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Variability of Broca's Area Homologue in African Great Apes: Implications

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Variability of Broca's Area Homologue in African Great Apes: Implications THE ANATOMICAL RECORD PART A 271A:276–285 (2003) Variability of Broca’s Area Homologue in African Great Apes: Implications for Language Evolution CHET C. SHERWOOD,1–3* DOUGLAS C. BROADFIELD,4,5 1,3 3,6 RALPH L. HOLLOWAY, PATRICK J. GANNON, AND PATRICK R. HOF2,3,7,8 1Department of Anthropology, Columbia University, New York, New York 2Fishberg Research Center for Neurobiology and Kastor Neurobiology of Aging Laboratories, Mount Sinai School of Medicine, New York, New York 3New York Consortium in Evolutionary Primatology, New York, New York 4Department of Anthropology, Florida Atlantic University, Boca Raton, Florida 5Department of Biomedical Sciences, Florida Atlantic University, Boca Raton, Florida 6Department of Otolaryngology, Mount Sinai School of Medicine, New York, New York 7Departments of Geriatrics and Adult Development, Mount Sinai School of Medicine, New York, New York 8Department of Ophthalmology, Mount Sinai School of Medicine, New York, New York 9Foundation for Comparative and Conservation Biology, Rockville, Maryland ABSTRACT The cortical circuits subserving neural processing of human language are localized to the inferior frontal operculum and the posterior perisylvian region. Functional language dominance has been related to anatomical asymmetry of Broca’s area and the planum temporale. The evolutionary history of these asymmetric patterns, however, remains obscure. Although testing of hypotheses about the evolution of language areas requires comparison to homologous regions in the brains of our closest living relatives, the great apes, to date little is known about normal interindividual variation of these regions in this group. Here we focus on Brodmann’s area 44 in African great apes (Pan troglodytes and Gorilla gorilla). This area corresponds to the pars opercularis of the inferior frontal gyrus (IFG), and has been shown to exhibit both gross and cytoarchitectural asymmetries in humans. We calculated frequencies of sulcal variations and mapped the distribution of cytoarchitectural area 44 to determine whether its boundaries occurred at consistent macrostructural landmarks. A considerable amount of variation was found in the distribution of the inferior frontal sulci among great ape brains. The inferior precentral sulcus in particular was often bifurcated, which made it impossible to determine the posterior boundary of the pars opercularis. In addition, the distribution of Brodmann’s area 44 showed very little correspondence to surface anatomy. We conclude that gross morphologic patterns do not offer substantive landmarks for the measurement of Brodmann’s area 44 in great apes. Whether or not Broca’s area homologue of great apes exhibits humanlike asymmetry can only be resolved through further analyses of microstruc- tural components. Anat Rec Part A 271A:276–285, 2003. © 2003 Wiley-Liss, Inc. Key words: Broca’s area; brain evolution; language; great apes; chimpanzee; gorilla Broca’s area, located in the inferior frontal gyrus (IFG) of humans, is a key component of the cortical circuitry that subserves language production. In approximately 95% of humans the left hemisphere is dominant for language (Branche et al., 1964), as demonstrated by functional imag- Grant sponsor: National Science Foundation; Grant numbers: ing (Petersen et al., 1988) and cortical stimulation studies BCS0121286; IBN9905402; SBR9617262; Grant sponsor: LSB Leakey Foundation; Grant sponsor: Wenner-Gren Foundation; (Rasmussen and Milner, 1975; Ojemann, 1991). Whereas Grant sponsor: National Institute on Aging; Grant number: numerous studies of gross and microscopic structure have AG14308. revealed anatomic asymmetries that may underlie this func- *Correspondence to: Chet C. Sherwood, Department of Anthro- tional dominance in humans, an important unresolved ques- pology, Columbia University, 452 Schermerhorn Ext., 1200 Am- tion is whether this asymmetric pattern is evolutionarily sterdam Ave., New York, NY 10027. Fax: (212) 854-7347. novel to humans (autapomorphic) or is shared with our clos- E-mail: [email protected] est living relatives, the great apes (synapomorphic). Received 7 May 2002; Accepted 27 December 2002 At the microstructural level, Broca’s area is comprised DOI 10.1002/ar.a.10046 of Brodmann’s areas 44 and 45 (Aboitiz and Garcia, 1997). Published online 7 March 2003 in Wiley InterScience Studies of microstructural features in Broca’s area of hu- (www.interscience.wiley.com). © 2003 WILEY-LISS, INC. BROCA’S AREA HOMOLOGUE IN GREAT APES 277 man brains have revealed several significant asymme- laris: the fronto-orbital sulcus and the inferior precentral tries. Volumetric cytoarchitecture-based studies have sulcus) is