Planum Parietale of Chimpanzees and Orangutans: a Comparative Resonance of Human-Like Planum Temporale Asymmetry

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Planum Parietale of Chimpanzees and Orangutans: a Comparative Resonance of Human-Like Planum Temporale Asymmetry THE ANATOMICAL RECORD PART A 287A:1128–1141 (2005) Planum Parietale of Chimpanzees and Orangutans: A Comparative Resonance of Human-Like Planum Temporale Asymmetry 1 2 3 PATRICK J. GANNON, * NANCY M. KHECK, ALLEN R. BRAUN, AND RALPH L. HOLLOWAY4 1Department of Otolaryngology, Mount Sinai School of Medicine, New York, New York 2Department of Medical Education, Mount Sinai School of Medicine, New York, New York 3National Institutes of Health, National Institute on Deafness and Other Communication Disorders, Bethesda, Maryland 4Department of Anthropology, Columbia University, New York, New York ABSTRACT We have previously demonstrated that leftward asymmetry of the planum temporale (PT), a brain language area, was not unique to humans since a similar condition is present in great apes. Here we report on a related area in great apes, the planum parietale (PP). PP in humans has a rightward asymmetry with no correlation to the LϾR PT, which indicates functional independence. The roles of the PT in human language are well known while PP is implicated in dyslexia and communication disorders. Since posterior bifurcation of the syl- vian fissure (SF) is unique to humans and great apes, we used it to determine characteristics of its posterior ascending ramus, an indicator of the PP, in chimpanzee and orangutan brains. Results showed a human-like pattern of RϾLPP(P ϭ 0.04) in chimpanzees with a nonsig- nificant negative correlation of LϾR PT vs. RϾLPP(CCϭϪ0.3; P ϭ 0.39). In orangutans, SF anatomy is more variable, although PP was nonsignificantly RϾL in three of four brains (P ϭ 0.17). We have now demonstrated human-like hemispheric asymmetry of a second language-related brain area in great apes. Our findings persuasively support an argument for addition of a new component to the comparative neuroanatomic complex that defines brain language or polymodal communication areas. PP strengthens the evolutionary links that living great apes may offer to better understand the origins of these progressive parts of the brain. Evidence mounts for the stable expression of a neural foundation for language in species that we recently shared a common ancestor with. © 2005 Wiley-Liss, Inc. Key words: brain language areas; evolution; polymodal language; primates; dyslexia; comparative neurobiology; great apes Abbreviations: AG, angular gyrus; CS, central sulcus; cm, cen- *Correspondence to: Patrick J. Gannon, Department of Otolar- timeters; G-V, gestural visual communication; HG, Heschl’s gy- yngology, Annenberg 10 (1189), Mount Sinai School of Medicine, rus; HlSF, horizontal limb of the sylvian fissure (lateral fissure); 5th Avenue at 100th Street, New York, NY 10029. Fax: 212-831- IP, inferior parietal gyrus; L, left hemisphere; PCS, postcentral 3700. E-mail: [email protected] sulcus; parSF, posterior ascending ramus (limb) of the sylvian Received 16 August 2005; Accepted 17 August 2005 fissure; pdrSF, posterior descending ramus (limb) of the sylvian fissure (lateral fissure); SMG, supramarginal gyrus; SyP, sylvian DOI 10.1002/ar.a.20256 point; STG, superior temporal gyrus; V-A, vocal auditory commu- Published online 7 October 2005 in Wiley InterScience nication. (www.interscience.wiley.com). © 2005 WILEY-LISS, INC. GREAT APE BRAIN LANGUAGE AREAS 1129 The evolutionary origin of human brain language areas evolutionary foundation of neural specializations for com- is an issue that has captured the interest of many groups munication, or species-specific language in nonhuman pri- of scientists, in particular comparative and paleoneurolo- mates. Here we have continued our comparative anatomic gists, physical anthropologists, primatologists, linguists, analysis of brain language areas in representatives of and paleolinguists. Some have addressed this subject by closely related nonhuman primates, the great apes. Ana- studying the human fossil record to capture the only direct tomic indicators of traditional human-like brain language evidence from human ancestors (Holloway, 1976, 1983; areas such as the sylvian fissure, Heschl’s gyrus, the areas Tobias, 1987; Tattersall, 2004). In this report, we have of Wernicke and Broca, and the plana temporale and used the comparative approach to assess the anatomic parietale may allow us to build a platform on which the representation of a newly described area of the brain, the cross-specific neurobiological origins of language can be planum parietale, which is thought to be involved with logically reconstructed. As we review some of these ana- polymodal language functions in humans. First we will tomic indicators and examples of the functions and disor- briefly review current thinking of some key components