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Comparative Primate Neuroimaging: Insights Into Human Brain Evolution

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Review Comparative primate neuroimaging: insights into human brain evolution 1,2,3,4 James K. Rilling 1 Department of Anthropology, Emory University, Atlanta, GA 30322, USA 2 Department of Psychiatry and Behavioral Sciences, Emory University, Atlanta, GA 30322, USA 3 Yerkes National Primate Research Center, Emory University, Atlanta, GA 30322, USA 4 Center for Translational Social Neuroscience, Emory University, Atlanta, GA 30322, USA Comparative neuroimaging can identify unique features We have extensive knowledge of rhesus macaque brain of the human brain and teach us about human brain anatomy and physiology obtained through lesion studies, evolution. Comparisons with chimpanzees, our closest single-cell electrophysiology, and tracer studies. Similar living primate relative, are critical in this endeavor. detailed knowledge from humans and great apes is highly Structural magnetic resonance imaging (MRI) has been desirable, but these invasive methods cannot be ethically used to compare brain size development, brain structure applied in humans and great apes. Fortunately, the recent proportions and brain aging. Positron emission tomog- advent of non-invasive neuroimaging techniques has raphy (PET) imaging has been used to compare resting opened new possibilities for comparative studies (Box 2) brain glucose metabolism. Functional MRI (fMRI) has [2]. been used to compare auditory and visual system path- ways, as well as resting-state networks of connectivity. Structural MRI Finally, diffusion-weighted imaging (DWI) has been used The earliest comparative neuroimaging studies utilized to compare structural connectivity. Collectively, these structural MRI to compare the absolute and relative size methods have revealed human brain specializations of brain structures across anthropoid primate species. with respect to development, cortical organization, con- Similar studies had been conducted earlier using post- nectivity, and aging. These findings inform our knowl- mortem brain specimens [6–8], but MRI offered the advan- edge of the evolutionary changes responsible for the tage that data could be rapidly collected from living, special features of the modern human mind. healthy, nonelderly adult subjects without sacrificing ani- mals or waiting for them to die. This facilitated collection of The importance of comparative primate neuroimaging larger within-species sample sizes that permitted formal In the quest for a scientific understanding of human na- statistical tests of between-species differences. Another ture, no topic is more important than the evolution of the important advantage of MRI is that brain structure special features of the human brain [1,2]. The fossil record volumes do not need to be corrected for shrinkage that shows that brain size approximately tripled over the last occurs during the post-mortem fixation process [9]. 2.5 million years of human evolution [3]; however, the fossil Against the backdrop of evidence that brain structure record cannot identify potential evolutionary changes to size could be accurately predicted from overall brain size the internal organization of the brain [4]. To investigate across a broad sample of mammals [10], early MRI findings this question, we must turn to the comparative study of the showed that human brains in fact deviated from predic- brains of living primate species. If we can identify a tions derived from non-human anthropoid primates in characteristic of the human brain that is not found in some important respects, and could not simply be consid- the brain of any closely related primate species, then we ered scaled-up versions of typical non-human primate can infer that the trait evolved in the hominin lineage (see brains [11]. In particular, relative to a hypothetical ‘typical’ Glossary) after we diverged from our common ancestor anthropoid primate of our brain size, humans have larger with chimpanzees some 5–7 million years ago (mya). This approach renders the study of chimpanzees crucial for learning about human brain evolution: we cannot infer Glossary that a trait uniquely evolved in the human lineage unless it Allometry: study of how one part of an organism grows either in relation to the is absent in modern chimpanzees (Box 1) [5]. whole organism or to some other part. Many allometric relationships are well a described by the equation Y = bX , where a is the allometry exponent. When a = 1, the relationship is linear. When a > 1, increases in Y outpace increases in Corresponding author: Rilling, J.K. ([email protected]). X and the relationship is positively allometric. When a < 1, increases in Y do Keywords: neuroimaging; evolution; comparative; human; chimpanzee. not keep pace with increases in X and the relationship is negatively allometric. 