Updated imaging and phylogenetic comparative methods reassess relative temporal lobe size in anthropoids and modern humans

Objectives

Two decades ago, Rilling and Seligman, hereafter abbreviated to RAS Study, suggested modern humans had relatively larger temporal lobes for brain size compared to other anthropoids. Despite many subsequent studies drawing conclusions about the evolutionary implications for the emergence of unique cerebral specializations in Homo sapiens, no re-assessment has occurred using updated methodologies.

Methods

We reassessed the association between right temporal lobe volume (TLV) and right hemisphere volume (HV) in the anthropoid brain. In a sample compiled de novo by us, T1-weighted in vivo Magnetic Resonance Imaging (MRI) scans of 11 extant anthropoid species were calculated by-voxel from the MRI and the raw data from RAS Study directly compared to our sample. Phylogenetic Generalized Least-Squares (PGLS) regression and trait-mapping using Blomberg's K (kappa) tested the correlation between HV and TLV accounting for anthropoid phylogeny, while bootstrapped PGLS regressions tested difference in slopes and intercepts between monkey and ape subsamples.

Results

PGLS regressions indicated statistically significant correlations (r² < 0.99; p ≤ 0.0001) between TLV and HV with moderate influence from phylogeny (K ≤ 0.42). Bootstrapped PGLS regression did not show statistically significant differences in slopes between monkeys and apes but did for intercepts. In our sample, human TLV was not larger than expected for anthropoids.

Discussion

Updated imaging, increased sample size and advanced statistical analyses did not find statistically significant results that modern humans possessed a disproportionately large temporal lobe volume compared to the general anthropoid trend. This has important implications for human and non-human primate brain evolution.     

Frontal White Matter Volume Is Associated with Brain Enlargement and Higher Structural Connectivity in Anthropoid Primates

Previous research has indicated the importance of the frontal lobe and its ‘executive’ connections to other brain structures as crucial in explaining primate neocortical adaptations. However, a representative sample of volumetric measurements of frontal connective tissue (white matter) has not been available. In this study, we present new volumetric measurements of white and grey matter in the frontal and non-frontal neocortical lobes from 18 anthropoid species. We analyze this data in the context of existing theories of neocortex, frontal lobe and white versus grey matter hyperscaling. Results indicate that the ‘universal scaling law’ of neocortical white to grey matter applies separately for frontal and non-frontal lobes; that hyperscaling of both neocortex and frontal lobe to rest of brain is mainly due to frontal white matter; and that changes in frontal (but not non-frontal) white matter volume are associated with changes in rest of brain and basal ganglia, a group of subcortical nuclei functionally linked to ‘executive control’. Results suggest a central role for frontal white matter in explaining neocortex and frontal lobe hyperscaling, brain size variation and higher neural structural connectivity in anthropoids.     

The primate neocortex in comparative perspective using magnetic resonance imaging.

In this study we use neuroanatomic data from living anthropoid primate subjects to test the following three hypotheses: (1) that the human neocortex is significantly larger than expected for a primate of our brain size, (2) that the human prefrontal cortex is significantly more convoluted than expected for our brain size, and (3) that increases in cerebral white matter volume outpace increases in neocortical gray matter volume among anthropoid primates. Whole brain MRI scans were obtained from 44 living primate subjects from 11 different species. Image analysis software was used to calculate total brain volume, neocortical gray matter volume, cerebral white matter volume, and the cross sectional area of the spinal cord in each scan. Allometric regression analyses were used to compare the relative size of these brain structures across species, with an emphasis on determining whether human brain proportions correspond with predictions based on nonhuman primate allometric trajectories. All three hypotheses were supported by our analysis. The results of this study provide additional insights into human brain evolution beyond the important observation that brain volume approximately tripled in the hominid lineage by demonstrating that the neocortex was uniquely modified throughout hominid evolution. These modifications may constitute part of the neurobiological substrate that supports some of our species most distinctive cognitive abilities.     

The brain and its main anatomical subdivisions in living hominoids using magnetic resonance imaging

