Brain, Vol. 123, No. 2, 404-406,
February 2000
© 2000 Oxford University Press
Letters to the Editor |
Language processing in both sexes: evidence from brain studies
Prince of Wales Medical Research Institute, University of New South Wales, Australia
Correspondence to:
Dr Jenny Harasty, Prince of Wales Medical Research Institute, University of New South Wales, AustraliaE-mail: j.harasty{at}unsw.edu.au
Thank you for the interesting paper by Frost et al. (Frost et al., 1999
). As they suggest, understanding sex differences in the human brain is not trivial. Many studies of disease groups are conducted on one sex only and extrapolated across genders. Indeed, the basis of the Talairach atlas is one example of this approach. Therefore, determining whether clear sex differences exist in language-associated brain is important for future work.
The work by Frost et al. adds important data to this confusing field. They report no differences between men and women on a semantic monitoring task (identify if an animal is `found in the United States' and `used by human') and then report no differences in functional MRI brain activation. The authors should be commended for their tight statistical design with a large number of subjects, an aspect of the work which should be used in future studies.
However, it is important to note that such a semantic monitoring task would not be expected to show sex differences. These differences have been identified and replicated clearly in many studies in which females excel in tasks of verbal fluency and verbal memory types of language skills (Bradshaw, 1989; Mann et al., 1990; Halpern, 1992; Kimura, 1996). In defence of the expectation of Frost et al. that their semantic–lexical task would show sex differences, the authors argue that their task is an auditory equivalent of Pugh's task on sex differences in aspects of reading. However, the task of Pugh et al. differs significantly from these auditory tasks due to the involvement of grapheme-based visuospatial aspects that change the task from a simple lexical–semantic task by adding in aspects of reading (Pugh et al., 1996).
Unfortunately, Frost et al. have suggested that their results lead to a conclusion that there are no sex differences in language processing or in the neural organization of such processing [apart from those shown by Witelson et al. (1995)]. Although they discuss the data of Shaywitz et al. (1995) on functional language differences (Shaywitz et al., 1995) and our data on large proportional size differences in the planum temporale and Broca's area (Harasty et al., 1997), the authors prefer to obscurate these data.
Indeed Frost et al. suggest that our data are contradicted by those of Abiotiz et al. and by those of Witelson and Kigar (Aboitiz et al., 1992; Witelson and Kigar, 1992). This is not the case. Previous data relate to the length of the planum temporale, while we report a difference in the volume of the cortex of this important language-processing structure in the order of a proportional 30% size difference between men and women. Such a morphometric difference needs to be replicated especially across age groups and cultures (as our subjects were post-mortem specimens from ages of ~60 years and over). However, to date, our findings have not been contradicted by other data and do suggest a clear neurobiological difference in the morphometry of the language areas.
It would be a pity if the work of Frost et al. on a semantic monitoring task led to a general conclusion that there is no functional or morphometric evidence for a neurobiological basis for sex differences in language.
Acknowledgments
Thank you to Professor Simon Gandevia and Dr Glenda Halliday for comments on earlier versions of this letter.
References
Aboitiz F, Scheibel AB, Zaidel E. Morphometry of the Sylvian fissure and the corpus callosum, with emphasis on sex differences. Brain 1992; 115: 1521–41.
Bradshaw JL. Hemispheric specialization and psychological function. Chichester (UK): John Wiley; 1989.
Frost JA, Binder JR, Springer JA, Hammeke TA, Bellgowan PS, Roa SM, et al. Language processing is strongly left lateralized in both sexes: evidence from fMRI. Brain 1999; 122: 199–208.
Halpern DF. Sex differences in cognitive abilities. Hillsdale (NJ): Lawrence Erlbaum; 1986.
Harasty J, Double KL, Halliday GM, Kril JJ, McRitchie DA. Language-associated cortical regions are proportionally larger in the female brain. Arch Neurol 1997; 54: 171–6.
Kimura D. Sex, sexual orientation and sex hormones influence human cognitive function. [Review]. Curr Opin Neurobiol 1996; 6: 259–63.[Web of Science][Medline]
Mann VA, Sasanuma S, Sakuma N, Masaki S. Sex differences in cognitive abilities: a cross-cultural perspective. Neuropsychologia 1990; 28: 1063–77.[Web of Science][Medline]
Pugh KR, Shaywitz BA, Shaywitz SE, Constable RT, Skudlarski P, Fulbright RK, et al. Cerebral organization of component processes in reading. Brain 1996; 119: 1221–38.
