The corpus callosum in primates: processing speed of axons and the evolution of hemispheric asymmetry

Interhemispheric communication may be constrained as brain size increases because of transmission delays in action potentials over the length of axons. Although one might expect larger brains to have progressively thicker axons to compensate, spatial packing is a limiting factor. Axon size distributions within the primate corpus callosum (CC) may provide insights into how these demands affect conduction velocity. We used electron microscopy to explore phylogenetic variation in myelinated axon density and diameter of the CC from 14 different anthropoid primate species, including humans. The majority of axons were less than 1 µm in diameter across all species, indicating that conduction velocity for most interhemispheric communication is relatively constant regardless of brain size. The largest axons within the upper 95th percentile scaled with a progressively higher exponent than the median axons towards the posterior region of the CC. While brain mass among the primates in our analysis varied by 97-fold, estimates of the fastest cross-brain conduction times, as conveyed by axons at the 95th percentile, varied within a relatively narrow range between 3 and 9 ms across species, whereas cross-brain conduction times for the median axon diameters differed more substantially between 11 and 38 ms. Nonetheless, for both size classes of axons, an increase in diameter does not entirely compensate for the delay in interhemispheric transmission time that accompanies larger brain size. Such biophysical constraints on the processing speed of axons conveyed by the CC may play an important role in the evolution of hemispheric asymmetry.

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Correction to ‘The corpus callosum in primates: processing speed of axons and the evolution of hemispheric asymmetry’

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.2620 ◽

2015 ◽

Vol 282 (1819) ◽

pp. 20152620

Author(s):

Kimberley A. Phillips ◽

Cheryl D. Stimpson ◽

Jeroen B. Smaers ◽

Mary Ann Raghanti ◽

Bob Jacobs ◽

...

Keyword(s):

Corpus Callosum ◽

Processing Speed ◽

Hemispheric Asymmetry

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Interhemispheric connectivity endures across species: An allometric exposé on the corpus callosum

10.1101/2021.01.10.426155 ◽

2021 ◽

Author(s):

Ben Cipollini ◽

Garrison W. Cottrell

Keyword(s):

Functional Connectivity ◽

Corpus Callosum ◽

Brain Size ◽

Mammalian Species ◽

Primate Species ◽

Fiber Density ◽

Cortical Areas ◽

Wrong Thing ◽

Interhemispheric Connectivity ◽

Callosal Fiber

Rilling & Insel have argued that in primates, bigger brains have proportionally fewer anatomical interhemispheric connections, leading to reduced functional connectivity between the hemispheres (1). They based this on a comparison between surface areas of the corpus callosum and cortex rather than estimating connection counts, while leaving out other quantities also dependent on brain size such as callosal fiber density, neuron density, and number of functional areas.We use data from the literature to directly estimate connection counts. First, we estimate callosal fiber density as a function of brain size. We validate this by comparing out-of-sample human data to our function’s estimate. We then mine the literature to obtain function estimates for all other quantities, and use them to estimate intra- and interhemispheric white matter connection counts as a function of brain size.The results show a much larger decrease in the scaling of interhemispheric to intrahemispheric connections than previously estimated. However, we hypothesize that raw connection counts are the wrong quantity to be estimating when considering functional connectivity. Instead, we hypothesize that functional connectivity is related to connection counts relative to the number of cortical areas.Accordingly, we estimate inter-area connection counts for intra- and interhemispheric connectivity and find no difference in how they scale with brain size. We find that, on average, an interhemispheric inter-area connection contains 3-8x more connections than an intrahemispheric inter-area connection, regardless of brain size. In doing so, we find that the fiber count of the human corpus callosum has been underestimated by 20%.Significance StatementThere are arguments in the literature that larger brains have proportionally fewer interhemispheric connections. We find that the decrease is even larger than previously estimated. However, we argue that this quantity is the wrong thing to measure: Rather, we should measure functional connectivity between cortical areas. We show that the ratio of interhemispheric and intrahemispheric connectivity between cortical areas is constant across mammalian species. These findings are consistent with a growing literature that suggest interhemispheric connectivity is special across all primate species.

