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Identification of in Io Sulci on the External Surface of Eight Dult Chimpanzee Brains

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Identification of in Io Sulci on the External Surface of Eight Dult Chimpanzee Brains )ORULGD6WDWH8QLYHUVLW\/LEUDULHV 2018 Identification of In Vivo Sulci on the External Surface of Eight Adult Chimpanzee Brains: Implications for Interpreting Early Hominin Endocasts Dean Falk, Christoph Zollikofer, Marcia Ponce de León and Katerina Semendeferi This is the accepted manuscript of the article published by Brain, Behavior and Evolution and can be found at https://doi.org/10.1159/000487248. © 2018 S. Karger AG, Basel Follow this and additional works at DigiNole: FSU's Digital Repository. For more information, please contact [email protected] 1 Identification of In Vivo Sulci on the External Surface of Eight Adult Chimpanzee Brains: 2 Implications for Interpreting Early Hominin Endocasts 3 Dean Falk1,2, Christoph P. E. Zollikofer3, Marcia Ponce de León3, Katerina Semendeferi4, José 4 Luis Alatorre Warren3, William D. Hopkins5,6 5 6 1Department of Anthropology, Florida State University, Tallahassee, Florida 7 2 School for Advanced Research, Santa Fe, New Mexico 8 3 Anthropological Institute, University of Zurich, Zurich, Switzerland 9 4 Department of Anthropology, University of California San Diego, La Jolla, California 10 5 Neuroscience Institute, Georgia State University, Atlanta, Georgia 11 6 Division of Developmental and Cognitive Neuroscience, Yerkes National Primate Research 12 Center, Atlanta, Georgia 13 14 Short title: Sulci on eight chimpanzee brains 15 16 Number of figures: five 17 18 Number of tables: one 19 20 Keywords 21 Annectant gyri. Arcuate fasciculus. Australopithecines. Broca’s area. Chimpanzee brains. 22 Cortical sulci. Hominin endocasts. Language evolution. Lunate sulcus. 23 24 Corresponding author’s contact information 25 Dean Falk, SAR, 660 Garcia St., Santa Fe, NM 87505; USA 26 Phone: 850-339-3877; fax: 505-954-7235; email: [email protected] or [email protected] 27 28 29 30 Abstract 1 31 The only direct source of information about hominin brain evolution comes from the fossil 32 record of endocranial casts (endocasts) that reproduce details of the external morphology of the 33 brain imprinted on the walls of the braincase during life. Surface traces of sulci that separate the 34 brain’s convolutions (gyri) are reproduced sporadically on early hominin endocasts. 35 Paleoneurologists rely heavily on published descriptions of sulci on brains of great apes, 36 especially chimpanzees (humans’ phylogenetically closest living relatives), to guide their 37 identifications of sulci on ape-sized hominin endocasts. However, the few comprehensive 38 descriptions of cortical sulci published for chimpanzees usually relied on post mortem brains, 39 (now) antiquated terminology for some sulci, and photographs or line drawings from limited 40 perspectives (typically right or left lateral views). The shortage of adequate descriptions of 41 chimpanzee sulcal patterns partly explains why identities of certain sulci on australopithecine 42 endocasts (e.g., the inferior frontal and middle frontal sulci) have been controversial. Here, we 43 provide images of lateral and dorsal surfaces of 16 hemispheres from four male and four female 44 adult chimpanzee brains that were obtained using in vivo magnetic resonance imaging. Sulci on 45 the exposed surfaces of the frontal, parietal, temporal, and occipital lobes are identified on the 46 images, based on their locations, positions relative to each other, and homologies known from 47 comparative studies of cytoarchitecture in primates. These images and sulcal identifications 48 exceed the quantity and quality of previously published illustrations of chimpanzee brains with 49 comprehensively labeled sulci and, thus, provide a larger number of examples for identifying 50 sulci on hominin endocasts than hitherto available. Our findings, even in a small sample like the 51 present one, overturn published claims that australopithecine endocasts reproduce derived 52 configurations of certain sulci in their frontal lobes that never appear on chimpanzee brains. The 53 sulcal patterns in these new images also suggest that changes in two gyri that bridge between the 54 parietal and occipital lobes may have contributed to cortical reorganization in early hominins. It 55 is our hope that these labeled in vivo chimpanzee brains will assist future researchers to identify 56 sulci on hominin endocasts, which is a necessary first step in the quest to learn how and when the 57 external morphology of the human cerebral cortex evolved from apelike precursors. 58 59 Introduction 60 Two major trends characterized hominin brain evolution: Brains enlarged over time and their 61 circuitry and cellular composition became more complex (neurological reorganization). 