BRAIN AND COGNITION 9, 238-243 (1989) lntrahemispheric Sex Differences in the Functional Representation of Language and Praxic Functions in Normal individuals RICHARD S. LEWIS AND LOIS CHIUSTIANSEN Pomona College, Claremont, California Kimura (1980, The Behavioral and Brain Sciences, 3,240-241; 1983, Canadian Journal of Psychology, 37, 19-35; 1987, Canadian Psychology, 28, 133-147) recently proposed that there are intrahemispheric sex differences in the organization of particular language and praxic functions such that in females these functions are more focally represented. This hypothesis, as well as supporting data, was derived from research with brain-injured subjects. The purpose of the present study was to test the utility of using dual-task methodology for investigating sex- related variation in intrahemispheric functional organization in normal individuals. Women were found to show greater interference than men on concurrent tasks of language and right-hand finger tapping. In support of Kimura’s model, the present findings yielded evidence suggestive of intrahemispheric sex differences in the “functional distance” between language and praxic functions within the left hemisphere of normal individuals. Q 1989 Academic PESS, IW. Variation in the lateral representation of cognitive functions has been the focus of much attention in neuropsychology and has been associated with the subject characteristics of sex (see McGlone, 1980)and handedness (see Herr-on, 1980). Kimura (1980, 1983, 1987) has recently stressed that the anterior-posterior direction may also be an important dimension of variation in functional brain organization, and reported sex differences in the intrahemispheric representation of language and praxic functions. She studied a group of right-handed patients with unilateral brain damage that was localized anterior to or posterior to the Rolandic fissure of the left hemisphere. Kimura found that women suffered from aphasia and apraxia more often after left anterior lesions than after left posterior lesions. Men showed a different pattern of results with no significant We express our appreciation to William P. Banks, Ph.D., for his valuable comments on an earlier draft, and Julie A. Lindberg for her artistry. Requests for reprints should be addressed to Richard S. Lewis, Department of Psychology, Pomona College, Claremont, CA 91711. 238 0278-2626189 $3.00 Copyright 0 1989 by Academic Press, Inc. All rights of reproduction in any form reserved.
Transcript
BRAIN AND COGNITION 9, 238-243 (1989)
lntrahemispheric Sex Differences in the Functional Representation of Language and Praxic Functions in
Normal individuals
RICHARD S. LEWIS AND LOIS CHIUSTIANSEN
Pomona College, Claremont, California
Kimura (1980, The Behavioral and Brain Sciences, 3,240-241; 1983, Canadian Journal of Psychology, 37, 19-35; 1987, Canadian Psychology, 28, 133-147) recently proposed that there are intrahemispheric sex differences in the organization of particular language and praxic functions such that in females these functions are more focally represented. This hypothesis, as well as supporting data, was derived from research with brain-injured subjects. The purpose of the present study was to test the utility of using dual-task methodology for investigating sex- related variation in intrahemispheric functional organization in normal individuals. Women were found to show greater interference than men on concurrent tasks of language and right-hand finger tapping. In support of Kimura’s model, the present findings yielded evidence suggestive of intrahemispheric sex differences in the “functional distance” between language and praxic functions within the left hemisphere of normal individuals. Q 1989 Academic PESS, IW.
Variation in the lateral representation of cognitive functions has been the focus of much attention in neuropsychology and has been associated with the subject characteristics of sex (see McGlone, 1980) and handedness (see Herr-on, 1980). Kimura (1980, 1983, 1987) has recently stressed that the anterior-posterior direction may also be an important dimension of variation in functional brain organization, and reported sex differences in the intrahemispheric representation of language and praxic functions. She studied a group of right-handed patients with unilateral brain damage that was localized anterior to or posterior to the Rolandic fissure of the left hemisphere. Kimura found that women suffered from aphasia and apraxia more often after left anterior lesions than after left posterior lesions. Men showed a different pattern of results with no significant
We express our appreciation to William P. Banks, Ph.D., for his valuable comments on an earlier draft, and Julie A. Lindberg for her artistry. Requests for reprints should be addressed to Richard S. Lewis, Department of Psychology, Pomona College, Claremont, CA 91711.
238 0278-2626189 $3.00 Copyright 0 1989 by Academic Press, Inc. All rights of reproduction in any form reserved.
INTRAHEMISPHERIC SEX DIFFERENCES 239
difference in frequency of aphasia and apraxia after either anterior or posterior left hemisphere lesions. Kimura concluded that particular language and praxic functions may be more diffusely represented within the left hemisphere of males.
Mateer, Polen, and Ojemann (1982) reported supporting evidence for Kimura’s claims that women show a more restricted representation of language functions. They found that men demonstrated naming errors after stimulation to the frontal and parietal lobes, but that women did not show naming errors after posterior parietal stimulation.
In a study of global aphasia, Vignolo, Boccardi, and Caverni (1986) reported that all cases of global aphasia (in their sample) after lesions restricted to the left posterior hemisphere (as judged from CT scans) were in men, whereas all cases of global aphasia after lesions restricted to the anterior left hemisphere were in women.