Primary comparative data on the hominoid brain are scarce and major neuroanatomical differences between humans and apes have not yet been described satisfactorily, even at the gross level. Basic questions that involve the evolution of the human brain cannot be addressed adequately unless the brains of all extant hominoid species are analyzed. Contrary to the scarcity of original data, there is a rich literature on the topic of human brain evolution and several debates exist on the size of particular sectors of the brain, e.g., the frontal lobe.In this study we applied a non-invasive imaging technique (magnetic resonance) on living human, great ape and lesser ape subjects in order to investigate the overall size of the hominoid brain. The images were reconstructed in three dimensions and volumetric estimates were obtained for the brain and its main anatomical sectors, including the frontal and temporal lobes, the insula, the parieto-occipital sector and the cerebellum.A remarkable homogeneity is present in the relative size of many of the large sectors of the hominoid brain, but interspecific and intraspecific variation exists in certain parts of the brain. The human cerebellum is smaller than expected for an ape brain of human size. It is suggested that the cerebellum increased less than the cerebrum after the split of the human lineage from the African ancestral hominoid stock. In contrast, humans have a slightly larger temporal lobe and insula than expected, but differences are not statistically significant.Humans do not have a larger frontal lobe than expected for an ape brain of human size and gibbons have a relatively smaller frontal lobe than the rest of the hominoids. Given the fact that the frontal lobe in humans and great apes has similar relative size, it is parsimonious to suggest that the relative size of the whole of the frontal lobe has not changed significantly during hominid evolution in the Plio-Pleistocene.     

Neural connectivity and cortical substrates of cognition in hominoids

Cognitive functions and information processing recruit discrete neural systems in the cortex and white matter. We tested the idea that specific regions in the cerebrum are differentially enlarged in humans and that some of the neural reorganizational events that took place during hominoid evolution were species-specific and independent of changes in absolute brain size. We used magnetic resonance images of the living brains of 10 human and 17 ape subjects to obtain volumetric estimates of regions of interest. We parcellated the white matter in the frontal and temporal lobes into two sectors, including the white matter immediately underlying the cortex (gyral white matter) and the rest of white matter (core). We outlined the dorsal, mesial, and orbital subdivisions of the frontal lobe and analyzed the relationship between cortex and gyral white matter within each subdivision. For all regions analyzed, the observed human values are as large as expected, with the exception of the gyral white matter, which is larger than expected in humans. We found that orangutans had a relatively smaller orbital sector than any other great ape species, with no overlap in individual values. We found that the relative size of the dorsal subdivision is larger in chimpanzees than in bonobos, and that the ratio of gyral white matter to cortex stands out in Pan in comparison to Gorilla and Pongo. Individual variability, possible sex differences, and hemispheric asymmetries were present not only in humans, but in apes as well. Differences in the distribution of neural connectivity and cortical sectors were identified among great ape species that share similar absolute brain sizes. Given that these regions are part of neural systems with distinct functional attributes, we suggest that the observed differences may reflect different evolutionary pressures on regulatory mechanisms of complex cognitive functions, including social cognition.     

Relationship between body mass index and gray matter volume in 1,428 healthy individuals

Objective: To investigate any correlation between BMI and brain gray matter volume, we analyzed 1,428 healthy Japanese subjects by applying volumetric analysis and voxel‐based morphometry (VBM) using brain magnetic resonance (MR) imaging, which enables a global analysis of brain structure without a priori identification of a region of interest. Methods and Procedures: We collected brain MR images from 690 men and 738 women, and their height, weight, and other clinical information. The collected images were automatically normalized into a common standard space for an objective assessment of neuroanatomical correlations in volumetric analysis and VBM with BMI. Results: Volumetric analysis revealed a significant negative correlation in men (P < 0.001, adjusting for age, lifetime alcohol intake, history of hypertension, and diabetes mellitus), although not in women, between BMI and the gray matter ratio, which represents the percentage of gray matter volume in the intracranial volume. VBM revealed that, in men, the regional gray matter volume of the bilateral medial temporal lobes, anterior lobe of the cerebellum, occipital lobe, frontal lobe, precuneus, and midbrain showed significant negative correlations with BMI, while those of the bilateral inferior frontal gyri, posterior lobe of the cerebellum, frontal lobes, temporal lobes, thalami, and caudate heads showed significant positive correlations with BMI. Discussion: Global loss and regional alterations in gray matter volume occur in obese male subjects, suggesting that male subjects with a high BMI are at greater risk for future declines in cognition or other brain functions.     

Human and nonhuman primate brains: Are they allometrically scaled versions of the same design?

Allometric analyses of brain structure sizes across the primate order demonstrate that human, ape, and other anthropoid brains are not simply allometrically scaled versions of the same generalized design. Both human and ape brains exhibit specializations with respect to other anthropoid brains. Ape specializations include elaboration of the cerebellum (all apes) and frontal lobes (great apes only), and probably connectivity between them. Human brain specializations include an overall larger proportion of neocortex, with disproportionate enlargement of prefrontal and temporal association cortices; an apparent increase in cerebellar connections with cerebral cortical association areas involved in cognition; and a probable augmentation of intracortical connectivity in prefrontal cortex.     

