1 Division of Psychiatric Neuro-Imaging, Department of Psychiatry and Behavioral Science, Johns Hopkins University School of Medicine, Baltimore, MD 21287 and , 2 Department of Radiology, University of Washington School of Medicine, Seattle, WA 98195, USA
Address correspondence to Godfrey D. Pearlson, MD, Division of Psychiatric Neuro-Imaging, Department of Psychiatry and Behavioral Sciences, Johns Hopkins Medical University School of Medicine, 600 North Wolfe Street, Baltimore, MD 21287, USA. Email: godfr{at}jhmi.edu.
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Abstract |
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Introduction |
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The parietal lobes subserve cognitive functions primarily involving attention and perception. More specifically, the IPL is involved in selective attention (Petersen et al., 1989; Mirsky et al., 1992
; Heilman et al., 1993
) and visuospatial processing (Keating and Gooley, 1988
; Petersen et al., 1989
). Some of these cognitive tasks appear to lateralize to either the right or the left parietal lobe. For example, the right parietal lobe may be more involved in spatial working memory tasks (Jonides et al., 1993
), sensing relationships between body parts (Cutting, 1991
) and the recognition of affect (Borod et al., 1986
; Cleghorn et al., 1989a
,b
). The left IPL is more involved in cognitive tasks related to perception, such as mental rotation of three-dimensional figures (Alivisatos and Petrides, 1997
), judgments of target speed (Corbetta et al., 1991
) and position (Lacquaniti et al., 1997
), time estimation (Maquet et al., 1996
), complex motor planning (Winstein et al., 1997
) and non-semantic aspects of verbal processing (Vandenberghe et al., 1996
).
Thus, given normal sex differences in brain structure and function, especially with regard to asymmetries in HASC regions, and normal lateralization of cognitive functions, it is reasonable to hypothesize that sex differences in structural IPL asymmetry may underlie some sex differences in cognitive functioning. Indeed, in an MRI study of cortical volumes Kennedy et al. found normal sex differences in the parietal lobe, but although left and right hemispheric measurements were obtained, the authors did not specifically examine sex-by-hemisphere interactions (Kennedy et al., 1998). As sex-based asymmetries in the IPL have not previously been examined, we thus made the following hypotheses: (i) males have greater total IPL volumes compared to women, (ii) males have larger left versus right IPL volumes and (iii) males have larger left IPL volumes compared to women.
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Materials and Methods |
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We examined 15 pairs of normal male and female subjects who were individually matched on age (±5 years), race, handedness and parental socioeconomic status (Hollingshead, 1975), giving a total of 30 subjects. The male versus female groups did not differ significantly on age (mean age of males = 39.7 years, range = 2458 years; mean age of females = 38.4 years, range = 2353 years), race (86.67% Caucasian and 13.33% non-Caucasian in both gender groups) or family socioeconomic status (20% of level 2 and 80% of level 3 in both gender groups). All 30 subjects were right-handed as assessed by the Chapman inventory (Chapman and Chapman, 1987
).
Volunteer study subjects were recruited from the community via advertisement (n = 12), via random telephone-digit dialing as part of a community-based aging study (n = 4), as well as from the Epidemiologic Catchment Area (ECA) study (Regier et al., 1984) (n = 5). In addition, nine subjects served as normal controls in a study by a collaborator in London. No subjects had a history or MRI evidence of overt brain disease (via radiological interpretation), lifetime history of substance abuse/ dependence or any medical illnesses known to affect the brain, e.g. severe head injury with loss of consciousness >1 h, severe hypertension (e.g. requiring treatment with two or more medications), or significant cardiovascular disease requiring medical or surgical treatment. In addition, subjects had no current or history of major mental illness as assessed by the Schedules for Clinical Assessment in Neuropsychiatry (Wing et al., 1990
) and DSM III-R criteria, or in any first-degree relatives (assessed by questionnaire).
Magnetic Resonance Imaging
All subjects gave written informed consent in accordance with institutional standards. MRI scans were obtained on one of three GE Signa 1.5 T units all using the same edition of GE software and identical scanning sequences. Approximately equal numbers of male and female subjects were scanned on each MRI unit. Contiguous slices were acquired through the entire brain in the coronal plane using a spoiled gradient recall acquisition in the steady state (GRASS) sequence (TR = 35, TE = 5) with a flip angle of 45°. Slices were 1.5 mm thick with a field of view of 20 or 24 and a matrix size of 256 x 256.
