Geometric morphometrics and paleoneurology: brain shape evolution in the genus Homo

Paleoneurology concerns the study and analysis of fossil endocasts. Together with cranial capacity and discrete anatomical features, shape can be analysed to consider the spatial relationships between structures and to investigate the endocranial structural system. A sample of endocasts from fossil specimens of the genus Homo has been analysed using traditional metrics and 2D geometric morphometrics based on lateral projections of endocranial shape. The maximum and frontal widths show a size-related pattern of variation shared by all the taxa considered. Furthermore, as cranial capacity increases in the non-modern morphotypes there is a general endocranial vertical stretching (mainly centred at the anterior ascending circumvolution) with flattening and relative shortening of the parietal areas. This pattern could have involved some structural stress between brain development and vault bones at the parietal midsagittal profile in the heavy encephalised Neandertals. In contrast, modern humans show a species-specific neomorphic hypertrophy of the parietal volumes, leading to a dorsal growth and ventral flexion (convolution) and consequent globularity of the whole structure. Brain tensors such as the falx cerebri have been hypothesised to represent one of the main physical constraints on morphogenetic trajectories, with additional influences from cranial base structures. The neurofunctional inferences discussed here stress the role of the parietal areas in the visuo-spatial coordination and integration, which can be involved in higher cerebral functions and related to conceptual thinking.     

Variation in enamel thickness within the genus Homo

Recent humans and their fossil relatives are classified as having thick molar enamel, one of very few dental traits that distinguish hominins from living African apes. However, little is known about enamel thickness in the earliest members of the genus Homo, and recent studies of later Homo report considerable intra- and inter-specific variation. In order to assess taxonomic, geographic, and temporal trends in enamel thickness, we applied micro-computed tomographic imaging to 150 fossil Homo teeth spanning two million years. Early Homo postcanine teeth from Africa and Asia show highly variable average and relative enamel thickness (AET and RET) values. Three molars from South Africa exceed Homo AET and RET ranges, resembling the hyper thick Paranthropus condition. Most later Homo groups (archaic European and north African Homo, and fossil and recent Homo sapiens) possess absolutely and relatively thick enamel across the entire dentition. In contrast, Neanderthals show relatively thin enamel in their incisors, canines, premolars, and molars, although incisor AET values are similar to H. sapiens. Comparisons of recent and fossil H. sapiens reveal that dental size reduction has led to a disproportionate decrease in coronal dentine compared with enamel (although both are reduced), leading to relatively thicker enamel in recent humans. General characterizations of hominins as having ‘thick enamel’ thus oversimplify a surprisingly variable craniodental trait with limited taxonomic utility within a genus. Moreover, estimates of dental attrition rates employed in paleodemographic reconstruction may be biased when this variation is not considered. Additional research is necessary to reconstruct hominin dietary ecology since thick enamel is not a prerequisite for hard-object feeding, and it is present in most later Homo species despite advances in technology and food processing.     

A bivariate approach to the widening of the frontal lobes in the genus Homo

Within the genus Homo, the most encephalized taxa (Neandertals and modern humans) show relatively wider frontal lobes than either Homo erectus or australopithecines. The present analysis considers whether these changes are associated with a single size-based or allometric pattern (positive allometry of the width of the anterior endocranial fossa) or with a more specific and non-allometric pattern. The relationship between hemispheric length, maximum endocranial width, and frontal width at Broca's area was investigated in extant and extinct humans. Our results do not support positive allometry for the frontal lobe's width in relation to the main endocranial diameters within modern humans (Homo sapiens). Also, the correlation between frontal width and hemispheric length is lower than the correlation between frontal width and parieto-temporal width. When compared with the australopithecines, the genus Homo could have experienced a non-allometric widening of the brain at the temporo-parietal areas, which is most evident in Neandertals. Modern humans and Neandertals also display a non-allometric widening of the anterior endocranial fossa at the Broca's cap when compared with early hominids, again more prominent in the latter group. Taking into account the contrast between the intra-specific patterns and the between-species differences, the relative widening of the anterior fossa can be interpreted as a definite evolutionary character instead of a passive consequence of brain size increase. This expansion is most likely associated with correspondent increments of the underlying neural mass, or at least with a geometrical reallocation of the frontal cortical volumes. Although different structural changes of the cranial architecture can be related to such variations, the widening of the frontal areas is nonetheless particularly interesting when some neural functions (like language or working memory, decision processing, etc.) and related fronto-parietal cortico-cortical connections are taken into account.     

