormone influences on postnatal development. The Journal of Genetic Psychology, 150(1), 101-112. doi: 10.1080/00221325.1989.9914580
Geschwind, N., & Behan, P. (1982). Left-handedness: association with immune disease, migraine, and developmental learning disorder. Proceedings of the National Academy of Sciences of the United States of America, 79(16), 5097- 5100.
Geschwind, N. & Galaburda, A. M. (1985). Cerebral lateralization: Biological mechanisms, associations, and pathology. Archives of Neurology, 42(5), 428-459. doi: 10.1001/archneur.1985.04060050026008
Gitau, R., Adams, D., Fisk, N. M., & Glover, V. (2005) Fetal plasma testosterone correlates positively with cortisol. Archives of Disease in Childhood. Fetal and Neonatal Edition, 90, F166-F169. doi: 10.1136/adc.2004.049320
Goldenfeld, N., Baron-Cohen, S., & Wheelwright, S. (2005). Empathizing and systemizing in males, females and autism. Clinical Neuropsychiatry, 2(6), 338-345. doi: 10.1017/CBO9780511543753.019
Goy, R. W., Bercovitch, F. B., & McBrair, M. C. (1988). Behavioural masculinisation is independent of genital masculinisation in prenatally androgenised female rhesus macaques. Hormones and Behaviour, 22(4), 552-571. doi: 10.1016/0018-506X(88)90058-X
Goy, R. W., & McEwen, B. S. (1980). Sexual differentiation of the brain, ed., MIT Press, Cambridge, MA, reviewed in Walled, K. (2005) Hormonal influences on sexually differentiated behaviour in nonhuman primates. Frontiers in Neuroendocrinology, 26, 7-26
Hill, E.L., & Frith, U. (2003). Understanding autism: insights from mind and brain. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 358(1430), 281-289. doi: 10.1098/rstb.2002.1209
Hines, M. (2006). Prenatal testosterone and gender related behaviour. European Journal of Endocrinology, 155 (Suppl. 1), S115-121. doi: 10.1530/eje.1.02236
Hines, M., Fane, B. A., Pasterski, V. L., Matthews, G. A., Conway, G. S., & Brook C. (2003). Spatial abilities follow- ing prenatal androgen abnormality: targeting and mental rotations performance in individuals with congenital adrenal hyperplasia. Psychoneuroendocrinology, 28(8), 1010 -1026.
Hughes, J. R. (2008). A review of recent reports on autism: 1000 studies published in 2007. Epilepsy & Behaviour, 13 (3), 425-437. doi: 10.1016/j.yebeh.2008.06.015
Jones, A., Cork, C., Chowdhury, U. (2006). Autistic spectrum disorders. 1: Presentation and assessment. Community Practitioner: The Journal of the Community Practitioners’ & Health Visitors’ Association, 79 (3), 97-98.
Knickmeyer, R. C. & Baron-Cohen, S. (2006). Fetal testosterone and sex differences. Early Human Development, 82 (12), 755-760. doi: 10.1016/j.earlhumdev.2006.09.014
Knickmeyer, R. C., & Baron-Cohen, S. (2006). Fetal testosterone and sex differences in typical social development and in autism. Journal of Child Neurology, 21(10), 825- 845. doi: 10.1177/08830738060210101601
Knickmeyer, R., Baron-Cohen, S., Fane, B. A., Wheelwright, S., Mathews, G. A., Conway, G. C., & Hines, M. (2006a). Androgens and autistic traits: A study of individuals with congenital adrenal hyperplasia. Hormones and Behaviour, 50(1), 148-153. doi: 10.1016/ j.yhbeh.2006.02.006
Knickmeyer, R., Baron-Cohen, S., Raggatt, P., & Taylor, K. (2005). Foetal testosterone, social relationships, and restricted interests in children. Journal of Child Psychology and Psychiatry, 46(2), 198-210. doi: 10.1111/j.1469- 7610.2004.00349.x
Knickmeyer, R., Baron-Cohen, S., Raggatt, R., Taylor, K., & Hackett, G. (2006b). Fetal testosterone and empathy. Hormones and Behaviour, 49(3), 282-292. doi: 10.1016/j.yhbeh.2005.08.010
Manning, J. T., Baron-Cohen, S., Wheelwright, S., & Sanders, G. (2001). The 2nd to 4th digit ratio and autism. Developmental Medicine and Child Neurology, 43 (3), 160-164. doi: 10.1111/j.1469-8749.2001.tb00181.x
Manson, J. E. (2008). Prenatal exposure to sex steroid hormones and behavioural/cognitive outcomes. Metabolism: Clinical and Experimental, 57(Suppl. 2), S16-21. doi: 10.1016/j.metabol.2008.07.010
Marco, E.J., & Skuse, D. H. (2006). Autism – lessons from the X chromosome. Social Cognitive and Affective Neuroscience, 1(3), 183-193. doi: 10.1093/scan/nsl028
Phoenix, C. H., Goy, R. W., Gerall, A. A., & Young, W. C. (1959). Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behaviour in the female guinea pig. Endocrinology, 65, 369- 382. Retrieved from http://dx.doi.org/10.1210/endo-65-3-369
Pomerantz, S. M., Fox, T. O., Sholl, S. A., Vito, C. C., & Goy, R. W. (1985). Androgen and estrogen receptors in fetal rhesus monkey brain and anterior pituitary. Endocrinology, 116(1), 83-89. Retrieved from http://dx.doi.org/10.1210/endo-116-1-83
Skuse, D. H. (2009). Is autism really a coherent syndrome in boys, or girls? British Journal of Psychology, 100(Pt1), 33-37. doi: 10.1348/000712608X369459
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 (2), 250-270. Retrieved from http://dx.doi.org/10.1037/0033-2909.117.2.250
Wakabayashi, A., Baron-Cohen, S., Uchiyama, T., Yoshida, Y., Kuroda, M., & Wheelwright, S. (2007). Empathizing and systemizing in adults with and without autism spectrum conditions: cross-cultural stability. Journal of Autism and Developmental Disorders, 37(10), 1823-1832. doi: 10.1007/s10803-006-0316-6
Wallen, K. (2005). Hormonal influences on sexually differentiated behaviour in nonhuman primates. Frontiers in Neuroendocrinology, 26(1), 7-26. doi: 10.1016/j.yfrne.2005.02.001
Wallen, K., Maestripieri, D., & Mann, D. R. (1995). Effects of neonatal testicular suppression with a GnRH antagonist on social behaviour in group-living juvenile rhesus monkeys. Hormones and Behaviour, 29(3), 322-337. doi: 10.1006/hbeh.1995.1023
Ward, I. L., Ward, O. B., Affuso, J. D., Long, W. D. 3rd, French, J. A., & Hendricks, S. E. (2003). Fetal testosterone surge: specific modulation induced in male rates by maternal stress and/or alcohol consumption. Hormones and Behaviour, 43, 531-539. doi: 10.1016/S0018-506X(03) 00061-8
Whitehouse, A. J., Mayberry, M. T., Hart, R., Mattes, E., Newnham, J. P., Sloboda, D. M., Stanley, F. J., & Hickey, M. (2010). Fetal androgen exposure and pragmatic language ability of girls in middle childhood: implications for the extreme male-brain theory of autism. Psychoneuroendocrinology, 35(8), 1259-1264. doi: 10.1016/j.psyneuen.2010.02.007
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