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A Farewell to the Encephalization Quotient: A New Brain Size Measure for Comparative Primate Cognition

Brain Behavior and Evolution ◽

10.1159/000517013 ◽

2021 ◽

pp. 1-12

Author(s):

Carel P. van Schaik ◽

Zegni Triki ◽

Redouan Bshary ◽

Sandra A. Heldstab

Keyword(s):

Body Size ◽

Cognitive Abilities ◽

Brain Size ◽

Estimation Error ◽

Primate Species ◽

Mammal Species ◽

Mean Values ◽

Encephalization Quotient ◽

Body Sizes ◽

Size Measure

Both absolute and relative brain sizes vary greatly among and within the major vertebrate lineages. Scientists have long debated how larger brains in primates and hominins translate into greater cognitive performance, and in particular how to control for the relationship between the noncognitive functions of the brain and body size. One solution to this problem is to establish the slope of cognitive equivalence, i.e., the line connecting organisms with an identical bauplan but different body sizes. The original approach to estimate this slope through intraspecific regressions was abandoned after it became clear that it generated slopes that were too low by an unknown margin due to estimation error. Here, we revisit this method. We control for the error problem by focusing on highly dimorphic primate species with large sample sizes and fitting a line through the mean values for adult females and males. We obtain the best estimate for the slope of circa 0.27, a value much lower than those constructed using all mammal species and close to the value expected based on the genetic correlation between brain size and body size. We also find that the estimate of cognitive brain size based on cognitive equivalence fits empirical cognitive studies better than the encephalization quotient, which should therefore be avoided in future studies on primates and presumably mammals and birds in general. The use of residuals from the line of cognitive equivalence may change conclusions concerning the cognitive abilities of extant and extinct primate species, including hominins.

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Molecular evolutionary analysis of human primary microcephaly genes

BMC Ecology and Evolution ◽

10.1186/s12862-021-01801-0 ◽

2021 ◽

Vol 21 (1) ◽

Author(s):

Nashaiman Pervaiz ◽

Hongen Kang ◽

Yiming Bao ◽

Amir Ali Abbasi

Keyword(s):

Evolutionary History ◽

Genetic Basis ◽

Brain Size ◽

Primate Species ◽

Evolutionary Analysis ◽

Australopithecus Afarensis ◽

Primary Microcephaly ◽

Modern Humans ◽

History Of ◽

The Brain

Abstract Background There has been a rapid increase in the brain size relative to body size during mammalian evolutionary history. In particular, the enlarged and globular brain is the most distinctive anatomical feature of modern humans that set us apart from other extinct and extant primate species. Genetic basis of large brain size in modern humans has largely remained enigmatic. Genes associated with the pathological reduction of brain size (primary microcephaly-MCPH) have the characteristics and functions to be considered ideal candidates to unravel the genetic basis of evolutionary enlargement of human brain size. For instance, the brain size of microcephaly patients is similar to the brain size of Pan troglodyte and the very early hominids like the Sahelanthropus tchadensis and Australopithecus afarensis. Results The present study investigates the molecular evolutionary history of subset of autosomal recessive primary microcephaly (MCPH) genes; CEP135, ZNF335, PHC1, SASS6, CDK6, MFSD2A, CIT, and KIF14 across 48 mammalian species. Codon based substitutions site analysis indicated that ZNF335, SASS6, CIT, and KIF14 have experienced positive selection in eutherian evolutionary history. Estimation of divergent selection pressure revealed that almost all of the MCPH genes analyzed in the present study have maintained their functions throughout the history of placental mammals. Contrary to our expectations, human-specific adoptive evolution was not detected for any of the MCPH genes analyzed in the present study. Conclusion Based on these data it can be inferred that protein-coding sequence of MCPH genes might not be the sole determinant of increase in relative brain size during primate evolutionary history.

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Effect sizes and meta-analysis indicate no sex dimorphism in the human or rodent corpus callosum

Behavioral and Brain Sciences ◽

10.1017/s0140525x98351213 ◽

1998 ◽

Vol 21 (3) ◽

pp. 338-339

Author(s):

Douglas Wahlsten ◽

Katherine M. Bishop

Keyword(s):

Standard Deviation ◽

Corpus Callosum ◽

Brain Size ◽

Meta Analysis ◽

Effect Sizes ◽

Sex Dimorphism ◽

Standard Deviations ◽

Average Size

Sex dimorphism occurs when group means differ by four or more standard deviations. However, the average size of the corpus callosum is greater in males by about one standard deviation in rats, 0.2 standard deviation in humans, and virtually zero in mice. Furthermore, variations in corpus callosum size are related to brain size and are not sex specific.