Limb-size proportions in Australopithecus afarensis and Australopithecus africanus

Previous analyses have suggested that Australopithecus africanus possessed more apelike limb proportions than Australopithecus afarensis. However, due to the errors involved in estimating limb length and body size, support for this conclusion has been limited. In this study, we use a new Monte Carlo method to (1) test the hypothesis that A. africanus had greater upper:lower limb-size proportions than A. afarensis and (2) assess the statistical significance of interspecific differences among these taxa, extant apes, and humans. Our Monte Carlo method imposes sampling constraints that reduce extant ape and human postcranial measurements to sample sizes comparable to the fossil samples. Next, composite ratios of fore- and hindlimb geometric means are calculated for resampled measurements from the fossils and comparative taxa. Mean composite ratios are statistically indistinguishable (alpha=0.05) from the actual ratios of extant individuals, indicating that this method conserves each sample's central tendency. When applied to the fossil samples, upper:lower limb-size proportions in A. afarensis are similar to those of humans (p=0.878) and are significantly different from all great ape proportions (p< or =0.034), while Australopithecus africanus is more similar to the apes (p> or =0.180) and significantly different from humans and A. afarensis (p< or =0.031). These results strongly support the hypothesis that A. africanus possessed more apelike limb-size proportions than A. afarensis, suggesting that A. africanus either evolved from a more postcranially primitive ancestor than A. afarensis or that the more apelike limb-size proportions of A. africanus were secondarily derived from an A. afarensis-like ancestor. Among the extant taxa, limb-size proportions correspond with observed levels of forelimb- and hindlimb-dominated positional behaviors. In conjunction with detailed anatomical features linked to arboreality, these results suggest that arboreal posture and locomotion may have been more important components of the A. africanus behavioral repertoire relative to that of A. afarensis.     

A new Homo erectus (Zhoukoudian V) brain endocast from China

A new Homo erectus endocast, Zhoukoudian (ZKD) V, is assessed by comparing it with ZKD II, ZKD III, ZKD X, ZKD XI, ZKD XII, Hexian, Trinil II, Sambungmacan (Sm) 3, Sangiran 2, Sangiran 17, KNM-ER 3733, KNM-WT 15 000, Kabwe, Liujiang and 31 modern Chinese. The endocast of ZKD V has an estimated endocranial volume of 1140 ml. As the geological age of ZKD V is younger than the other ZKD H. erectus, evolutionary changes in brain morphology are evaluated. The brain size of the ZKD specimens increases slightly over time. Compared with the other ZKD endocasts, ZKD V shows important differences, including broader frontal and occipital lobes, some indication of fuller parietal lobes, and relatively large brain size that reflect significant trends documented in later hominin brain evolution. Bivariate and principal component analyses indicate that geographical variation does not characterize the ZKD, African and other Asian specimens. The ZKD endocasts share some common morphological and morphometric features with other H. erectus endocasts that distinguish them from Homo sapiens.     

Developmental and regional distribution of aspartoacylase in rat brain tissue

The function of N-acetyl-aspartate (NAA), a predominant molecule in the brain, has not yet been determined. However, NAA is commonly used as a putative marker of viable neurones. To investigate the possible function of NAA, we determined the anatomical, developmental and cellular distribution of aspartoacylase, which catalyses the hydrolysis of NAA. Levels of aspartoacylase activity were measured during postnatal development in several brain regions. The differential distribution of aspartoacylase activity in purified populations of cells derived from the rat CNS was also investigated. The developmental and anatomical distribution of aspartoacylase correlated with the maturation of white matter tracts in the rat brain. Activity increased markedly after 7 days and coincided with the time course for the onset of myelination in the rat brain. Gray matter showed little activity or developmental trend. There was a 60-fold excess in optic nerve (a white matter tract) when compared with cortex at 21 days of development. In the adult brain there was a 18-fold difference in corpus callosum compared with cortex (stripped of corpus callosum). Cellular studies demonstrated that purified cortical neurons and cerebellar granular neurones have no activity. Primary O-2A progenitor cells had moderate activity, with three-fold higher activity in immature oligodendrocyte and 13-fold increase in mature oligodendrocytes (myelinating cells of the CNS). The highest activity was seen in type-2 astrocytes (20-fold difference compared with O-2A progenitors) derived from the same source. Aspartoacylase activity increased with time in freshly isolated astrocytes, with significantly higher activity after 15 days in culture. We conclude that aspartoacylase activity in the developing postnatal brain corresponds with maturation of myelination, and that the cellular distribution is limited to glial cells.     

