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Cross-Species Comparisons of the Retrosplenial Cortex in Primates: Through Time and Neuropil Space

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Cross-Species Comparisons of the Retrosplenial Cortex in Primates: Through Time and Neuropil Space ! ! ! CROSS-SPECIES COMPARISONS OF THE RETROSPLENIAL CORTEX IN PRIMATES: THROUGH TIME AND NEUROPIL SPACE A thesis submitted to Kent State University in partial fulfillment of the requirement for the degree of Master of Arts by Mitch Sumner May, 2013 Thesis written by Mitch Andrew Sumner B.A., Indiana University of Pennsylvania, USA 2009 Approved by: __________________________________________ Dr. Mary Ann Raghanti Advisor __________________________________________ Dr. Richard Meindl Chair, Department of Anthropology __________________________________________ Dr. Raymond A. Craig Associate Dean, Collage of Arts and Sciences ! ii! TABLE OF CONTENTS LIST OF FIGURES ................................................................................................. v LIST OF TABLES ................................................................................................. vi AKNOWLEDGEMENTS ..................................................................................... vii ABSTRACT ......................................................................................................... viii Chapter I. INTRODUCTION ............................................................................. 1 Declarative vs. nondeclarative memory ........................................... 4 Episodic memory and mental time travel in humans ....................... 6 Memory in non-human animals ........................................................ 9 Connectivity and behavior .............................................................. 13 Neuropil space ................................................................................ 15 The role of the retrosplenial cortex ................................................ 17 II. HYPOTHESES ............................................................................... 20 III. MATERIALS AND METHODS ................................................... 22 Specimens ....................................................................................... 22 Histological identification of the retrosplenial cortex .................... 26 Tissue preparation ......................................................................... 26 Data collection ............................................................................... 27 Neuropil fraction ............................................................................ 27 Cell volume .................................................................................... 28 Statistical analysis .......................................................................... 28 IV. RESULTS ....................................................................................... 32 Neuropil fraction ............................................................................ 32 Neuron size ..................................................................................... 33 Regression analysis ........................................................................ 37 V. DISCUSSION ................................................................................. 41 ! iii! Principal Findings ........................................................................... 41 The emergence of mental time travel ............................................. 42 VI. CONCLUSIONS ............................................................................ 45 APPENDIX A. Individual neuropil fractions ....................................................... 47 APPENDIX B. Individual neuron volumes .......................................................... 48 REFERENCES ...................................................................................................... 50 ! iv! LIST OF FIGURES 1. The anatomical position of Brodmann’s areas 29 and 30 .................................. 2 2. An example Nissl stained section of a macaque brain ....................................... 3 3. Classifications of different types of memory ..................................................... 5 4. Phylogeny of the primate species used in this study ........................................ 23 5. Photomicrograph of areas 29 and 30 ............................................................... 24 6. Cytoarchitecture of each area in each species .................................................. 25 7. Example sites selected with fractionator sampling .......................................... 29 8. Example of the conversion method used to calculate neuropil ........................ 30 9. An example of the method used to calculate neuron volume .......................... 31 10. Differences in neuropil space among study species ...................................... 33 11. Differences in neuron volume in area 29 ....................................................... 35 12. Differences in neuron volume in area 30 ....................................................... 36 13. Regression analysis of volume for area 29, layer II and NF area 29 ............. 38 14. Regression analysis of volume for area 29, layer III and NF area 29 ............ 38 15. Regression analysis of volume for area 29, layers V/VI and NF area 29 ...... 39 16. Regression analysis of volume for area 30, layer II and NF area 30 ............. 39 17. Regression analysis of volume for area 30, layer III and NF area 30 ............ 40 18. Regression analysis of volume for area 30, layer V/VI and NF area 30 ....... 40 ! v! LIST OF TABLES 1. Individuals used in this study ........................................................................... 23 2. Neuropil fractions for each species .................................................................. 32 3. Neuron volume for each species ...................................................................... 34 ! vi! ACKNOWLEDGEMENTS First, I would like to thank Dr. Mary Ann Raghanti for support and expert advice while working towards the completion of this project, as well as for being an excellent science role model. I would also like to thank the other members of my committee, Dr. Richard Miendl and Dr. F. Robert Treichler, as well as Dr. Muhammad Spocter, Dr. Chet Sherwood, Chery Stimpson, Dr. Patrick Hof, Dr. Marilyn Norconk, Dr. Linda Spurlock, and Caroline Tannert for not only support and/or science advice, but for generally being incredibly helpful. Finally, a special thanks goes to my friends in the Anthropology department, my family, Aidan Ruth, and Echo the Dog, all of whom provided valuable motivational support during the past two years. ! vii! ABSTRACT Chronesthesia, or mental time travel (MTT), is the ability to be conscious of both past experiences and possible future scenarios. Behavioral studies have demonstrated that some non-human animals are capable of episodic-like memory, yet there exists no scientific consensus on the extent of memory abilities, including complex future thinking or planning, among non-human species. The retrosplenial cortex (Brodmann’s areas 29 and 30) plays a critical role in episodic memory, which is vital for MTT. Because MTT appears to be a uniquely human capacity, this region is of major interest for evolutionary studies. However, comparative neuroanatomical data for these regions are scarce. The goal of the present analysis was to compare neuropil space among capuchins, macaques, chimpanzees, and humans to determine if humans significantly differ from the other species. The amount of neuropil space provides a proxy measure of connectivity because a large component of the neuropil is comprised of dendrites, synapses, and axons. Digital images were analyzed using ImageJ software to obtain a neuropil fraction. The results showed significantly higher neuropil fractions in humans relative to the other species examined. Further analysis showed that this difference could not be attributed to a decrease in cell volume. These results demonstrate a unique neuroanatomical reorganization of the human retrosplenial cortex. If it is true that an increase in neuropil space is indicative of an increase in connectivity, then it may be that this is a neuroanatomical substrate that evolved to support complex mental time travel in humans. ! viii! ! CHAPTER ONE Introduction The ability to contemplate the future and reflect on past events, referred to as chronesthesia or mental time travel, has been hypothesized to be a uniquely human capacity (Tulving, 2002a). The emergence of mental time travel would have provided our ancestors with significant behavioral advantages in terms of anticipating and planning for the future, likely having a significant impact on the survivorship of our species. Behavioral studies have demonstrated that some non-human primates and other animals seem to be capable of episodic-like memory (Schwartz and Evans, 2001; Correia, Sérgio P. C. et al., 2007), yet there exists no scientific consensus on the extent of these memory abilities, including complex future thinking or planning, among non-human species. The neuroanatomical substrates that support mental time travel are of evolutionary interest yet comparative data for the brain areas associated with these functions are sparse. To address this paucity of data, the present study used microscope-based image analysis techniques and advanced stereology to conduct a comparative examination of the retrosplenial cortex (i.e., Brodmann’s areas 29 and 30; Figures 1 and 2) (Brodmann, 1909), based on evidence of its role in the network of areas responsible for mental time travel (Addis et al., 2007; Botzung et al., 2008; Suddendorf, 2009; Vann et al., 2009). Neuropil, the space
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