asymmetric in great ape brains. Based on sur- shown that area 44, but not area 45, is leftward dominant face area measurements, the authors concluded that the (Galaburda, 1980; Amunts et al., 1999). Using Golgi im- majority of African great ape brains exhibit significant left pregnation of the posterior IFG, Scheibel and colleagues hemisphere dominance in this region. Certainly, if this (Scheibel, 1984; Scheibel et al., 1985) found a greater region of great ape brains is asymmetric, the evolution of number of higher-order branches on the basal dendrites of human brain language areas will require reevaluation. pyramidal neurons in the left hemisphere compared to the Several problems, however, potentially mitigate against right, suggesting more integrative function in the domi- using MRI data to accurately measure asymmetries of nant hemisphere. In another study, layer III magnopyra- pars opercularis or area 44 in these species. It is possible midal neurons of area 45 were found to be significantly that, similar to humans, interindividual variability in the larger, and to express nonphosphorylated neurofilament expression of sulcal landmarks (Tomaiuolo et al., 1999) protein at higher frequencies in the left hemisphere com- and cytoarchitectural boundaries (Amunts et al., 1999) of pared to the right. This indicates a possible anatomical the IFG may confound a direct relationship between ex- specialization of area 45 for language in the dominant ternal features and cytoarchitecture in this region. Al- hemisphere (Hayes and Lewis, 1995). though the sulci of the chimpanzee and gorilla IFG have In humans, cytoarchitectural subdivisions of Broca’s been the subject of several studies (Cunningham, 1892; Le area generally fall within distinct morphological bound- Gros Clark, 1927; Mingazzini, 1928; Tilney and Riley, aries of the IFG. The ascending (vertical) ramus of the 1928; Papez, 1929; Walker and Fulton, 1936; von Bonin, Sylvian fissure separates the pars opercularis (area 44) 1949; Bailey et al., 1950) there is little information avail- from the pars triangularis (area 45), and the anterior able regarding variability in the frequencies of morpho- ramus divides the pars triangularis from the pars orbitalis logical patterns, and microstructural variability is not (area 47). Numerous studies have investigated macro- documented whatsoever. The purpose of the present study structural asymmetry in Broca’s area using these sulcal was to investigate the distribution of sulcal variation in landmarks to subdivide the region. Results from these the IFG of African great apes, and to map interindividual macrostructural studies, however, have differed markedly variation in the correspondence between cytoarchitecture depending upon methodology and anatomical definitions. and external morphology. The results of this study have Although cortical surface area measures of the frontal implications for the use of surface morphology to assess operculum do not reveal significant population-level left- asymmetries of anterior language areas of living great ward dominance (Wada et al., 1975; Witelson and Kigar, apes and fossil early hominins. 1992), asymmetries are significant when the intrasulcal MATERIALS AND METHODS portion of this cortex is included (Falzi et al., 1982; To- maiuolo et al., 1999). Some volumetric MRI-based studies Analysis of External Morphology have concluded that both the pars triangularis (Foundas Postmortem cerebral hemispheres from a total of 90 et al., 1998, 2001) and the pars opercularis (Foundas et al., African great apes, including 77 common chimpanzees 1998) are leftward dominant; however, others have not (Pan troglodytes) and 13 Western lowland gorillas (Gorilla found volumetric asymmetry in the pars opercularis (To- gorilla gorilla), were available for examination of surface maiuolo et al., 1999). In sum, a consensus does not yet morphology. Only adult brain specimens that were un- exist regarding macrostructural asymmetries of the hu- damaged in the region of the IFG were analyzed. Thirty- man IFG. seven hemispheres were obtained from the Smithsonian In great apes, the fronto-orbital sulcus (not the ascend- Institution’s collection of wild-caught animal brains (from ing ramus) forms the anterior border of the pars opercu- 29 chimpanzees and eight gorillas). Fifty-three brain laris (Connolly, 1950; Shantha and Manocha, 1969), and hemispheres were obtained from animals (48 chimpanzees the pars triangularis is not consistently present (Connolly, and five gorillas) that lived in research or zoological facil- 1950). Nevertheless, cytoarchitectural studies of the chim- ities. panzee and orang-utan frontal cortex describe a dysgranu- Variability of IFG sulci was analyzed from photographic lar region lying just anterior to the inferior precentral images. Each hemisphere was photographed with a digital sulcus designated Brodmann’s
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