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Laboratory for Comparative Human Biology
James K. Rilling

Areas of Interest
comparative primate neurobiology and primate brain evolution; neurobiology of primate social behavior; psychoneuroendocrinology

Research
My original research in the Laboratory for Comparative Human Biology was motivated by an interest in hormonal influences on human thought and behavior, particularly the role of androgens in aggression. Since only non-SHBG bound testosterone is freely available to tissues (including the brain), we thought it important to utilize a measure that reflected free testosterone levels. In collaboration with Ben Campbell, we compared testosterone levels in matching salivary and blood spot samples obtained from Zimbabwean males at various stages of pubertal development. We also developed a blood spot assay to measure SHBG levels in these samples. Our results showed an inverse correlation between SHBG levels and the proportion of plasma testosterone recovered in saliva, supporting the idea the non-SHBG fraction has preferential access to the salivary gland. This observation suggested that salivary T bettter reflects bioavailable T. However, plasma testosterone levels were more effective than salivary levels in distinguishing among subjects at various stages of genital development (based on self-reported Tanner genital stage ratings). The latter observation suggests that plasma T levels provide a better indication of T bioavailability. Thus, we concluded that neither measure is clearly superior to the other as an index of T bioavailability.

My interest in the biological basis of behavior led me to study the brain for my disseration research. My dissertation project was a comparative study of anthropoid primate neuroanatomy using Magnetic Resonance Imaging. Whole brain MRI scans were obtained from 44 living anthropoid primate subjects across 11 species. The size of various brain structures were measured and compared across species to determine whether the internal proportions of the human brain correspond with predictions based on non-human primate allometric trajectories. This study produced four results that I feel are of interest to the field:

  1. The surface area of the corpus callosum does not keep pace with increases in cortical surface area across our sample of anthropoid primates. Therefore, as brain size increases, the surface containing interhemispheric connections does not increase in size as much as the surface containing the neuronal elements to be connected. Hence, larger brains, like the human brain, may have relatively less interhemispheric connectivity. This might constitute the anatomical basis for the pronounced laterality of the human brain.
  2. The human neocortex (gray matter, white matter, or their combined total) is significantly larger than expected for a typical anthropoid primate of the same brain size; that is, humans depart from non-human primate allometric trends, implying that natural selection displaced us from that constraint throughout human evolution. Not only did the brain enlarge throughout human evolution, it was also reorganized so that its internal proportions were modified away from the "typical" anthropoid pattern.
  3. As brains increase in size, the cortex predictably becomes more convoluted. Our data show that overall the human brain has the degree of gyrification expected for a primate of our brain size. However, in one specific region of the brain (a coronal slice cutting through the prefrontal cortex), the human brain is significantly more gyrified than predicted by non-human anthropoid allometric trends. This is an intriguing observation given the role of the prefrontal cortex in many of our higher cognitive functions (social intelligence, planning, symbolic thinking, working memory, executive function).
  4. The cerebellum of apes is about 45% larger than the cerebellum of monkeys after the effect of overall brain size is removed. When cerebellar volume is regressed on brain volume, apes and monkeys lie along roughly parallel lines in which the ape line has a higher y-intercept than the monkey line. This observation could be linked with the emphasis on brachiation in apes (a form of locomotion which is absent in our monkey sample). Alternatively, in view of new evidence that the cerebellum is involved in higher cognitive function in humans, it could be related to cognitive skills that apes possess to a greater extent than monkeys.
Currently, I am a postdoctoral fellow in the Department of Psychiatry and Behavioral Sciences at emory University in the laboratory of Dr. Clinton Kilts. The fellowship involves training in the design and methods of functional neuroimaging experiments (Positron Emmission Tomography and functional MRI). My main goal in this fellowship is to use functional neuroimaging techniques to investigate the neurobiological basis of primate social behavior. This is possible because the tracer (radioactive deoxyglucose) used in these experiments gets trapped inside neurons for at least 45 minutes so that PET images acquired after a social behavioral episode (in an anesthetized subject) reflect brain activity that took place during that episode. I am currently involved in a PET study of juvenile rhesus monkeys for which the goal is to identify brain regions that show increased metabolic activity in response to the stress of an acute separation from their mothers. I am also involved with a study that seeks to determine whether langauge competent chimpanzees (from the Language Research center at Georgia State University) process language using the same neurological circuits that humans use (i.e., Broca's and Wernicke's areas). This study should inform our knowledge of human brain evolution from a functional perspective, and allow us to answer questions like: when did the neurological substrate for language evolve? Was it already present in the common ancestor of humans and great apes, or did it uniquely evolve in the hominid lineage?