Image Processing and Measurement
All raters were blind to subject sex. Using the software Measure' developed in our laboratory (Barta et al., 1997), raters stripped all brains of skull and dura via reliable semi-automated techniques (Aylward et al., 1997
; Buchanan et al., 1998
). Realistic three-dimensional brain images were rendered, enabling easy visualization of sulcalgyral patterns. All brains were aligned along the anteriorposterior commissural (ACPC) line and the interhemispheric fissure.
By using a paint and point-counting' method similar to that described by Buchanan et al. for subparcellating the frontal lobe (Buchanan et al., 1998), the IPL was first delineated by painting along the IPL sulcalgyral landmarks on a cortical surface three-dimensional rendering. These painted boundaries would later (see below) be superimposed upon two-dimensional orthogonal slices in order to select grid points lying within the boundaries. Utilizing such surface renderings for determining sulcalgyral landmarks and transferring these boundaries to serial sections has been described by other authors (Damasio and Frank, 1992
; Barta et al., 1995
; Kulynych et al., 1996). For a more in-depth discussion of these techniques, as well as a detailed description of our IPL measurement methodology, see M.E. Frederikse et al. (submitted). The IPL boundaries included the postcentral sulcus anteriorally and the intraparietal sulcus superiorally. The inferior boundary consisted of: (i) the Sylvian fissure from the postcentral sulcus to the planum temporale (PT) posterior lateral edge; (ii) a plane passing through the PT posterior lateral edge and the temporo-occipital incisure to the superior temporal (or parallel) sulcus; and (iii) the parallel sulcus to its horizontal segment (anterior occipital sulcus) and its connection with the intraparietal sulcus.
The SPGR data set was filtered using locally developed anisotropic diffusion filtering software (K = 1.5 x average sigma value of ten random values within the caudate nucleus; number of iterations = 3) to better visualize the gray-white boundary (Gerig et al., 1990). A three-dimensional grid of points spaced 4.5 mm apart and yielding ~200 points per IPL was superimposed on the entire volume. Paint' demarcating the IPL anatomical borders was then superimposed upon the filtered image set, and gray matter points lying within the painted borders were selected. Both this stereological volume estimation method (Cavalieri') (Barta et al., 1997
) and the paint method (Buchanan et al., 1998
) have been discussed in previous publications. Due to imprecise white matter boundaries for this and other cortical regions, IPL white matter volumes were not obtained. Interrater reliability for the volume measurement yielded an unbiased intraclass coefficient (of Bartko and Carpenter) of 0.98 in five randomly selected brains.
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Results |
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In order to determine if TBV need be a covariate in the statistical analysis, ANOVA of TBV between males and females was first conducted. This analysis revealed no significant difference in TBV between males and females (F = 2.63, df = 1,29, P = 0.12), indicating no need to covary for TBV. Repeated- measures ANOVA was then conducted with hemisphere as the repeated measure and sex as the between-subjects variable. This analysis revealed a main effect of sex (F = 11.66, df = 1,28, P < 0.01), with males having significantly larger total IPL volume than females. Although there was no main effect of hemisphere (F = 2.60, df = 1,28, P = 0.66), the hemisphere-by-sex interaction approached statistical significance (F = 3.47, df = 1,28, P = 0.07).
Given our hypothesis that the left IPL is larger than the right in men, repeated-measures ANOVA was performed in males only with hemisphere as the repeated measure. In this analysis, left IPL volume was not significantly greater than right IPL volume in men (F = 3.03, df = 1,14, P = 0.10).
Because of the significant sex difference in total IPL volume, as well as our a priori hypotheses, we wanted to examine which side contributed most to the male/female total IPL volume difference. Analyses of variance revealed that men had significantly larger left IPL volumes compared to females (F = 11.54, df = 1,29, P = 0.02). The right IPL, however, showed no significant sex differences on ANOVA (F = 3.18, df = 1,29, P = 0.09). Figure 2 depicts mean IPL volume/TBV ratios in the left and right IPLs for males versus females, demonstrating that the left, but not the right, IPL is significantly larger in males compared to females.
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Discussion |
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In a cytoarchitectonic parcellation of the parietal lobes of eight human brains, Eidelberg and Galaburda showed leftward asymmetry for most of the angular gyrus (area PG'), correlating with a larger left planum temporale (Eidelberg and Galaburda, 1984). Conversely, another, yet smaller, portion of the angular gyrus (area PEG'), corresponding to the most posterior superior aspect of the gyrus, showed rightward asymmetry (Eidelberg and Galaburda, 1984
). As reported by the authors, there was no significant effect of sex or age, although this analysis would have likely required a larger sample as only four male and four female brains were examined. Other limitations of the Eidelberg and Galaburda study included widely varying subject age (males 2586 years; females 467 years), lack of handedness information, and volumetric analyses of only the angular (not the supramarginal) gyrus. Because our study did not separate the angular and the supramarginal gyri, we are unable to compare our volumes with those of the Eidelberg and Galaburda study.