Volumetric and asymmetry determinations on recent hominid endocasts: Spy I and II,Djebel Ihroud I,and the salè Homo erectus specimens,with some notes on neandertal brain size

Full brain endocast reconstructions of the Neandertals, Spy I and II, Djebel Ihroud I, and the Homo erectus specimen from Salè, Morocco have yielded accurate volumes. Spy I = 1,305 ml; Spy II = 1,553 ml; Djebel Ihroud I = 1,305 ml; Salè = 880 ml. While there are no remarkable gyral and sulcal patterns one can delineate, the brain endocasts do show evidence of left-occipital, right-frontal petalias, suggesting right-handedness, and possibly human cognitive specialization, involving symbol processing and visuospatial integration. Some speculations regarding Neandertal brain size are also offered, in which it is suggested that their possibly larger brain sizes were related to greater muscularity than in modern Homo sapiens.     

Brain organization and the origin of insects: an assessment

Within the Arthropoda, morphologies of neurons, the organization of neurons within neuropils and the occurrence of neuropils can be highly conserved and provide robust characters for phylogenetic analyses. The present paper reviews some features of insect and crustacean brains that speak against an entomostracan origin of the insects, contrary to received opinion. Neural organization in brain centres, comprising olfactory pathways, optic lobes and a central neuropil that is thought to play a cardinal role in multi-joint movement, support affinities between insects and malacostracan crustaceans.     

The metabolic cost of walking in humans, chimpanzees, and early hominins

Bipedalism is a defining feature of the hominin lineage, but the nature and efficiency of early hominin walking remains the focus of much debate. Here, we investigate walking cost in early hominins using experimental data from humans and chimpanzees. We use gait and energetics data from humans, and from chimpanzees walking bipedally and quadrupedally, to test a new model linking locomotor anatomy and posture to walking cost. We then use this model to reconstruct locomotor cost for early, ape-like hominins and for the A.L. 288 Australopithecus afarensis specimen. Results of the model indicate that hind limb length, posture (effective mechanical advantage), and muscle fascicle length contribute nearly equally to differences in walking cost between humans and chimpanzees. Further, relatively small changes in these variables would decrease the cost of bipedalism in an early chimpanzee-like biped below that of quadrupedal apes. Estimates of walking cost in A.L. 288, over a range of hypothetical postures from crouched to fully extended, are below those of quadrupedal apes, but above those of modern humans. These results indicate that walking cost in early hominins was likely similar to or below that of their quadrupedal ape-like forebears, and that by the mid-Pliocene, hominin walking was less costly than that of other apes. This supports the hypothesis that locomotor energy economy was an important evolutionary pressure on hominin bipedalism.     

Early evidence of the genus Homo in East Asia

The timing and route of the earliest dispersal from Africa to Eastern Asia are contentious topics in the study of early human evolution because Asian hominin fossil sites with precise age constraints are very limited. Here we report new high-resolution magnetostratigraphic results that place stringent age controls on excavated hominin incisors and stone tools from the Yuanmou Basin, southwest China. The hominin-bearing layer resides in a reverse polarity magnetozone just above the upper boundary of the Olduvai subchron, yielding an estimated age of 1.7Ma. The finding represents the age of the earliest documented presence of Homo, with affinities to Homo erectus, in mainland East Asia. This age estimate is roughly the same as for H. erectus in island Southeast Asia and immediately prior to the oldest archaeological evidence in northeast Asia. Mammalian fauna and pollen obtained directly from the hominin site indicate that the Yuanmou hominins lived in a varied habitat of open vegetation with patches of bushland and forest on an alluvial fan close to a lake or swamp. The age and location are consistent with a rapid southern migration route of initial hominin populations into Eastern Asia.     

