Elsevier

Brain and Language

Volume 83, Issue 3, December 2002, Pages 403-424
Brain and Language

Variability in the anatomy of the planum temporale and posterior ascending ramus: Do right- and left handers differ?

https://doi.org/10.1016/S0093-934X(02)00509-6Get rights and content

Abstract

The anatomy of the planum temporale (PT) and posterior ascending ramus (PAR) was studied in vivo in 67 healthy right- and left-handed adults using MRI-based morphometry. The left PT was significantly larger than the right, and there was a weakly significant effect of the right PAR larger than the left. A leftward PT asymmetry was found in 72%, and a rightward PAR asymmetry was found in 64% of the sample. The “typical” configuration of a larger left PT and larger right PAR co-occurred in 56% of the subjects studied, which was only slightly more often than predicted by chance. Eight of 67 subjects had “reversed” PT and PAR asymmetries, with consistent left and mixed handers over-represented in this group. Right PAR size was the only variable that predicted writing hand, and left PT size was the only measure that differed by sex. The left PT was expanded relative to the left PAR in 93% of the sample, suggesting that this configuration may be developmentally regulated and may be a critical substrate for the development of language. These findings demonstrate that important relationships exist between hand preference, and the anatomy of posterior cortical language areas.

Introduction

Hand preference is perhaps the most blatant behavioral asymmetry observed in man, and the relationship between handedness and lateralized behaviors has been of interest since the latter part of the 19th century, when Paul Broca (1861) described language disturbances associated with a contralateral hemiparesis in right handers. The notion that most right handers have language lateralized to the left cerebral hemisphere has been supported by nearly 150 years of research using the ablation paradigm, intracarotid amytal studies, electrocortical stimulation, functional neuroimaging studies and indirect behavioral paradigms (for review, see Galaburda, 1995; Geschwind and Galaburda, 1985a, Geschwind and Galaburda, 1985b, Geschwind and Galaburda, 1985c; Hellige, 1993; Kitterle, 1991). There is evidence that left- and right handers differ when compared on a variety of behavioral measures (for review, see Annett & Alexander, 1996; Herron, 1980; Peters, 1995). Generally, right handers are more homogeneous then left handers on behavioral measures, as they are more likely to prefer the right hand for manual activities, to be more dexterous and powerful with the right hand, and to have language lateralized to the contralateral left cerebral hemisphere. Thus, in right handers the neural systems that contribute to these behaviors are lateralized predominantly to the left cerebral hemisphere, and the hand used to write is contralateral to the hemisphere mediating language functions. In contrast, in most left handers language is ipsilateral to the preferred hand, as about 70% of left handers are left hemisphere dominant for language. In addition, left handers are more likely to be dissociated on measures of hand preference, skill and strength than right handers (for review, see Peters, 1995; Schacter, 1997). Many investigators have studied the relationship of anatomical asymmetries to lateralized behaviors, and differences between right- and left handers have been reported but, it remains unclear as to whether distinct anatomical configurations within the temporoparietal opercular regions are more common in right versus left handers (Beaton, 1997).

It is well established that anatomical asymmetries exist in the posterior temporal and parietal opercula of the human cerebral cortex with the planum temporale (PT) larger in the left cerebral hemisphere in about 70% (for review, see Galaburda, 1995; Leonard et al., 1996; Steinmetz, 1996; Witelson & Kigar, 1988), and the posterior ascending ramus (PAR) larger in the right hemisphere in about 69% of post-mortem brains unselected for handedness (Witelson & Kigar, 1992). The PT, located on the postcentral horizontal portion of the supratemporal plane visible within the Sylvian fossa, is comprised of auditory association cortex important in higher order auditory processing and constitutes a portion of Wernicke’s area. The PAR is the vertical continuation of the lateral Sylvian fissure into the inferior parietal lobe, is comprised of heteromodal association cortex, and the gyral banks surrounding this ramus constitute the supramarginal gyrus. Because of the prominent asymmetries, divergent cytoarchitecture within these cortical regions (Eidelberg & Galaburda, 1984; Galaburda et al., 1978) and clinical-behavioral studies, it has been suggested that the left PT may be a neuroanatomical substrate for language (Blonder, Pettigrew, & Smith, 1994; Foundas, Leonard, Gilmore, Fennell, & Heilman, 1994; LeMay & Culebras, 1972) whereas the right PAR may be a substrate for sensory attentional systems (Eidelberg & Galaburda, 1984) and/or for visuospatial processing with the left mediating praxis functions (Witelson & Kigar, 1992). Conclusive evidence regarding the functional significance of these anatomical regions is lacking. There is even less direct evidence of whether right- and left handers differ on anatomical measures of cortical speech-language areas that may be linked to interhemispheric differences. Despite the fact that hand preference is used as an indirect measure of cerebral laterality, and left handers are often considered “atypical,” left handers are often excluded from studies and there are only a few studies that have investigated anatomical variation in right- and left handers (Beaton, 1997).

