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Edler Thesis A COMPARATIVE ANALYSIS OF HIPPOCAMPUS SIZE AND ECOLOGICAL FACTORS IN PRIMATES A thesis submitted to Kent State University in partial fulfillment of the requirements for the degree of Master of Arts by Melissa Edler August 2007 Thesis written by Melissa Edler B.A., Kent State University, 2000 M.A., Kent State University, 2007 Approved by Dr. Chet C. Sherwood, Advisor Dr. Richard S. Meindl, Chair, Department of Anthropology Dr. John R. D. Stalvey, Dean, College of Arts and Sciences ii TABLE OF CONTENTS LIST OF FIGURES…………………………………………………………………… v LIST OF TABLES……………………………………………………………………. vii ACKNOWLEDGEMENTS…………………………………………………………… ix Chapter I. INTRODUCTION………………………………………………………… 1 Overview…………………………………………………………………... 1 Role of the Hippocampus in Memory………………………………........... 2 Spatial Memory……………………………………………………………. 7 Place Cells…………………………………………………………………. 9 Spatial View Cells…………………………………………………………. 12 Use of Spatial Memory in Foraging…………………………………....….. 17 Cognitive Adaptations to the Environment………………………………... 21 II. METHODS………………………………………………………………... 26 Species Analyses…………………………………………………………... 31 Independent Contrast Analyses……………………………………………. 33 III. RESULTS………………………………………………………………….. 37 Percentage of Frugivorous Diet……………………………………………. 37 Percentage of Folivorous Diet……………………………………………... 39 Percentage of Insectivorous Diet…………………………………………... 42 iii Home Range……………………………………………………………….. 44 Diurnal Activity Pattern……………………………………………………. 47 Nocturnal Activity Pattern…………………………………………….….... 48 Arboreal Habitat……………………………………………………………. 49 Semi-Terrestrial Habitat……………………………………………………. 50 Terrestrial Habitat………………………………………………………….. 51 IV. DISCUSSION……………………………………………………………… 52 Diet and Hippocampus Volume……………………………………………. 52 Home Range and Hippocampus Volume…………………………………… 56 Activity Patterns and Hippocampus Volume………………………………. 59 Habitats and Hippocampus Volume……………………………………….. 61 V. CONCLUSION…………………………………………………………….. 65 REFERENCES………………………………………………………………………..... 67 iv LIST OF FIGURES Figure 1: Hippocampus and Surrounding Cortices…………………………………… 3 Figure 2: Information Flow through Medial Temporal Lobe………………………… 4 Figure 3: Odor Discrimination Test………………………………………………….. 6 Figure 4: Radial Arm Maze Test……………………………………………………... 8 Figure 5: Place Cells in the Hippocampus…………………………………………… 10 Figure 6: Microcircuits of the Hippocampus…………………………………………. 16 Figure 7: Phylogenetic Tree for Primates……………………………………………... 36 Figure 8: Plot of Log Hippocampus Volume versus Percentage of Frugivorous Diet…………………………………………………………….. 38 Figure 9: Plot of Hippocampus Residual from Medulla Oblongata versus Percentage of Frugivorous Diet……………………………………… 38 Figure 10: Plot of Hippocampus/Medulla Oblongata Ratio versus Percentage of Frugivorous Diet…………………………………………….. 39 Figure 11: Plot of Log Hippocampus Volume versus Percentage of Folivorous Diet……………………………………………………………… 40 Figure 12: Plot of Hippocampus Residual from Medulla Oblongata versus Percentage of Folivorous Diet……………………………………….. 41 Figure 13: Plot of Hippocampus/Medulla Oblongata Ratio versus Percentage of Folivorous Diet………………………………………………. 41 v Figure 14: Plot of Log Hippocampus Volume versus Percentage of Insectivorous Diet…………………………………………… 43 Figure 15: Plot of Hippocampus Residual from Medulla Oblongata versus Percentage of Insectivorous Diet…………………………………… 43 Figure 16: Plot of Hippocampus/Medulla Oblongata Ratio versus Percentage of Insectivorous Diet…………………………………………… 44 Figure 17: Plot of Log Hippocampus Volume versus Log Home Range…………….. 46 Figure 18: Plot of Hippocampus Residual from Medulla Oblongata versus Log Home Range……………………………………………………. 46 Figure 19: Plot of Hippocampus/Medulla Oblongata Ratio versus Log Home Range…………………………………………………………… 47 Figure 20: Plot of Log Body Mass versus Percentage of Frugivorous Diet…………. 54 vi LIST OF TABLES Table 1: Raw Data Values for Hippocampus and Medulla Volumes, Home Range Areas, Diet, Activity Pattern and Habitat .....………………… 27 Table 2: Correlation Values between Hippocampus Volume and Percentage of Frugivorous Diet………………………………………… 37 Table 3: Correlation Values between Hippocampus Volume and Percentage of Folivorous Diet………………………………………….. 40 Table 4: Correlation Values between Hippocampus Volume and Percentage of Insectivorous Diet……………………………………….. 42 Table 5: Correlation Values between Hippocampus Volume and Home Range……… 45 Table 6: Correlation Values between Hippocampus Volume and Diurnal Activity Pattern………………………………………………… 48 Table 7: Correlation Values between Hippocampus Volume and Nocturnal Activity Pattern……………………………………………… 49 Table 8: Correlation Values between Hippocampus Volume and Arboreal Habitat….. 50 Table 9: Correlation Values between Hippocampus Volume and Semi-Terrestrial Habitat………………………………………………… 51 Table 10: Correlation Values between Hippocampus Volume and Terrestrial Habitat………………………………………………………. 