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Relaxed genetic control of cortical organization in human brains compared with chimpanzees

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1512646112 ◽

2015 ◽

Vol 112 (48) ◽

pp. 14799-14804 ◽

Cited By ~ 79

Author(s):

Aida Gómez-Robles ◽

William D. Hopkins ◽

Steven J. Schapiro ◽

Chet C. Sherwood

Keyword(s):

Genetic Control ◽

Cultural Context ◽

Brain Size ◽

Environmental Influence ◽

Modern Human ◽

Primate Species ◽

Additional Line ◽

Cortical Organization ◽

Anatomical Basis ◽

Human Brains

The study of hominin brain evolution has focused largely on the neocortical expansion and reorganization undergone by humans as inferred from the endocranial fossil record. Comparisons of modern human brains with those of chimpanzees provide an additional line of evidence to define key neural traits that have emerged in human evolution and that underlie our unique behavioral specializations. In an attempt to identify fundamental developmental differences, we have estimated the genetic bases of brain size and cortical organization in chimpanzees and humans by studying phenotypic similarities between individuals with known kinship relationships. We show that, although heritability for brain size and cortical organization is high in chimpanzees, cerebral cortical anatomy is substantially less genetically heritable than brain size in humans, indicating greater plasticity and increased environmental influence on neurodevelopment in our species. This relaxed genetic control on cortical organization is especially marked in association areas and likely is related to underlying microstructural changes in neural circuitry. A major result of increased plasticity is that the development of neural circuits that underlie behavior is shaped by the environmental, social, and cultural context more intensively in humans than in other primate species, thus providing an anatomical basis for behavioral and cognitive evolution.

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Cortical Projection Topography of the Human Splenium: Hemispheric Asymmetry and Individual Differences

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2009.21290 ◽

2010 ◽

Vol 22 (8) ◽

pp. 1662-1669 ◽

Cited By ~ 67

Author(s):

Mary Colvin Putnam ◽

Megan S. Steven ◽

Karl W. Doron ◽

Adam C. Riggall ◽

Michael S. Gazzaniga

Keyword(s):

Visual Processing ◽

Visual Information ◽

Hemispheric Asymmetry ◽

Right Hemisphere ◽

Diffusion Tensor ◽

Cortical Projection ◽

Interhemispheric Communication ◽

Posterior Portion ◽

Interhemispheric Connectivity ◽

Visual Areas

The corpus callosum is the largest white matter pathway in the human brain. The most posterior portion, known as the splenium, is critical for interhemispheric communication between visual areas. The current study employed diffusion tensor imaging to delineate the complete cortical projection topography of the human splenium. Homotopic and heterotopic connections were revealed between the splenium and the posterior visual areas, including the occipital and the posterior parietal cortices. In nearly one third of participants, there were homotopic connections between the primary visual cortices, suggesting interindividual differences in splenial connectivity. There were also more instances of connections with the right hemisphere, indicating a hemispheric asymmetry in interhemispheric connectivity within the splenium. Combined, these findings demonstrate unique aspects of human interhemispheric connectivity and provide anatomical bases for hemispheric asymmetries in visual processing and a long-described hemispheric asymmetry in speed of interhemispheric communication for visual information.

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Persistent reduction of conduction velocity and myelinated axon damage in vibrated rat tail nerves

Muscle & Nerve ◽

10.1002/mus.21235 ◽

2009 ◽

Vol 39 (6) ◽

pp. 770-775 ◽

Cited By ~ 15

Author(s):

Michael A. Loffredo ◽

Ji-Geng Yan ◽

Dennis Kao ◽

Lin Ling Zhang ◽

Hani S. Matloub ◽

...

Keyword(s):

Conduction Velocity ◽

Myelinated Axon ◽

Axon Damage ◽

Rat Tail

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Neuronal factors determining high intelligence

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2015.0180 ◽

2016 ◽

Vol 371 (1685) ◽

pp. 20150180 ◽

Cited By ~ 58

Author(s):

Ursula Dicke ◽

Gerhard Roth

Keyword(s):

Conduction Velocity ◽

Packing Density ◽

Cortical Neurons ◽

Brain Size ◽

General Information ◽

New World Monkeys ◽

Brain Volumes ◽

Axonal Conduction ◽

High Intelligence ◽

Best Fit

Many attempts have been made to correlate degrees of both animal and human intelligence with brain properties. With respect to mammals, a much-discussed trait concerns absolute and relative brain size, either uncorrected or corrected for body size. However, the correlation of both with degrees of intelligence yields large inconsistencies, because although they are regarded as the most intelligent mammals, monkeys and apes, including humans, have neither the absolutely nor the relatively largest brains. The best fit between brain traits and degrees of intelligence among mammals is reached by a combination of the number of cortical neurons, neuron packing density, interneuronal distance and axonal conduction velocity—factors that determine general information processing capacity (IPC), as reflected by general intelligence. The highest IPC is found in humans, followed by the great apes, Old World and New World monkeys. The IPC of cetaceans and elephants is much lower because of a thin cortex, low neuron packing density and low axonal conduction velocity. By contrast, corvid and psittacid birds have very small and densely packed pallial neurons and relatively many neurons, which, despite very small brain volumes, might explain their high intelligence. The evolution of a syntactical and grammatical language in humans most probably has served as an additional intelligence amplifier, which may have happened in songbirds and psittacids in a convergent manner.

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