Recent origin of a hominoid-specific splice form of neuropsin, a gene involved in learning and memory

Neuropsin is a secreted-type serine protease involved in learning and memory. The type II splice form of neuropsin is abundantly expressed in the human brain but not in the mouse brain. We sequenced the type II-spliced region of neuropsin gene in humans and representative nonhuman primate species. Our comparative sequence analysis showed that only the hominoid species (humans and apes) have the intact open reading frame of the type II splice form, indicating that the type II neuropsin originated recently in the primate lineage about 18 MYA. Expression analysis using RT-PCR detected abundant expression of the type II form in the frontal lobe of the adult human brain, but no expression was detected in the brains of lesser apes and Old World monkeys, indicating that the type II form of neuropsin only became functional in recent time, and it might contribute to the progressive change of cognitive abilities during primate evolution.     

Red cell polymorphisms in nonhuman primates: A review

Abstract: Development as well as current status of the knowledge of nonhuman primate blood groups are discussed together with some practical implications of the red cell antigen polymorphisms in anthropoid apes, Old and New World monkeys and prosimians. Recent data on molecular biology and genetics throw light on the relationships among simian and human red cell antigens and their evolutionary pathways.     

Allometry of primate hair density and the evolution of human hairlessness

Allometric analyses of hair densities in 23 anthropoid primate taxa reveal that increasingly massive primates have systematically fewer hairs per equal unit of body surface. Considering the absence of effective sweating in monkeys and apes, the negative allometry of relative hair density may represent an architectural adaptation to thermal constraints imposed by the decreasing ratios of surface area to volume in progressively massive primates. Judging by estimates of body volume, denudation of the earliest hominids should have progressed to a considerable extent prior to their shift from a forest to a grassland habitat during the Pliocene. We propose that, lacking a reflective coat of hair, the exploitation of eccrine sweating emerged as the primary mechanism for adaptation to the increased heat loads of man's new environment and permitted further reduction of the remnant coat to its present vestigial condition.     

Investigation of the human Rh blood group system in nonhuman primates and other species with serologic and Southern blot analysis

To investigate the evolution of the Rh blood-group system in anthropoid apes, New and Old World monkeys, and nonprimate animals, serologic typing of erythrocytes from these species with antibodies specific for the human Rh blood-group antigens was performed. In addition, genomic DNA from these animals was analyzed on Southern blots with a human Rh-specific cDNA.Consistent with earlier reports, serologic results showed that gorilla and chimpanzee erythrocytes had epitopes recognized by human Rh D and c antisera, and gibbon erythrocytes were recognized by the c antisera. Surprisingly, some Old and New World monkeys also expressed a Rh c epitope on their erythrocytes. No erythrocytes from the nonprimate animals reacted specifically with any of the human Rh antisera.Southern blot analysis with a human Rh-specific cDNA probe detected Rh-related sequences in anthropoid apes, all New and Old World monkeys, and in most nonprimate animals tested. Although some Rh-related restriction fragments were conserved across species lines in primates, the Rh locus was more polymorphic in chimpanzees and gorillas than in humans. In addition, restriction fragments segregating with the presence of the D antigen in humans were present in the primate species that expressed the D antigen.     

Assessing endocranial variations in great apes and humans using 3D data from virtual endocasts

Modern humans are characterized by their large, complex, and specialized brain. Human brain evolution can be addressed through direct evidence provided by fossil hominid endocasts (i.e. paleoneurology), or through indirect evidence of extant species comparative neurology. Here we use the second approach, providing an extant comparative framework for hominid paleoneurological studies. We explore endocranial size and shape differences among great apes and humans, as well as between sexes. We virtually extracted 72 endocasts, sampling all extant great ape species and modern humans, and digitized 37 landmarks on each for 3D generalized Procrustes analysis. All species can be differentiated by their endocranial shape. Among great apes, endocranial shapes vary from short (orangutans) to long (gorillas), perhaps in relation to different facial orientations. Endocranial shape differences among African apes are partly allometric. Major endocranial traits distinguishing humans from great apes are endocranial globularity, reflecting neurological reorganization, and features linked to structural responses to posture and bipedal locomotion. Human endocasts are also characterized by posterior location of foramina rotunda relative to optic canals, which could be correlated to lesser subnasal prognathism compared to living great apes. Species with larger brains (gorillas and humans) display greater sexual dimorphism in endocranial size, while sexual dimorphism in endocranial shape is restricted to gorillas, differences between males and females being at least partly due to allometry. Our study of endocranial variations in extant great apes and humans provides a new comparative dataset for studies of fossil hominid endocasts.     