51 vii Table 11: Correlation Values between Hippocampus Volume and Home Range after Removing Frugivorous-Insectivores…………………………………… 59 viii ACKNOWLEDGEMENTS I thank Dr. Chet Sherwood for serving as my advisor all the way from Washington, D.C. Thanks also goes to Dr. Chris Vinyard for taking the time to help me learn Mesquite and making sure that I grasped the statistical analyses. I thank Dr. Owen Lovejoy for agreeing to serve on my thesis committee. In addition, thanks to Dr. Emmanuel Gilissen for allowing me to use much of the primate socio-ecological data he previously gathered. I thank Marianne Blankenship for finding an old MacIntosh that would support CAIC and the techies who rigged it to work on a classic operating system. I thank my family, especially my Mom, and friends for their support, encouragement and a kick in the butt when it was needed along the way. Finally, I thank my husband Ryan who surrendered his wife for many months to the thesis monster and who cooked dinner, cleaned house and washed laundry to allow me time to work on my thesis. ix CHAPTER I: INTRODUCTION Overview An animal’s ecological surroundings can provide clues to its morphology. For instance, various areas of the mammalian brain have been shown to adapt in response to environmental influences (Eisenberg and Wilson, 1978; Barton et al., 1995; Hutcheon et al., 2002). One well-studied example is the hippocampus, known for its role in spatial memory, which selectively increases in response to environmental pressures in animals such as birds, rodents, bats and humans (Krebs et al., 1989; Jacobs et al., 1990; Safi and Dechmann, 2005; Maguire et al., 2000). Whether a similar relationship exists between the primate hippocampus and environment has yet to be examined. The goal of this study is to determine whether variation in primate hippocampal size is related to environmental factors, such as diet (frugivory, folivory or insectivory), home range size, activity pattern (diurnal or nocturnal) and habitat (arboreal, semi- terrestrial or terrestrial). Based on results from prior studies, this current analysis tests the following hypotheses: Hypothesis 1: Primates with a higher percentage of frugivory in their diet should have larger hippocampi than those with a higher percentage of folivory or 1 2 insectivory in their diet (Clutton-Brock and Harvey, 1980; Harvey et al., 1980; Safi and Dechmann, 2005). Hypothesis 2: As home range size increases, hippocampus volume also should increase in primates due, in part, to its role in spatial memory (Clutton-Brock and Harvey, 1977; Clutton-Brock and Harvey, 1980; Harvey et al., 1980). Hypothesis 3: Hippocampus volume size should not differ significantly between diurnal and nocturnal primates (Clutton-Brock and Harvey, 1980; Bicca-Marques and Garber, 2004). Hypothesis 4: Arboreal primates view space three-dimensionally and rely more heavily on spatial abilities than terrestrial primates, thus arboreal primates should have larger hippocampal size than terrestrial primates (Russon, 2002). Role of the Hippocampus in Memory Located in the medial temporal lobe, the hippocampal formation comprises the perirhinal, entorhinal, and parahippocampal cortices and the rhinal sulcus (see Figure 1). In primates, major input connections to the hippocampus come from association areas of the cerebral cortex, including the parietal cortex, the temporal lobe’s visual and auditory areas and the frontal cortex, and the hippocampus supplies outputs to the fornix and cerebral cortex via the subiculum, entorhinal cortex and parahippocampal gyrus (see Figure 2) (Van Hoesen, 1982; Amaral, 1987; Suzuki and Amaral, 1994; Rolls, 1999). 3 Figure 1. The brain is sectioned coronally showing the hippocampus and its surrounding cortices. (Source: Bear et al., 1996) The hippocampus plays a large role in memory and learning. Two main theories exist concerning the role of the hippocampus in memory. The episodic theory of hippocampal function suggests that the hippocampus plays a selective role in episodic memory, which involves the capacity to remember specific personal experiences and detailed series of events, with little or no contribution to semantic memory, that of facts and world knowledge (Vargha-Khadem et al., 1997; Fujii et al., 2000). In contrast, the declarative theory of medial temporal lobe function argues that the hippocampus, along with surrounding cortices, contributes to both semantic and episodic memory. This view is supported by a large body of similar findings from studies in human amnesic patients (Manns and Squire, 2002; Squire and Zola, 1998). Scoville and Milner (1957) were the first to hypothesize that hippocampal damage might be
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