The studies that have been done have defined handedness groups in different ways. Witelson and Kigar (1992) studied anatomical asymmetries in two hand preference groups: consistent right handers (CRH) and non-consistent right handers (NCRH). Based on hand preference from an inventory, CRH were defined as individuals who reported exclusive right-hand use, and NCRH included individuals who preferred the left hand for one or more items. Thus, the NCRH group included mixed right- and left handers. Foundas, Leonard, and Heilman (1995) studied the anatomy of frontal and posterior cortical language areas in right- and left handers, with hand preference groups defined by writing hand and by scores on a handedness inventory. Steinmetz and colleagues (Steinmetz, 1995; Steinmetz, Volkman, Jancke, & Freund, 1991) have also studied anatomical differences in right- and left handers with hand preference defined by writing hand. Although results of these studies offer partial support for the notion that left handers are more anatomically “atypical” than right handers, the use of different handedness groups in these studies and small sample size make these results tenuous. In addition, we do not know of any studies that have examined left- and right handedness and degree of handedness within subjects to determine whether right- and left handers differ. Thus, it is unclear whether the group designation, CRH–NCRH versus right- and left handers, has influenced the results or whether these groups are really biologically distinct.

The major goal of this study was to determine whether healthy right- and left handers differ on measures of the anatomy of temporoparietal cortex. Volumetric MRI methodologies were utilized to measure the PT and the PAR in a sample of healthy right- and left-handed adults. Three questions were asked: (1) Will the size of the PT and PAR differ in right- and left handers? (2) Will there be differences in the interhemispheric asymmetry distributions when right- and left handers are compared?, and (3) Will there be differences when intrahemispheric configurations are compared between right- and left handers? The following predictions were made: (1) the left PT would be significantly larger than the right, and the right PAR would be significantly larger than the left, (2) independent of handedness, a larger left PT would exist in about 70% of the sample and a larger right PAR would exist in about 69%, consistent with data from post-mortem and neuroimaging studies to date, (3) anatomical asymmetries of the PT and PAR would be normally distributed with the former shifted to the left and the latter shifted to the right, (4) writing hand and degree of handedness would be related to anatomical asymmetries with consistent right handers more likely to have “typical” anatomy than left handers, who would have more anatomical variation within these regions, (5) subjects with completely “reversed” anatomy (i.e., a larger right PT and larger left PAR) would be more likely to be left handers and/or mixed right handers than consistent right handers. The intrahemispheric relationship of the PT to the PAR was studied in our sample, as we were interested in learning whether the “typical” configuration of a larger left PT and larger right PAR co-occurred within subjects at a frequency greater than predicted by chance. If these anatomical configurations co-occurred within subjects more often than predicted by chance, then these asymmetries may be developmentally regulated, whereas if these asymmetries co-occur at chance or below, than these anatomical asymmetries are less likely to be developmentally regulated, and may sort independently (Geschwind and Galaburda, 1985a, Geschwind and Galaburda, 1985b, Geschwind and Galaburda, 1985c). In addition to the interhemispheric PT and PAR asymmetries, a “typical” intrahemispheric relationship of the PT to the PAR has been observed (Leonard, Glendinning, Wilfong, Cooper, & Vierick, 1992). Leonard et al. (1993) suggested that within the left hemisphere the PT, temporal bank, is usually larger than the PAR, parietal bank. Rarely, the parietal bank expands relative to the temporal bank, with this variation occurring more often in dyslexic children and family members of dyslexics than in linguistically intact controls. This configuration was uncommon in controls and occurred more often in the individuals with dyslexia, therefore, Leonard et al. (1992) speculated that this configuration may interfere with phonological decoding abilities.

Section snippets

Subjects

The sample of subjects (N=67) included healthy adults, between the ages of 18–55 years, recruited to participate as healthy controls for studies of brain morphology at the University of Florida, Health Sciences Center, Gainesville, Florida. The subject group consisted of approximately equal numbers of men (n=36, 54%) and women (n=31, 46%). For the sample, mean age was 30.44 years (SD=11.31, range 18–55 years), and educational level was 15.2 years (SD=2.1, range 11–20 years), with age and

PT and PAR anatomy: Effects of hemisphere, sex, writing hand and degree of handedness

A repeated measures multivariate analysis of variance (MANOVA) was conducted to determine the difference in measurements of PT, PAR, and PT plus PAR of the left hemisphere compared to measurements of the right hemisphere as a function of sex and writing hand (right or left). Means and standard deviations for these measures are summarized by writing hand and hemisphere in Table 1. The between subjects effects were not significant for main effects for sex [F(1,63)=.29, p<.59], or writing hand [F

Discussion

It is well established that anatomical asymmetries exist in humans within the posterior perisylvian regions with the most common configuration being a larger left planum temporale (PT) and a larger right posterior ascending ramus (PAR). The specific relationship of these anatomical configurations to hand preference and degree of handedness has not been adequately studied (Beaton, 1997). Thus, MRI-based morphometry was used to study anatomical asymmetries in vivo in a large sample of healthy

Acknowledgements

The authors would like to acknowledge the Department of Radiology and the MR technicians of the Shands Hospital at the University of Florida Health Sciences Center, Gainesville, Florida for their assistance with the acquisition of the MR scans. The authors would like to thank Julie H. Aguilar and Christine Kastner for their assistance with the preparation of the manuscript. This study was supported by NIH Grant DC00135 (ALF) and the Department of Veterans Affairs VISN 16 MIRECC. Portions of

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