Comparative primate neuroimaging: insights into human brain evolution

doi:10.1016/j.tics.2013.09.013

Trends in Cognitive Sciences

Volume 18, Issue 1, January 2014, Pages 46-55

https://doi.org/10.1016/j.tics.2013.09.013 Get rights and content

Highlights

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Comparative neuroimaging can identify unique features of the human brain.
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Comparisons with chimpanzees are crucial for learning about human brain evolution.
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Human brains are special in terms of size, cortical organization, and connectivity.
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Human brains are special in terms of development and aging.

Comparative neuroimaging can identify unique features of the human brain and teach us about human brain evolution. Comparisons with chimpanzees, our closest living primate relative, are critical in this endeavor. Structural magnetic resonance imaging (MRI) has been used to compare brain size development, brain structure proportions and brain aging. Positron emission tomography (PET) imaging has been used to compare resting brain glucose metabolism. Functional MRI (fMRI) has been used to compare auditory and visual system pathways, as well as resting-state networks of connectivity. Finally, diffusion-weighted imaging (DWI) has been used to compare structural connectivity. Collectively, these methods have revealed human brain specializations with respect to development, cortical organization, connectivity, and aging. These findings inform our knowledge of the evolutionary changes responsible for the special features of the modern human mind.

Section snippets

The importance of comparative primate neuroimaging

In the quest for a scientific understanding of human nature, no topic is more important than the evolution of the special features of the human brain 1, 2. The fossil record shows that brain size approximately tripled over the last 2.5 million years of human evolution [3]; however, the fossil record cannot identify potential evolutionary changes to the internal organization of the brain [4]. To investigate this question, we must turn to the comparative study of the brains of living primate

Structural MRI

The earliest comparative neuroimaging studies utilized structural MRI to compare the absolute and relative size of brain structures across anthropoid primate species. Similar studies had been conducted earlier using post-mortem brain specimens 6, 7, 8, but MRI offered the advantage that data could be rapidly collected from living, healthy, nonelderly adult subjects without sacrificing animals or waiting for them to die. This facilitated collection of larger within-species sample sizes that

continues at the prenatal for another

Structural MRI studies of non-human primates were followed in time by PET studies that enabled measurement of brain function by injection of radioactive tracers that could measure regional cerebral blood flow or glucose metabolism. An early application relevant to human brain evolution was to ask whether listening to species-specific vocalizations activated homologs of human language areas in macaque monkeys [49]. Indeed, in a small sample of macaque monkeys, blood flow responses were more

Functional MRI

fMRI is able to measure changes in blood flow without use of the radioactive tracers required for PET imaging. fMRI images can also be acquired in less time than it takes to acquire PET images (fMRI has higher temporal resolution). The lack of fMRI data from awake chimpanzees constitutes a crucial gap in our knowledge of comparative higher primate brain function. The sensitivity of fMRI to head movement would require either restraint of these very strong animals, or training them to lie still

Diffusion-weighted imaging

DWI is another structural neuroimaging method and the most recent to be applied in a comparative framework. DWI is able to measure the diffusion of water molecules in the brain [71]. Because water preferentially diffuses parallel to the direction in which axons are oriented, tractography software can use this information to attempt to reconstruct the trajectory of major white-matter fiber tracts in the brain 72, 73.

DWI has been used to describe differences between humans and non-human primates

Concluding remarks

This review has highlighted neuroimaging studies that compare humans and chimpanzees because these comparisons are the most informative with respect to understanding the evolution of the unique features of the human brain. What have these comparative neuroimaging studies taught us about the evolution of the neural substrates of human uniqueness? The most obvious specialization of the human brain is its size. Comparative neuroimaging has clarified how these dramatic differences in brain size

Acknowledgments

I thank Matthew Glasser, Longchuan Li, Todd Preuss, and Hanne Van Der Iest for their many helpful comments and suggestions on this manuscript.

Glossary

Allometry: study of how one part of an organism grows either in relation to the whole organism or to some other part. Many allometric relationships are well described by the equation Y = bX^a, where a is the allometry exponent. When a = 1, the relationship is linear. When a > 1, increases in Y outpace increases in X and the relationship is positively allometric. When a < 1, increases in Y do not keep pace with increases in X and the relationship is negatively allometric.
Hominin: living and extinct members

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Trends in Cognitive Sciences

ReviewComparative primate neuroimaging: insights into human brain evolution

Highlights

Section snippets

The importance of comparative primate neuroimaging

Structural MRI

continues at the prenatal for another

Functional MRI

Diffusion-weighted imaging

Concluding remarks

Acknowledgments

Glossary

Brain Res.

J. Hum. Evol.

J. Hum. Evol.

J. Hum. Evol.

J. Hum. Evol.

J. Hum. Evol.

Int. Rev. Neurobiol.

Neuron

Med. Image Anal.

Neurobiol. Aging

Curr. Biol.

Neurobiol. Aging

Neurosci. Biobehav. Rev.

Neurobiol. Aging

Neurobiol. Aging

Neurobiol. Aging

Neuropsychologia

Trends Cogn. Sci.

Neuroimage

J. Magn. Reson. B

Neuroimage

Neuroimage

What is Special about the Human Brain

The human brain: rewired and running hot

Ann. N. Y. Acad. Sci.

Evolution of the brain in humans: paleoneurology

Who's afraid of Homo sapiens?

J. Biomed. Discov. Collab.

The Human Primate

Human brain evolution: II. Embryology and brain allometry

Comparative size of brain and brain components

Linked regularities in the development and evolution of mammalian brains

Science

Human and non-human primate brains: are they allometrically scaled versions of the same design?

Evol. Anthropol.

Prefrontal white matter volume is disproportionately larger in humans than in other primates

Nat. Neurosci.

The Human Brain in Figures and Tables

What is it like to be a human?

Mapping human cortical areas in vivo based on myelin content as revealed by T1- and T2-weighted MRI

J. Neurosci.

Trends and properties of human cerebral cortex: correlations with cortical myelin content

Neuroimage

Human brain left–right asymmetries in temporal speech region

Science

Planum temporale asymmetries in great apes as revealed by magnetic resonance imaging (MRI)

Neuroreport

Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog

Science

Neuroanatomical localization of the motor hand area with magnetic resonance imaging: the left hemisphere is larger in great apes

Behav. Neurosci.

Chimpanzee (Pan troglodytes) precentral corticospinal system asymmetry and handedness: a diffusion magnetic resonance imaging study

PLoS ONE

Gesture handedness predicts asymmetry in the chimpanzee inferior frontal gyrus

Neuroreport

Handedness is associated with asymmetries in gyrification of the cerebral cortex of chimpanzees

Cereb. Cortex

Asymmetries of the parietal operculum in chimpanzees (Pan troglodytes) in relation to handedness for tool use

Cereb. Cortex

Handedness is more than laterality: lessons from chimpanzees

Ann. N. Y. Acad. Sci.

Primate laterality and the biology and evolution of human handedness: a review and synthesis

Ann. N. Y. Acad. Sci.

Anatomical study of cerebral asymmetry in the temporal lobe of humans, chimpanzees, and rhesus monkeys

Science

Review
Comparative primate neuroimaging: insights into human brain evolution