The evolution of brain size and intelligence in man

The brain size of hominids has increased approximately threefold during the evolution of the hominids fromAustralopithecus toHomo sapiens. It is proposed that the principal reason for this increase is that larger brains conferred greater intelligence, and greater intelligence conferred a selection advantage. A number of anthropologists have difficulty accepting this thesis because they believe that brain size is not associated with intelligence in man. Evidence is reviewed, and new evidence from two studies is presented, to show that brain size as measured by head size is positively correlated with intelligence as measured by intelligence tests. On two recent samples statistically significant correlations of .21 and .30 were obtained between estimates of brain size and IQ. It is considered that brain size is positively associated with intelligence in man and that this is the major reason for the increase in brain size of the hominids during the last 3.2 million years.     

Endocranial shape asymmetries in Pan paniscus, Pan troglodytes and Gorilla gorilla assessed via skull based landmark analysis

Brain shape asymmetries or petalias consist of the extension of one cerebral hemisphere beyond the other. A larger frontal or caudal projection is usually coupled with a larger lateral extent of the more projecting hemisphere relative to the other. The concurrence of these petalial components is characteristic of hominins. Studies aimed at quantifying petalial asymmetries in human and great ape endocasts rely on the definition of the midline of the endocranial surface. Studies of brain material show that, at least in humans, most of the medial surface of the left occipital lobe distorts along the midline and protrudes on to the right side, making it difficult for midline and corresponding left and right reference point identification. In order to accurately quantify and compare brain shape asymmetries in extant hominid species, we propose here a new protocol based on the objective definition of cranial landmarks. We describe and quantify for the first time in three dimensions the positions of frontal and occipital protrusions in large samples of Pan paniscus, Pan troglodytes and Gorilla gorilla. This study confirms the existence of frontal and occipital petalias in African apes. Moreover, the detailed analysis of the 3D structure of these petalias reveals shared features, as well as features that are unique to the different great ape species.     

Apples, oranges, and the lunate sulcus

Holloway (1984) used a method of direct tape-arc measurements on chimpanzee brain casts to reject the hypothesis that the lunate sulcus is located in an anterior position in the Taung endocast. However, Holloway neglected to measure the occipital pole-lunate sulcus (OP-LS) arc directly on the Taung endocast as he did on chimpanzee brain casts (a crucial part of his methodology); instead, he determined the relative position of Taung's lunate sulcus on the basis of a calculation that confounds direct measurements and measurements from photographs. When arc OP-LS is measured directly on Taung according to Holloway's methods, the feature that has been identified as the medial end of the lunate sulcus is shown to be located within the range that Holloway determined for chimpanzees. Thus Holloway's methodology and data support rather than refute the claim that the lunate sulcus is located in a pongid-like position in australopithecines.     

Competition,niche specialization and the evolution of brain size in the genus Peromyscus

Previous studies of relative brain size in mammals have suggested an association with complex habitats and with low reproductive rate. In order to examine the causal relationships more thoroughly, a detailed examination of relative brain size variation in the genus Peromyscus was undertaken. Endocranial volumes were used to estimate brain weight for 32 species including 161 subspecies, and relative brain size calculated as the species deviation from the allometric relationship between brain and body size. The intrageneric allometric coefficient was higher than most values previously reported from low taxonomic levels, but intraspecific coefficients were generally lower than this. Island species, and relict species isolated on mountain tops, which may be ecological ‘islands’, had consistently small relative brain sizes, but peninsular species were large brained. Among the remaining species there were significant correlations between litter size and relative brain size, and between the number of competitor species and relative brain size. Species with many competitor species have relatively large brains and small litters. It is concluded that the nature of the geographical distribution, the pattern of species formation and habitat complexity all influence relative brain size in existing forms.     

Competition, niche specialization and the evolution of brain size in the genus Peromyscus

Previous studies of relative brain size in mammals have suggested an association with complex habitats and with low reproductive rate. In order to examine the causal relationships more thoroughly, a detailed examination of relative brain size variation in the genus Peromyscus was undertaken. Endocranial volumes were used to estimate brain weight for 32 species including 161 subspecies, and relative brain size calculated as the species deviation from the allometric relationship between brain and body size. The intrageneric allometric coefficient was higher than most values previously reported from low taxonomic levels, but intraspecific coefficients were generally lower than this.
Island species, and relict species isolated on mountain tops, which may be ecological 'islands', had consistently small relative brain sizes, but peninsular species were large brained. Among the remaining species there were significant correlations between litter size and relative brain size, and between the number of competitor species and relative brain size. Species with many competitor species have relatively large brains and small litters. It is concluded that the nature of the geographical distribution, the pattern of species formation and habitat complexity all influence relative brain size in existing forms.     