62 Estimates of brain sizes are obtained relatively easily by measuring the volumes of braincases 63 (cranial capacities). Research on neurological reorganization is more challenging because it 64 entails analyzing subtle details of gyral bulges and sulci that became imprinted on the inner walls 65 of braincases when animals were still alive [Jerison, 1973]. These impressions are reproduced 66 on internal casts of braincases (endocasts). Endocasts sometimes form naturally after animals 67 die, or they may be prepared manually by casting empty skulls or constructed virtually from 68 computerized tomography (CT) scans of fossilized skulls [Falk, 2004]. 69 The quality of cortical imprints on endocasts varies with species (smaller-brained species 70 within lineages yield more detailed endocasts than their larger-brained relatives [Radinsky, 71 1972]), developmental age (endocasts from juveniles generally reproduce more details than those 72 from mature individuals) [Connolly, 1950; Minh and Hamada, 2017], and (in the case of fossils) 2 73 geological conditions that affect preservation. The fidelity of sulcal reproduction on endocasts 74 varies with region of the brain (Minh and Hamada, 2017), as illustrated by a study that compared 75 traces of sulci reproduced on endocasts from six chimpanzees with the sulci on corresponding 76 brains, and found that some sulci (e.g., the fronto-orbital sulcus [fo]) reproduced well, while 77 others (e.g., the lunate [L]) did not [Clark et al., 1936]. 78 There are currently two prevailing hypotheses about the mechanisms that govern the 79 formation of sulci during fetal development. The axon tension hypothesis posits that species- 80 specific sulcal patterns are caused by tension along axons in subcortical white matter [Van 81 Essen, 1997]. The mechanical folding model, on the other hand, suggests that tangential 82 expansion of the cerebral cortex generates compression that leads to the development of cortical 83 sulci [Tallinen et al., 2016]. A recent study of developing cortex in rhesus monkey fetuses 84 suggests that maturation of dendrites within the cortex may be linked to the formation of sulci, 85 which may be more consistent with the mechanical folding model [Wang et al., 2017]. Although 86 these discussions about the mechanisms of how sulci form during development may seem 87 somewhat tangential to the present paper, the shape of the developing brain (endocast) modulates 88 the mechanical factors that influence the placement and orientations of sulci so that, in real 89 brains, the “primary convolutions are consistently reproducible in their location” (Tallinen et al., 90 2016:591). It is important to note, however, that the only information about sulci that can be 91 gleaned from primate, including hominin, endocasts depends on superficial traces [Pearce et al., 92 2013], which are often fragmentary. 93 Because chimpanzees are the closest living phylogenetic relatives of humans, 94 descriptions of their brains have traditionally been important for identifying sulci on 95 australopithecine endocasts [Clark et al., 1936; Dart, 1925; Falk, 2009] and comparison of 96 chimpanzee and human brains remains essential for addressing brain evolution in hominins since 97 the two groups split from a common ancestor [Gómez-Robles et al., 2015; Semendeferi et al., 98 1997, 2011]. The literature on chimpanzee brains prior to and during the first half of the 20th 99 century focused mostly on individual brains [e.g., Benham and Oxoii, 1895], although a few 100 studies included relatively large samples of chimpanzees [reviewed in Walker and Fulton, 1936]. 101 Early authors relied exclusively on post mortem brains, used terminology that is now outdated, 102 failed to recognize important sulci such as the middle frontal (fm) sulcus and Affenspalte (lunate 103 sulcus, L), and illustrated specimens with photographs or line drawings from limited perspectives 104 (typically right or left lateral views) [e.g., Mingazzini, 1928; Walker and Fulton, 1936]. Bailey 105 et al.’s important 1950 monograph, The Isocortex of the Chimpanzee, was an improvement over 106 earlier reports because it emphasized that sulcal homologies should be based on their 107 approximate relations to cytoarchitectural areas, and used modern terminology and correct 108 identifications for sulci. Although Bailey et al. provided line drawings that illustrated and 109 labeled the sulci for one generic left chimpanzee hemisphere [1950:18-19, Fig. 4a,b,c], they did 110 not include illustrations of individual chimpanzee brains with comprehensively labeled sulci. 111 John Connolly advanced knowledge of chimpanzee (and other primate) sulci in his 112 seminal 1950 monograph, External Morphology of the Primate Brain. Connolly’s identifications 113 of homologous primate sulci relied heavily on comparisons of brains across the primate order in 114 light of cytoarchitectonic
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