Iwasaki et al. found more intricate and extensive folding of the left IPL in 500 adults by examining cerebral white matter medullary branching patterns on CT (Iwasaki et al., 1986). In a later study with 276 children, the same group (Iwasaki et al., 1990
) demonstrated that childhood patterns did not differ significantly from those found in adults. Similarly, in a MRI study of 149 healthy subjects, Raz et al. showed asymmetry in the IPL, again with the left side being larger (Raz et al., 1997
). While the Raz study used neuroanatomical landmarks to define the region, IPL volume was estimated from a small number (510) of 0.86 mm coronal slices, 1.5 mm apart. Their delineation of the IPL corresponds approximately to Brodmann area 40 (supramarginal gyrus), but also includes portions of primary and secondary visual cortex (Brodmann areas 17 and 18). While their measurement technique may produce highly reliable data, it may be of more modest validity because of lack of anatomical precision.
As for sex differences in the IPL, we are only aware of the Kennedy et al. study cited earlier, which found sexual dimorphism in the IPL, specifically the angular gyrus (Kennedy et al., 1998). Kennedy et al. found the parietal lobe to be larger in volume in men compared to women, likely due to greater angular gyrus volume. While the volumes obtained between the Kennedy study and our study were very similar, our study differs in that we also examined sex-by-hemisphere interactions. Furthermore, while following sulcalgyral landmarks in two-dimensional views, Kennedy et al. utilized a coarser measurement methodology (Rademacher et al., 1992
; Caviness et al., 1996
) using 3 mm thick coronal slices (as opposed to our 1.5 mm thick coronal slices), as well as anterior and posterior borders defined by anatomically landmarked coronal planes. Other differences in their study include a smaller sample size (10 men, 10 women) and using both right- and left-handed subjects. Further inspection of their study reveals widely ranging interrater reliability coefficients from 0.29 to 0.96 for parietal regions. Such methodological differences suggest that the measurement methodology utilized in our study is as good as, if not superior to, the method employed by Kennedy et al., given our delineation of the IPL based upon surface sulcalgyral landmarks, visualization of the region in three orthogonal views and highly reliable measures.
Several studies have demonstrated global and regional brain sexual structural dimorphisms, in both normal children and adults (Witelsen and Kigar, 1992; Dreisen and Raz, 1995; Schlaepfer et al., 1995
; Raz et al., 1995
, 1997
; Reiss et al., 1996
; Giedd et al., 1997
; Kennedy et al., 1998
). These studies indicate the presence of sex-associated differences in cerebral development and organization, processes most likely beginning during fetal development [reviewed by Marsh and Casper (Marsh and Casper, 1998
)]. Of note, Schlaepfer et al., using 5 mm MRI sections and approximations to cortical regions of interest, demonstrated that in addition to women having significantly smaller brains compared to men, regional brain sex differences also existed. However, total IPL gray matter percentages were not significantly different between men and women (Schlaepfer et al., 1995
).
While our study was conducted in an exceptionally well-matched sample population and utilized a highly reliable measurement method, the lack of accompanying detailed neuropsychological data makes direct comparison between brain findings and cognitive data speculative. Other possible methodological deficiencies of this study include: (i) lack of IPL white matter measurements, (ii) using right-handed subjects only and (iii) raters not being blind to hemisphere being measured. As there are no precise white matter boundaries for the IPL, as well as other cortical structures, we are unable as yet to develop reliable measurement techniques for the white matter. As for the issue of handedness, many asymmetrical brain measures, e.g. planum temporale and radius of gyration, have correlated with handedness (Steinmetz et al., 1991; Bullmore et al., 1995
). Thus, it is possible that left-handed individuals show variants of the pattern we demonstrated. Whereas raters were blind to subject gender, the current imaging software does not allow for techniques such as counterbalanced mirroring which would blind raters to hemisphere, and thus experimenter bias may conceivably be a factor in these measures.
As described previously, men tend to outperform women on tasks of visuospatial processing, a function subserved by the IPL, particularly the left side. Given the finding of larger left IPL volume in males compared to females, this study provides a possible structural brain basis for such sex-based cognitive differences. In addition, this cross-sectional study only attempts to describe malefemale structural differences in the IPL, and does not permit making conclusions as to malefemale brain developmental differences. Future studies, e.g. functional neuroimaging studies, assessing activation during cognitive tests specific to parietal regions, as well as longitudinal studies, with an emphasis on sex differences, lateralization and development, in normal states would be useful.
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Acknowledgments |
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