Tool-use and the Chimpanzee Brain: An Investigation of Gray and White Matter, and a Focused Study of Inferior Parietal Microstructure by Laura Denise Reyes A.B. in Psychology, June 2008, Dartmouth College M.A. in Anthropology, May 2011, New Mexico State University M.Phil in Hominid Paleobiology, June 2013, The George Washington University A Dissertation submitted to The Faculty of The Columbian College of Arts and Sciences of The George Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy August 31, 2017 Chet C. Sherwood Professor of Anthropology The Columbian College of Arts and Sciences of The George Washington University certifies that Laura D. Reyes has passed the Final Examination for the degree of Doctor of Philosophy as of May 3, 2017. This is the final and approved form of the dissertation. Tool-use and the Chimpanzee Brain: An Investigation of Gray and White Matter, and a Focused Study of Inferior Parietal Microstructure Laura Denise Reyes Dissertation Research Committee: Chet C. Sherwood, Professor of Anthropology, Dissertation Director Kimberley Phillips, Professor of Psychology, Trinity University, Committee Member Scott Mackey, Assistant Professor of Psychiatry, University of Vermont, Committee Member ii © Copyright 2017 by Laura Denise Reyes All rights reserved. iii Acknowledgments The author would like to thank her parents, Loretta and Francisco Reyes; her grandparents, Celia and Ralph Lopez and Paula and Francisco Reyes; and all of her family and friends who offered support during the course of her education, especially Amelia Villaseñor and Chrisandra Kufeldt. The author acknowledges the dissertation committee, Brenda Bradley (Chair), Chet Sherwood (Advisor), David Braun, Scott Mackey, Kimberley Phillips, and Sarah Shomstein, as well as the following funding sources: National Science Foundation Doctoral Dissertation Research Improvement Grant BCS-1455629 and GWU Provost’s Fellowship. iv Abstract of Dissertation Tool-use and the Chimpanzee Brain: An Investigation of Gray and White Matter, and a Focused Study of Inferior Parietal Microstructure The goal of this dissertation is to investigate neural correlates of tool-use in chimpanzees and provide the groundwork for comparisons with humans and other primates. The dissertation contains three studies that integrate different techniques to investigate brain structures associated with tool-use in chimpanzees. The first two studies use neuroimaging techniques to investigate gray and white matter differences associated with tool-use performance in a sample of captive chimpanzees. The first study uses tensor-based morphometry to study gray matter, while the second study uses diffusion tensor imaging and tract-based spatial statistics to study white matter tracts. The third study uses histological methods to focus on the microstructure of the inferior parietal lobe in the chimpanzee. This type of integrative approach allows for a comprehensive study of tool-use and how it is linked with specific aspects of chimpanzee cortical anatomy, and can inform our understanding of how the brain evolved and adapted to tool-use and tool-making in hominins. The results from this dissertation show that the chimpanzee brain has specific tracts and areas that are associated with tool-use with distinct patterns of connectivity, similar to what is observed in humans. Chimpanzees, however, appear to rely more on areas involved in sensorimotor processing for tool-use than do humans. Human tool-use may therefore differ from that of chimpanzees in the recruitment of more areas associated with cognitive control and increased connectivity between areas involved in higher order cognitive functions. The additional cortical areas that have been identified in the human IPL that appear to lack chimpanzee homologues also may be essential for tool-related cognition in humans, especially cognition linked with complex processes such as stone tool-making. Investigations of both gray and white matter showed that chimpanzees also have notable sex differences in their neural correlates of tool-use. Male and female chimpanzees may process tool-use differently, and these differences may be linked with previously reported sex differences in tool-use behaviors. v To fully understand evolutionary changes in the brain that occurred in the human lineage since its split from the Pan-Homo last common ancestor, comparative work must be performed between humans and chimpanzees, and especially work that can reveal the structure and function of the chimpanzee brain to ensure the validity of any comparisons. This dissertation has provided a characterization of tool-use in the chimpanzee brain based on multiple modalities, and these results can form the basis of direct comparisons between chimpanzees, humans, and other primate species in the future. vi Table of Contents Acknowledgements.........................................................................................................................iv Abstract of Dissertation....................................................................................................................v List of Figures................................................................................................................................viii List of Tables...................................................................................................................................xi Chapter 1: Introduction.....................................................................................................................1 Chapter 2: Gray Matter and Performance Time on a Tool-use Task in Chimpanzees: An Analysis of Voxel-based Morphometry and Cortical Thickness.......................................................................8 Chapter 3: White Matter Correlates of Tool-use Performance in Chimpanzees Using Tract-Based Spatial Statistics.............................................................................................................................40 Chapter 4: Cyto- and Myeloarchitectural Parcellation of the Chimpanzee Inferior Parietal Lobe........................................................................................61 Chapter 5: Conclusion..................................................................................................................112 References...................................................................................................................................116 vii List of Figures Chapter 2: Gray matter and performance time on a tool-use task in chimpanzees: an analysis of tensor-based morphometry and cortical thickness 1. Plots depicting the distributions of tool-use performance time (log transformed), age at tool-use, and brain volume by sex.............................................................................................27 2. Significant clusters for logJ analysis in females shown in left/right, superior/inferior, and anterior/posterior 3-D renderings, and in axial sections.................................................................28 3. Pearson’s r values for the logJ analysis in females shown in left/right, superior/inferior, and anterior/posterior 3-D renderings, and in axial sections..........................................................29 4. Significant clusters for logJ analysis in males shown in left/right, superior/inferior, and anterior/posterior 3-D renderings, and in axial sections.................................................................30 5. Pearson’s r values for the logJ analysis in males shown in left/right, superior/inferior, and anterior/posterior 3-D renderings, and in axial sections..........................................................31 6. Significant clusters for the cortical thickness analysis in females shown in left/right, superior/inferior, and anterior/posterior 3-D renderings.................................................................32 7. Pearson’s r values for the cortical thickness analysis in females shown in left/right, superior/inferior, and anterior/posterior 3-D renderings.................................................................33 8. Significant clusters for the cortical thickness analysis in males shown in left/right, superior/inferior, and anterior/posterior 3-D renderings.................................................................34 9. Pearson’s r values for the cortical thickness analysis in males shown in left/right, superior/inferior, and anterior/posterior 3-D renderings.................................................................35 10. Clusters in males and females where Pearson’s r shows a medium or larger effect for TBM and cortical thickness results on 3-D rendered brains showing left, right, superior, inferior, anterior, and posterior views.............................................................................................36 11. Clusters from the TBM and cortical thickness analyses where Pearson’s r shows a medium or larger effect for TBM and cortical thickness results on 3-D rendered brains showing left, right, superior, inferior, anterior, and posterior views................................................38 viii Chapter 3: White Matter Correlates of Tool-use Performance in Chimpanzees Using Tract-Based Spatial Statistics 1. Plots depicting the distributions of tool-use performance time (log transformed), age at tool-use, and brain volume by sex..................................................................................................57