Fatty acid composition of wild anthropoid primate milks

Fatty acids in milk reflect the interplay between species-specific physiological mechanisms and maternal diet. Anthropoid primates (apes, Old and New World monkeys) vary in patterns of growth and development and dietary strategies. Milk fatty acid profiles also are predicted to vary widely. This study investigates milk fatty acid composition of five wild anthropoids (Alouatta palliata, Callithrix jacchus, Gorilla beringei beringei, Leontopithecus rosalia, Macaca sinica) to test the null hypothesis of a generalized anthropoid milk fatty acid composition. Milk from New and Old World monkeys had significantly more 8:0 and 10:0 than milk from apes. The leaf eating species G. b. beringei and A. paliatta had a significantly higher proportion of milk 18:3n-3, a fatty acid found primarily in plant lipids. Mean percent composition of 22:6n-3 was significantly different among monkeys and apes, but was similar to the lowest reported values for human milk. Mountain gorillas were unique among anthropoids in the high proportion of milk 20:4n-6. This seems to be unrelated to requirements of a larger brain and may instead reflect species-specific metabolic processes or an unknown source of this fatty acid in the mountain gorilla diet.     

Normal neuroanatomical variation in the human brain: an MRI-volumetric study

Normative data on the in vivo size of the human brain and its major anatomically defined subdivisions are not readily available. In this study, high-resolution magnetic resonance imaging was used to measure regional brain volumes in 46 normal, right-handed adults (23 men, 23 women) between the ages of 22-49 years. Parcellation of the brain was based on neuroanatomical landmarks. The following brain regions were measured: the cerebral hemispheres, frontal lobe, temporal lobe, parietal lobe, occipital lobe, cingulate gyrus, insula, cerebellum, corpus callosum, and lateral ventricles. Males tend to be significantly larger than females, for the whole brain and for nearly all of its major subdivisions, including the corpus callosum. However, the proportional sizes of regions relative to total volume of the hemisphere are remarkably similar in males and females. Variation in size of region is always greater than variation in proportional representation. Asymmetries in brain regions are not profound, with the exception of the cingulate gyrus, which is larger in the left hemisphere. Brain regions are highly correlated in size, with the exception of the lateral ventricles. After controlling for hemisphere size, the volumes of the frontal and parietal lobes are significantly negatively correlated. The occipital lobe tends to be less sexually dimorphic than other major lobes, and less correlated with other brain regions for volume. These results have implications for understanding whether or not certain sectors of the brain have shown relative expansion over the course of hominid and hominoid evolution.     

Polymorphism of glycophorins in nonhuman primate erythrocytes

Using immunoblotting techniques and polyclonal antisera to human erythrocyte glycophorin, we show that erythrocytes of several species of nonhuman primates, including representatives of anthropoid apes (19 chimpanzees, 3 gorillas, 6 orangutans, and 3 gibbons) and Old World monkeys (3 baboons, 5 rhesus monkeys, and 6 cynomologus macaques), contain human glycophorin-like molecules. Each species displays a unique glycophorin profile; in anthropoid apes the profile is more complex than in Old World monkeys and more similar to that seen in humans. The chimpanzee was the only species in which human -like glycophorin was detected but it differed from its human counterpart in electrophoretic mobility and reaction with M-specific monoclonal antibody. In contrast to humans, highly polymorphic glycophorin profiles were observed in each species of anthropoid apes and three distinct patterns were defined in each. No such polymorphism has been found so far among the Old World monkeys in the limited number of animals studied. The major glycophorins in all species but the chimpanzees failed to react with M- or N-specific monoclonal antibodies, suggesting structural differences from the human within the amino terminal regions. The reaction with the minor glycophorins showed inter- and intraspecies variability. All glycophorins, except -like glycophorin in the chimpanzee, reacted with the antiserum to the carboxyl terminal fragment of human glycophorin, indicating a structural relation to the human in this region. An unexpected correlation was observed, in the chimpanzee, between the patterns of electrophoretically resolved glycophorins and the V-A-B-D blood-group phenotypes, allowing the assignment of each determinant to specific glycophorin bands. The basis for the differences observed between human and nonhuman primate glycophorins is not clear but the possibilities include a common nonpolymorphic ancestor and differences in selective pressures.This research was supported by National Institutes of Health Grant 5 RO1 GM16389.     