Application of PIXE analysis to the study of the regional distribution of trace elements in normal human brain

A particle-induced X-ray emission (PIXE) analysis method is presented, which allows measurement of eight elements (i.e., K, Ca, Mn, Fe, Cu, Zn, Se, and Rb) in human brain samples of only a few mg dry weight. The precision and accuracy of the method were investigated by analyzing animal brain matter with both PIXE and instrumental neutron activation analysis (INAA). The method was applied to measure the 8 elements in 46 different regions of 3 human brains. The sections analyzed originated from either the left or the right cerebral hemisphere, brain stem, and cerebellum. For one of the brains, sections were also analyzed from 26 corresponding regions of both hemispheres. For all elements, similar concentrations were found in the corresponding areas of the left and right sides of the brain. The concentrations (in μg/g dry weight) of the elements K, Fe, Cu, Zn, Se, and Rb were consistently higher in cortical structures than in white matter. Deep nuclei and brain stem, which have a mixed composition, showed intermediate values for K, Zn, Se, and Rb. A hierarchical cluster analysis indicated that the various brain regions clustered into two large groups, one comprising gray and mixed matter regions and the other, white and mixed matter brain areas.     

Developmental changes and regional distribution of phospholipase D and base exchange enzyme activities in rat brain

Phospholipase D (PL-D) activity per mg protein of whole homogenate increased 5.1 fold between Embryonic (E) day 17 and Postpartum (P) day 14 and slightly decreased by P 30 days. This was due to the decrease of PL-D activity of the P₂ fraction. The PL-D activity of P₂ and P₃ fractions increased 11.2 and 6.1 fold respectively between E 17 and P 14. The 3 base exchange enzyme (BEE) activities per mg protein of whole homogenate increased up to P 14 or P 21 and then decreased. This decrease was greater in the P₂ fraction and the P₃ fraction increased after P14. Brains from 1 day to 25 month old rats were dissected into 7 separate regions and both PL-D and BEE activities were measured. In adult rats, the hippocampus and hypothalamus had the highest PL-D activities while medulla+pons and cerebellum had the lowest PL-D activities. The developmental patterns of 5 regions except for hippocampus and hypothalamus were similar. PL-D activity in the hippocampus was maximum at P 7 followed by a steep decrease till P30 suggesting that the PL-D activity of the hypothalamus develops later and that of the hippocampus develops earlier than any other region. The distributions of BEE activities were quite different from those of PL-D activities. In adult rats, the cerebellum had the highest activity while the striatum and medulla+pons had the lowest. The BEE activities of cerebellum were lowest at P 1 and showed steep increase during the next 2 weeks.To whom to address reprint request are to be sent.     

A combined analysis of regional energy metabolism and immunohistochemical ischemic damage in the gerbil brain

By combining immunohistochemical technique with microassay methods, we analyzed regional energy metabolism in vulnerable and tolerant areas of gerbil brains during evolution of neuronal damage after bilateral common carotid artery occlusion for 10 min with subsequent reperfusion. Four animals were used for each reperfusion period. Based on the information from the immunohistochemical examination, we dissected out vulnerable and tolerant subregions of the hippocampus, cerebral cortex, and thalamus from freeze-dried 20-microm-thick sections, and measured the levels of creatine phosphate (P-Cr), adenine nucleotides, guanine nucleotides, and purine bodies by HPLC, and the levels of glucose, glycogen, and lactate by an enzyme-immobilized column method. There were no significant differences in the levels of metabolites between vulnerable and tolerant subregions of control brains. After reperfusion, both vulnerable and tolerant subregions recovered preischemic metabolic profiles by 2 days. Although the regional differences between vulnerable and tolerant subregions were minimal at each reperfusion period, there were delays in the recovery of P-Cr, ATP, and/or total adenine nucleotides in all vulnerable subregions. A decline of P-Cr, ATP, and GTP levels without change in %ATP, AMP, or purine bodies occurred after reperfusion for 3 days, coinciding with the development of immunohistochemical damage by the immunoreaction for microtubule-associated protein 1A. The results supported the notion that subtle but sustained impairment of energy metabolism caused by mitochondrial dysfunction in the early reperfusion period might trigger delayed neuronal death in vulnerable subregions.