Although all three of these studies report converging evidence for Kimura’s hypothesis of intrahemispheric sex differences, their conclusions must be cautiously interpreted because all of these studies used brain- injured individuals. These findings would be strengthened if converging data were also found in studies of normal subjects.
Techniques such as visual half-field and dichotic listening that have been used to study lateralization of cognitive functions in normal individuals are not useful in studying the representation of functions along the anterior- posterior dimension. Dual task methodology, however, holds promise for investigating intrahemispheric functional organization.
Kinsboume and Hiscock (1983) proposed the cerebral functional distance model to account for experimental findings utilizing divided attention tasks. This principle states that the closer thefunctional distance between the representation of two functions, the greater the interference when the two functions are concurrently activated. Kinsbourne and Hiscock defined functional distance in terms of the degree of neural connectivity between two functional areas, rather than in terms of physical distance. Therefore, if we assume that the two cerebral hemispheres represent relatively independent attentional resources, then the functional distance principle would predict that more interference should be present when performing two functions represented within the left hemisphere, such as concurrently performing a verbal fluency task while tapping with the right hand, than when performing two functions represented within separate hemispheres, such as concurrently performing a verbal fluency task while finger tapping with the left hand, a finding supported by the majority of studies (Kinsbourne & Hiscock, 1983). This presumably occurs because of the greater degree of neural connectivity between areas represented within a hemisphere than usually found between hemispheres (except in the case of the extensive connections between complementary cortical areas). This principle should also hold for investigations of the functional
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distance within a cerebral hemisphere. If two functional areas within a hemisphere are more extensively connected than are two other functional areas within a hemisphere, we would expect to find greater interference when concurrently performing activities represented with the former two functions than when concurrently performing activities represented by the latter two functions.
Dual task methodology, therefore, offers a useful technique for in- vestigating variations in the intrahemispheric representation of cognitive functions. The present study was designed to test the utility of this method for investigating sex differences in the functional distance of language and praxic functions. It was hypothesized that if intrahemispheric sex differences in the representation of language and praxic functions exist, then there would most likely be a sex difference in the degree of neural connectivity between these two functions, resulting in a sex dif- ference in their functional distance. Therefore, if Kimura’s model is correct, we would expect to find a sex difference in the degree of in- terference when simultaneously performing a language and right-hand praxic task.
METHODS Subjects. Fourteen undergraduate men and 14 undergraduate women. age 18 to 21 years,
participated in this experiment. All of the subjects were self-reported right-handers. Hand- edness was verified by having the subjects demonstrate which hand they use during writing. This variable was selected because handwriting has been shown to have the highest loading on handedness factors (e.g. Orsini, Satz, Soper, & Light, 1985; Williams, 1986).
Materials and apparatus. Finger tapping was performed on a four-button apparatus connected to a digital counter that registered each time a sequence of four buttons was depressed. During the reading condition, subjects were asked to read aloud from five passages of an introductory psychology text, independently judged to be of similar difficulty. For the verbal fluency condition, subjects were instructed to generate words beginning with a target letter [F, A, S, C, and L, selected from Borkowski, Benton, & Spreen’s (1967) norms].
Procedure. First, subjects were familiarized with the finger tapping apparatus. They were then instructed to depress the buttons in a sequence using four fingers, starting from the index finger and progressing toward the little finger. Each subject was given two trials of 30 set each with each hand, one for practice, and the other to calculate a baseline finger tapping rate.
Two verbal tasks were administered to each subject, one of which was verbal fluency. This task involved generating as many words as possible starting with one of the target letters. Prior to the concurrent finger tapping-verbal fluency condition, subjects were given a practice trial of 30 set with one of five letters (F, A. S, C, L). The practice trial was followed by the concurrent finger tapping-verbal fluency conditions. Two trials of tapping with each hand were presented. The number of complete sequences of finger tapping was recorded.
The other verbal task was reading text passages aloud. Again subjects were presented with a practice trial during which they were asked to read aloud as many words as possible. This was followed by four 30-set concurrent task trials, finger tapping and reading, two with each hand. As in the previous conditions, the number of complete finger tapping sequences was recorded.
FIG. 1. Percentage decrement in finger tapping as a function of sex and tapping hand for the verbal fluency and reading aloud conditions.
The order of hand tapping, the verbal tasks, and the stimuli within the verbal tasks (i.e., the letters and reading passages) were randomly presented.
RESULTS
The number of finger tapping sequences was collapsed across the trials for each condition. The percentage decrement in finger tapping was cal- culated for each of the concurrent task conditions [(baseline tapping - concurrent tapping)/baseline tapping] x 100, and then entered into a multivariate analysis with the concurrent tasks and tapping hand the within-subject factors, and sex the between-subjects factor.
No three-way interaction was found between the effects of the tasks, tapping hand, and sex of the subject. A two-way interaction, however, was found between sex of the subject and tapping hand, F(1, 26) = 5.84, p = .023. As depicted in Fig. 1, for the right-hand condition, the women showed a significantly greater percentage decrement in finger tapping than the men, t(26) = 4.29, p < .OOl, but for the left-hand condition, there was no significant sex difference in finger tapping decrement, t(26) = 1.46, NS. A two-way interaction was not found between either the effects of tapping hand and task, or the effects of task and sex of subject.