1364-6613/$ – see front matter Hominin: living and extinct members of the human lineage after the split from ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tics.2013.09.013 chimpanzees. Homology: correspondence between species due to a common evolutionary origin. Voxel: the smallest volumetric element of a brain image, analogous to a pixel, but with the added dimension of depth. 46 Trends in Cognitive Sciences, January 2014, Vol. 18, No. 1 Review Trends in Cognitive Sciences January 2014, Vol. 18, No. 1 Box 1. Primate phylogeny Box 2. Neuroimaging techniques In taxonomic terms, primates are one of several orders in the MRI can be used to image either brain structure or brain function mammalian class. The earliest primates appear in the fossil record using the same instrument. In MRI, the subject is positioned within around 60 million years ago (mya), shortly after the dinosaurs the bore of a large magnet that exposes them to a strong magnetic became extinct. The two primate suborders, anthropoids and field, which causes a small fraction of the protons in their body to prosimians, diverged from each other early in primate evolution. orient in the direction of that magnetic field. If radiofrequency pulses Modern day prosimians are generally believed to have retained are then applied at the precession frequency of these protons, they more similarities with the earliest ancestral primates than anthro- are tipped out of alignment with the main magnetic field. The signal poid primates have. Anthropoid primates include New World intensity of voxels in MRI images is related to the behavior of the monkeys (from central and south America), Old World monkeys protons following this perturbation. This can be affected by (i) the (from Africa and Asia), and the hominoids, which include lesser water and fat content of tissues, (ii) the direction of water diffusion, apes (from Asia), great apes (from Africa and Asia), and humans. and (iii) the ratio of deoxygenated to oxygenated hemoglobin. Among the hominoids, humans are most distantly related to the These variables can be used, respectively, to create images that lesser apes, and most closely related to the African great apes. Our show (i) contrast between gray matter, white matter, and cere- two closest living primate relatives are the chimpanzees and the brospinal fluid (structural images for morphometrics), (ii) images of bonobos, both members of the genus Pan, with whom we shared a water diffusion (DWI images for measuring white matter integrity common ancestor some 5–7 mya. Chimpanzees and bonobos are and tractography), and (iii) increases in blood flow in response to believed to have shared their last common ancestor approximately stimuli (fMRI). 1–2 mya. To conclude that a neurobiological trait is uniquely human, PET involves the injection or consumption of radioactive com- we would ideally show that it is not present in any other living pounds, followed by detection of the distribution and concentration species. However, given the practical difficulty of doing so, the of radioactivity in the brain with an instrument known as a PET minimum criterion for suggesting that a trait uniquely evolved in scanner. PET can be used to measure cerebral glucose metabolism humans is to establish its absence in our closest living relative, and cerebral blood flow, both known correlates of synaptic activity either chimpanzees or bonobos, as well as in some more distantly in the brain. PET can also be used to image the density and related primate species that serves as an outgroup, to determine distribution of neurotransmitter receptors and transporters in the whether a difference between chimpanzees and humans represents brain. This involves injection of a radioactively labeled molecule that a chimpanzee or a human specialization. However, this more limited binds to a specific receptor (i.e., a ligand), followed by detection of approach leaves open the possibility of parallel evolution of the the location and intensity of the radioactivity. A great deal of human trait in a particular primate or even non-primate species. research is devoted to synthesizing radiolabeled ligands that have the appropriate binding characteristics in terms of their specificity and affinity for their receptors. Ligands are currently available for several subtypes of dopamine and serotonin receptors, as well as neocortices [9], temporal lobe volume [12,13], and estimat- their transporters. The number of available ligands will continue to ed prefrontal white matter volume [14], as well as greater grow in the future. All of these techniques are available for comparative neuroima- gyrification (cortical folding) in prefrontal cortex [9] and ging studies that teach us about human brain evolution. more
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