In the coming year or two, I hope to return to the issue I first began researching in the Laboratory for Comparative Human Biology, namely aggressive behavior and the emotions that underlie it (sexual jealousy, pride, etc.). I hope to use PET imaging to investigate the neurobiological basis of male-female aggression in rhesus macaques, using this as a model for domestic violence in humans.

Publications
in press James K. Rilling and Thomas R. Insel. Differential expansion of neural projection systems in primate brain evolution. NeuroReport.
in press James K. Rilling and Thomas R. Insel. The Human Neocortex in Comparative Perspective Using Magnetic Resonance Imaging. Journal of Human Evolution.
1998 James K. Rilling and Thomas R. Insel. Evolution of the Primate Cerebellum: differences in relative volume among monkeys, apes and humans. Brain, Behavior and Evolution 52: 308-314.
1998 Mar M. Sanchez, Elizabeth F. Hearn, Dung Do, James K. Rilling, James G. Herndon, and Thomas R. Insel. Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys. Brain Research 812:38-49.
1998 William H. Hopkins, Lori Marino, James K. Rilling, and L. MacGregor. Planum temporale asymmetries in Great apes but not in lesser apes. Neuroreport 9:2913-2918.
1996 James K. Rilling, Carol M. Worthman, Benjamin C. Campbell, Joy F. Stallings, Michael Mbizvi. Ratios of plasma and salivary testosterone throughout puberty: production vs. bioavailability. Steroids 61:374-378.
1992 Thaddeus G. Golos, Richard R. Handrow, Maureen Durning, Jennifer M. Fischer, and James K. Rilling. Regulation of Chorionic Gonadotropin-alpha and Chorionic Somatomammotropin Messenger Ribonucleic Acid Expression by 8-Bromo-Adenosin 3', 5'-Monophosphate and Dexamethasone in Cultured Rhesus Monkey Syncytiotrophoblasts. Endocrinology 131 (1): 89-100.

Abstracts
1999 J.K. Rilling and Thomas R. Insel. Evolution of neocortical size and gyrification in hominids: evidence from comparative neuroanatomy. American Journal of Physical Anthropology Suppl. Paper presented at the 1999 annual meeting of the American Association of Physical Anthropologists.
1998 J.K. Rilling and Thomas R. Insel. Differential expansion of neural projection systems in primate evolution. Society for Neuroscience Abstracts.
1997 James K. Rilling. Aggressive Behavior Among Men: Biological Underpinnings. Paper presented at the annual meeting of the American Anthropological Association.
1997 Mar M. Sanchez, Elizabeth F. Hearn, James Rilling, Thomas R. Insel, Paul M. Plotsky. The hypothalamo-pituitary-adrenal function and behaviour in infant rhesus monkeys: effects of differential rearing. Psychneuroendocrinology 22 (Suppl :2) :S198.
1997 M.M. Sanchez, E. Hearn, J. Rilling, D. Do, J.G. Herndon and T.R. Insel. Rearing condition alters cognitive function and corpus callosum size in infant rhesus monkeys. Society for Neuroscience Abstracts.
1997 J.K. Rilling, K. Semendeferi, H. Damasio, and T.R. Insel. The Human neocortex in comparative perspective using magnetic resonance imaging. American Journal of Physical Anthropology Suppl. 24:197. Paper presented at the 1997 annual meeting of the American Association of Physical Anthropologists.
1997 K. Semendeferi, H. Damasio, J. Rilling, and T. Insel. The volume of the cerebral hemispheres , frontal lobes, and cerebellum in living humans and apes using in vivo magnetic resonance morphometry. American Journal of Physical Anthropology Suppl. 24: 208. Poster presented at the 1997 annual meeting of the American Association of Physical Anthropologists.
1996 James K. Rilling. Migration Stress, pathogen pressure and illness. American Journal of Physical Anthropology Suppl. 22: 198. Paper presented at the 1996 annual meeting of the American Association of Physical Anthropologist.
1996 Thomas W. McDade, Carol M. Worthman, James K. Rilling, Joy F. Stallings, and Adrian Angold. Stress, depression, and immune function in American adolescents American Journal of Physical Anthropology Suppl. 22:162. Paper presented at the 1996 annual meetings of the American Association of Physical Anthropologists.
1994 J. Rilling, B.C. Campbell, J.F. Stallings, and C. M. Worthman. Ratios of plasma and salivary testosterone throughout puberty: production vs. bioavailability. American Journal of Physical Anthropology Suppl. 18:170. Poster presented at the 1994 annual meeting of the American Association of Physical Anthropologists.


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