in ders that help characterize them in humans, the subse- the comparative functional anatomy armamentarium for quent step to a comparative link is inherently speculative. evolutionary origins of brain language areas, the sylvian However, in many cases, new avenues of exploration such fissure, the planum temporale, and the planum parietale. as novel behavioral paradigms or utilization of functional The comparative approach has proven to be a useful imaging (PET or MRI) in living nonhuman primates may complement to assess the expression and transition of key be strongly indicated to provide functional correlates of neural elements within an evolutionary framework. Using anatomic homologs. this approach, the expression of human-like features in homologous brain regions of primates may indicate that a Sylvian Fissure precursor condition was present in a common ancestor A wealth of information has been derived from reports possibly many millions of years ago. However, the com- of the symmetry vs. asymmetry status of the sylvian fis- parative approach also recognizes the fact that evolution sure that adjoins receptive brain language area homologs is based on the concept of a foundation that underlies a in hominoids and other primates. As stated by LeMay subsequent species-specific and progressive building plan. (1976): “The most striking and consistently present cere- As such, homologous brain regions, although similarly bral asymmetries found in adult and fetal brains are in rooted, may have adapted differently to encompass the the region of the posterior end of the sylvian fissures—the unique form of the communication demands within other- areas generally regarded as being of major importance in wise closely genetically related species. language function.” A study of humans demonstrated that At the higher cognitive level, the key research issues are sylvian fissure (SF) LϾR asymmetry was present in al- not related to whether complex vocal-auditory (V-A; spo- most 70% of brains (Rubens et al., 1976). This pronounced ken-heard) or gestural-visual (G-V; gestured/signed/writ- asymmetry, although present in newborns (Witelson and ten-seen) language is unique to humans since of course it Pallie, 1973), becomes progressively pronounced through is. Evolutionarily, the seminal question, at least for homi- adolescence to adulthood and may be related to later ex- noids, is when might the neural foundation have become pression of cognitive advancements during maturation specialized to conduct lateralized higher-order associative (Sowell et al., 2002). This developmental occurrence has processing of V-A, G-V, or even polymodal communication. yet to be studied in great apes. One of the earliest com- This is particularly compelling since functional activation parative studies of the cerebral cortex of great apes and of human brain language areas seems to be equipotential New and Old World monkeys showed no consistent pat- across modalities (Emmorey et al., 2003). tern of SF asymmetry in apes where it was longer on the A recent timely review and synthesis (Hauser et al., right in orangutans but on the left in chimpanzees (Cun- 2002) dealt with these important issues by separating the ningham, 1892). Another comparative report demon- communicative repertoire of humans and nonhuman pri- strated that although humans showed marked leftward mates into two major categories, the faculty of language in asymmetry of the SF, chimpanzees did also but to a lesser the broad sense (FLB) and the narrow sense (FLN) (see degree, whereas macaques showed no asymmetry (Yeni- also Pinker and Jackendoff, 2005). FLN alone was consid- Komshian and Benson, 1976). Similarly, it was reported ered human-like since it involves recursive processes that that this condition was present in great apes, particularly provide “the capacity to generate an infinite range of ex- common in orangutans and not surprisingly also in “fossil pressions from a finite set of elements,” which may per- man” (LeMay, 1976). Our more recent studies of the syl- haps represent interpretations of Chomsky’s (1975) ear- vian fissure and the planum temporale (PT) area homolog lier compelling theories of the language organ and (area Tpt) in two species of Old World monkeys showed transformational grammar, in broader, more utilizable that although there were no asymmetries at the gross comparative terms. More recently, a newly conceptualized anatomic level that would indicate leftward predominance perspective on the human language organ was presented of the homolog, there were significant LϾR asymmetries (Anderson and Lightfoot, 2000). However, here we use the and heterogeneity at the cytoarchitectonic level (Gannon standard Merriam-Webster dictionary definition of lan- et al., 1999, 2001a, 2001b; Kheck et al., 2000). guage as “a systematic means of communicating ideas or It is well accepted that in humans
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