In addition, there was (1) a main effect for the concurrent task condition, F( 1, 26) = 5.94, p = .022, with greater finger tapping decrements occurring for the verbal fluency concurrent task; (2) a main effect for tapping hand, F( 1,26) = 15.02, p = .OOl, with a greater decrement in tapping occurring for the right-hand; and (3) a main effect for sex, F(1, 26) = 12.96, p = .OOl, with females showing greater tapping decrements.
DISCUSSION
The results of the present study, with normal subjects, are consistent with previous reports of intrahemispheric sex differences in the repre-
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sentation of particular language and praxic functions found in brain- injured subjects (Kimura, 1980, 1983, 1987; Mateer et al., 1982; Vignolo et al., 1986). Evidence was found suggesting that for the right-hand (left hemisphere) condition females, relative to males, show less functional distance between the language and praxic functions examined in this study. This sex difference in intrahemispheric functional representation was not found for the left-hand (right hemisphere) condition.
Previous research from brain-damaged samples suggested that certain language and praxic functions were found to be more focally represented within the left hemisphere of females. Together with the present study, this suggests that the smaller functional distance (i.e., increased inter- ference) between language and praxic functions found for women results from their more focal representation of these functions within the left hemisphere.
The main effect of tapping hand is consistent with the majority of data finding greater interference in the right-hand (left hemisphere) condition for verbal concurrent tasks (see Kinsboume & Hiscock, 1983) and supports the suggestion that the verbal tasks are interfering to a greater degree with left hemisphere functions.
The main effect of task, with greater interference in the finger tapping- verbal fluency condition relative to the finger tapping-reading aloud con- dition, suggests that the two former functions are functionally closer than reading and finger tapping, and is consistent with other studies finding similar results for these types of tasks (see Kinsboume & Hiscock, 1983). It is important to note that the present results suggest that dual task methodology may be limited in its usefulness for investigating variation in inrerhemispheric representation of function (at least for sex differences). Figure 1 shows that the percentage decrement of finger tapping between the left- and right-hand conditions is smaller for males than females. A laterahty index derived from these finger tapping values would usually be interpreted as reflecting greater hemispheric asymmetry for the females (or greater symmetrical representation for males), results at odds with the majority of evidence regarding sex differences in cerebral lateralization (see, e.g., McGlone, 1980). The present results, therefore, suggest that such an interpretation could be very misleading because the degree of interference may be due to functional differences in intrahemispheric variation as well.
In summary, the results of the present study support the presence of intrahemispheric sex differences in the representation of language and praxic functions in a normal sample. As such, these results support previous research using brain-damaged samples which find a sex difference in the intrahemispheric representation of these functions. Together with Kimura’s data this study suggests that the greater functional distance found for males is related to their more diffuse representation of language
INTRAHEMISPHERIC SEX DIFFERENCES 243
and praxic functions within the left hemisphere. This study has also demonstrated how dual-task methodology can be productively used to investigate variations in the intrahemispheric representation of cerebral functions and could be extended to other potential sources of variation such as hand preference. Furthermore, future studies using concurrent tasks to investigate variation in cerebral lateralization will need to take into account the influence of variation in the intrahemispheric representation of cognitive functions, especially on the outcome of lateralization indices.
REFERENCES Borkowski, J. G., Benton, A. L., & Spreen, 0. 1967. Word fluency and brain damage.
Neuropsychologia, 5, 135-140. Herron, J. 1980. Neuropsychology of left-handedness. New York: Academic Press. Kimura, D. 1980. Sex differences in intrahemispheric organization of speech. The Behavioral
and Brain Sciences, 3, 240-241. Kimura, D. 1983. Sex differences in cerebral organization for speech and praxic functions.
Canadian Journal of Psychology, 37, 19-35. Kimura, D. 1987. Are men’s and women’s brains really different? Canadian Psychology,
28, 133-147. Kinsbourne, M., & Hiscock, M. 1983. Asymmetries of dual-task performance. In J. B.
Hellige (Ed.), Cerebral hemisphere asymmetry; Method, theory, and application. New York: Praeger.
Mateer, C. A., Polen, S. B., & Ojemann, G. A. 1982. Sexual variation in cortical localization of naming as determined by stimulation mapping. The Behavioral und Brain Sciences, 5, 310-311.
McGlone, J. 1980. Sex differences in human brain asymmetry: A critical survey. The Behavioral and Brain Sciences, 3, 215-264.
Orsini, D. L., Satz, P., Soper, H. V., & Light, R. K. (1985). The role of familial sinistrality in cerebral organization. Neuropsychologia, 23, 223-232.
Vignolo, L. A., Boccardi, E., & Caverni, L. (1986). Unexpected CT-scan findings in global aphasia. Cortex, 22, 55-69.
Williams, S. M. 1986. Factor analysis of the Edinburgh Handedness Inventory. Cortex, 22, 325-326.