Shaywitz BA, Shaywitz SE, Pugh KR, Constable RT, Skudlarski P, Fulbright RK, et al. Sex differences in the functional organization of the brain for language. Nature 1995; 373: 607–9.[Medline]
Witelson SF, Kigar DL. Sylvian fissure morphology and asymmetry in men and women: bilateral differences in relation to handedness in men. J Comp Neurol 1992; 323: 326–40.[Web of Science][Medline]
Witelson SF, Glezer II, Kigar DL. Women have greater density of neurons in posterior temporal cortex. J Neurosci 1995; 15: 3418–28.[Abstract]
Reply
Department of Neurology, Medical College of Wisconsin, USA
Correspondence to:
Jeffrey Binder, Department of Neurology, Medical College of Wisconsin, 9200 West Wisconsin Avenue, Milwaukee, WI 53226, USA
We thank Dr Harasty for her interest in our paper and for pointing out some of its limitations. The question of whether large-scale functional or morphometric differences exist between the brains of women and men is complex and as yet not fully resolved. It is concerning such questions particularly that history teaches us to proceed with considerable scepticism (Gould, 1996).
There is little doubt that women, as a group, perform better than men as a group on tasks emphasizing verbal fluency. To conclude from this that women are better at language than men would be a gross over-generalization: most language tasks do not show reliable sex differences, and men, as a group, even excel slightly at some of these. As Dr Harasty makes clear, there is no a priori reason to expect sex differences in brain activation during tasks on which men and women perform equivalently. The fMRI results of Pugh et al., which show sex differences in lateralization of brain activity across a variety of phonological and semantic tasks even in the absence of performance differences (Pugh et al., 1996), are thus somewhat unanticipated and foster a general conclusion that the language systems of men and women show radical organizational differences independent of behavioural abilities. The purpose of reporting our data was to provide evidence against this more sweeping conclusion. In short, we believe it is significant that there is at least one language task for which brain activation patterns are very similar in women and men.
We thus agree that observation of sex differences during functional imaging should depend on the type of task employed, but evidence that this is the case has not been impressive. Whereas Pugh et al. found brain activation differences across all tasks, including semantic tasks on which men and women perform equivalently, Buckner et al. found no such differences using verbal fluency tasks on which men and women perform differently (Buckner et al., 1995), and Price et al. found none on tasks very similar to those used by Pugh et al. (Price et al., 1996). Because both of these studies (which gave negative results) employed tasks that involved reading, and because Pugh et al. controlled for visuospatial and grapheme processing, the discrepancies cannot be explained by `involvement of grapheme-like visuospatial aspects that change the task . . . by adding in aspects of reading.'
We concur with Dr Harasty that our findings should not be taken as support for a general conclusion that there are no functional or morphometric sex differences of any kind in the language-processing system. Our intention was rather to show that the data pertaining to this issue are far from consistent, and that more systematic, carefully controlled studies are needed with larger numbers of subjects. Our discussion of the literature on planum temporale morphometry was intended as a brief overview, and we apologize for omitting potentially important methodological differences between the studies by Harasty et al., Aboitiz et al. and Witelson and Kigar (Aboitiz et al., 1992; Witelson and Kigar, 1992; Harasty et al., 1997). As Dr Harasty points out, her study is the only one to use volumetric measurement of autopsy tissue, and the findings have not been contradicted. It should be noted, however, that these findings (i.e. bilaterally larger plana temporale in 11 women than in 10 men when normalized for overall brain size, P = 0.04) do not support the hypothesis of stronger language lateralization in men than women: in both groups, the plana were symmetrical in size. The findings of Harasty et al. and Pugh et al. are thus consistent in that both show sex differences related to language organization, but the differences observed are themselves inconsistent.
It seems likely that there is a publication bias against studies that demonstrate a null hypothesis (Dickersin and Min, 1993), so it is possible that many studies showing an absence of sex effects in language processing may never have been published. It would be a pity to discount those that have been published and that were conducted carefully with adequate statistical power, particularly in a field of inquiry so sorely in need of empirical data.
References
Aboitiz F, Scheibel AB, Zaidel E. Morphometry of the Sylvian fissure and the corpus callosum, with emphasis on sex differences. Brain 1992; 115: 1521–41.
Buckner RL, Raichle ME, Petersen SE. Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups. J Neurophysiol 1995; 74: 2163–73.
Dickersin K, Min YI. Publication bias: the problem that won't go away. Ann NY Acad Sci 1993; 703: 135–48.[Web of Science][Medline]
Gould SJ. The mismeasure of man. New York: W.W. Norton; 1996.
Harasty J, Double KL, Halliday GM, Kril JJ, McRitchie DA. Language-associated cortical regions are proportionally larger in the female brain. Arch Neurol 1997; 54: 171–6.
Price CJ, Moore CJ, Friston KJ. Getting sex into perspective. Neuroimage 1996; 3 (3 Pt 2): S586.
Pugh KR, Shaywitz BA, Shaywitz SE, Constable RT, Skudlarski P, Fulbright RK, et al. Cerebral organization of component processes in reading. Brain 1996; 119: 1221–38.
Witelson SF, Kigar DL. Sylvian fissure morphology and asymmetry in men and women: bilateral differences in relation to handedness in men. J Comp Neurol 1992; 323: 326–40.
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