Is the Clavicle of Apes Long? An Investigation of Clavicular Length in Relation to Body Mass and Upper Thoracic Width

An elongated clavicle is one of the distinct features of apes and humans. It plays an important role in providing mobility as well as stability for the shoulder joints. The relative length of the clavicle is an especially important factor in limiting the range of shoulder joint excursion. It is said that among primates, Asian apes, i.e., gibbons and orang-utans, have very long clavicles. At the same time, they also have a wide upper thoracic cage, which may diminish the effective length of the clavicle. To clarify the length of the clavicle in apes, from the standpoint of the functional anatomy of the shoulder girdle, we examined clavicular length in 15 anthropoid species exhibiting various positional behaviors. The results confirm that clavicle length in Asian apes is long, and chimpanzees have a short clavicle like that of Old and New World monkeys, when scaled to body mass. The clavicular length of chimpanzees, however, is intermediate between Old World monkeys and Asian apes when scaled against thoracic width. Therefore, living apes can be grouped together, albeit just barely, by possession of a relatively long clavicle for their thoracic cage size. Interestingly, New World monkeys tend to exhibit a longer clavicle than Old World monkeys of equivalent body mass or thoracic cage width. Although it is unclear whether the ancestral condition of clavicular length in anthropoids was similar to that of living Old or New World monkeys, an elongation of clavicle was an important step toward evolution of the modern body plan of hominoids.     

Regional distribution of adenosine deaminase in the human neuraxis

Adenosine deaminase was determined in 28 different areas of the human neuraxis in 5 adult male cadavers, with no known disease of the nervous system, using a very sensitive colorimetric method. The enzyme was highest in the frontal lobe white matter, and lowest in the medulla and all levels of the spinal cord. Enzyme content was about twice as great in the white matter of the frontal and temporal lobes and cerebellum as it was in the cortical gray matter of these areas, but only slightly higher in the white matter of the parietal and occipital lobes as compared to gray. Average values of the enzyme were found in the remaining areas of the brain, with the exception of the pons and cerebellar white matter, where a higher than average value was noted.     

Accelerated evolution of the electron transport chain in anthropoid primates

Mitochondria are both the power plant of the cell and a central integrator of signals that govern the lifespan, replication and death of the cell. Perhaps as a consequence, genes that encode components of the mitochondrial electron transport chain (ETC) are generally conserved. Therefore, it is surprising that many of these genes in anthropoid primates (New World monkeys, Old World monkeys and apes, including humans) have been major targets of darwinian positive selection. Sequence comparisons have provided evidence that marked increases of non-synonymous substitution rates occurred in anthropoid ETC genes that encode subunits of Complex III and IV, and the electron carrier molecule cytochrome c (CYC). Two important questions are: (i) how has evolution altered ETC function? and; (ii) how might functional changes in the ETC be linked to evolution of an expanded neocortical brain?     

Old world monkeys compare to apes in the primate cognition test battery

Understanding the evolution of intelligence rests on comparative analyses of brain sizes as well as the assessment of cognitive skills of different species in relation to potential selective pressures such as environmental conditions and social organization. Because of the strong interest in human cognition, much previous work has focused on the comparison of the cognitive skills of human toddlers to those of our closest living relatives, i.e. apes. Such analyses revealed that apes and children have relatively similar competencies in the physical domain, while human children excel in the socio-cognitive domain; in particular in terms of attention sharing, cooperation, and mental state attribution. To develop a full understanding of the evolutionary dynamics of primate intelligence, however, comparative data for monkeys are needed. We tested 18 Old World monkeys (long-tailed macaques and olive baboons) in the so-called Primate Cognition Test Battery (PCTB) (Herrmann et al. 2007, Science). Surprisingly, our tests revealed largely comparable results between Old World monkeys and the Great apes. Single comparisons showed that chimpanzees performed only better than the macaques in experiments on spatial understanding and tool use, but in none of the socio-cognitive tasks. These results question the clear-cut relationship between cognitive performance and brain size and--prima facie--support the view of an accelerated evolution of social intelligence in humans. One limitation, however, is that the initial experiments were devised to tap into human specific skills in the first place, thus potentially underestimating both true nonhuman primate competencies as well as species differences.     

Comparative study of musculature in goldon monkey (Rhinopithecus)

Some differences between the muscular system of three species of golden monkeys were shown. The major features of the myology in these animals, besides that ofCercopithecoidea, are similar to the anthropoid apes and humans. Although most of the features between taxa of golden monkeys are largely homologous, there are also some differences. Our results differ slightly from thosePatterson (1942) obtained inR. roxellanae. Some conclusions reported by Patterson were obviously incorrect, since the specimen he used did not have a head. Many mylogical characters are similar to other species ofCercopithecoidea while some resemble those of apes. Many are similar to those of the leaf monkey, though some of them show much more development. The golden monkey is more advanced than any other species ofCercopithecoidea. We hypothesize that in terms of the myological characters the golden monkeys seem to occupy a position between the leaf monkeys and the apes.