Ralph L. Holloway

Culture: A Human Domain

It is argued that a number of recent writings based on primate studies and on analysis of early hominid evolution have blurred certain central issues regarding human and non-human primate behavior. The central problem of how man organizes his experience and how he interacts with his environment is seldom squarely faced. A framework is provided here which examines tool-making in terms of psychological processes. It is argued that both tool-making and language come out of the same cognitive structure. The framework attempts to provide a means by which the appearance of emergent human behavior may be gauged from the fossil record. Two attributes, arbitrary form and imposition, are defined. It is argued that these two dimensions are specific to the human psychological structure, and that stone tools made to any standardized form satisfy the requirements of emergence in cognitive structure. Tool-making is analyzed using models for language behavior, and strong parallels are shown with certain design features that are specific to human communication. Tools are then viewed from the perspective of social psychological frameworks relating to the acquisition of norms of reference, perception, and the passage of objects from an unstructured to structured condition. This analysis suggests that arbitrary symbols played a major part in the development of social controls adaptive for early hominids utilizing strategies of division of labor, since symbols produce invariant relationships that can be defined outside of strictly biological relationships.

The Human Fossil Record

Brain Endocasts is the only comprehensive, single-volume work dealing exclusively and uniformly with fossil hominid brain endocasts. Never-beforepublished photographs come together with easily accessible, coherent descriptions to create a detailed reference on the paleoneurological evidence for human evolution. Each entry offers essential information related to the location, dating, associations, and morphology of a given endocast. The text also covers the latest methodologies and techniques available for studying endocasts. In addition, a concise summary shows how these fossil records contribute to our understanding of human evolution and behavior.

Brain shrinkage in chronic alcoholics: a pathological study.

A quantitative neuropathological necropsy study of 22 control and 22 chronic alcoholic subjects showed a statistically significant loss of brain tissue in the chronic alcoholic group. The loss of tissue appeared to be from the white matter of the cerebral hemispheres rather than the cerebral cortex. This may reflect a primary alteration in the composition or structure of the white matter or it may be secondary to loss of nerve cells from the cortex with subsequent degeneration of the axons in the white matter. Further morphometric analyses including cortical neuronal counts will be necessary to clarify this issue.

CULTURE, SYMBOLS, AND HUMAN BRAIN EVOLUTION: A SYNTHESIS

Conclusions and summary1.The brain has always played an important role in human evolution, but if brain size alone is the single neural variable considered, we cannot understand either the richness, complexity, or challenges inherent in a theory of human evolution. The brain is not simply a terminal product in mosaic human evolution.2.Brain size is only one phenotypic “window”, as it were, which allows the investigation of the role of the brain in human evolution. Of equal, if not more importance, are other phenotypic “windows”, on the brain such as its organizational (meaning the quantitative relationships among its parts) and its hierarchical development. This latter aspect refers to the species specific time-course of developmental, maturational, and social interactional and trans-actional patterns that shape the brain through natural selection.3.One aspect of brain size increase during human evolution relates to the geometric changes that took place in the central cortex. That is, one of the manifestations of increased cell size, decreased neuron density, increased dendritic branching, and increased glial/neural ratios, was an increase in absolute brain size. These aspects, albeit imperfectly, reflect one manifestation of neural complexity. Greater relative brain size, reorganization of cerebral tissues (e.g., the ratio of “association” cortex to primary visual cortex), hemispheric lateralization, and cognitive competence in symbolling and visuo-spatial integration, represent another set of neural evolutionary changes in Homo.4.While all animals may “learm” and perhaps even have “traditions,” no other being organizes its experiences in arbitrary symbol systems imposed by social groups, where there are non-iconic (arbitrary) relationships between the symbol(s) and referent. The power of this “new” language, integrated with “natural” neural “languages” is enormous, and escalates the complexity of social and material environments to which the human animal attends. Environments can be created through productivity and displacement. Culture is a human domain, if any definition of culture is to have meaning relative to the unique behavioral and cognitive patternings that typify the human being. It is impossible to understand the unique evolutionary past of our species without holistically integrating behavioral (cultural) and neural complexity, and the cognitive basis for both.5.Stone tool-making patterns from the prehistoric past should be viewed as indices or clues to the totality of complex social behavior in the past, rather than as targets for natural selection in the limited sense of tools as extrasomatic adaptations. Camping, living, manufacturing and butchering sites should be similarly viewed. The challenge is to try to understand these activities as clues to how social experience was organized and transmitted. In this framework, such activities reflect cultural and cognitive complexity and not cultural evolution per se.6.Prolonged dependency and growth periods must be integrated with the evolutionary changes in neural and cultural complexity. It is at this level that more molecular genetic changes, i.e., regulatory RNA, can be related to the more molar anthropologically-oriented evidence of the evolutionary past. Such changes in growth and dependency were probably dependent upon the development of affectional relationships between the sexes and members of social groups, which minimally increased the duration, if not intensity, of social, cooperative, nurturant relationships. Changes in sexual dimorphism, for example, which can only be inferred, are clues to those social relationships that set brain and behavioral complexity into a mutually-causal and interdependent evolutionary schema. The changes discussed above are the “initial kick” in that schema.

PALEONEUROLOGICAL EVIDENCE FOR LANGUAGE ORIGINS

If there is any hallmark that might be said to be unique to the human animal, it is surely the ability to speculate about the origin of language. I have too much respect and regard for the intellective capacities of chimpanzees to imagine them prone to such exercises in egoistic futility. Thus I approach the topic with a mild case of schizophrenic serenity, in which I simultaneously share a n agreement with the very rational Frenchmen of the Nineteenth Century who banned such discussions from their learned society, and yet share a delight that the topic is available for organized discussion from so many viewpoints, disciplines, and scientific experimentation as represented by the interactants of these conferences. For me, a t least, the very fact that this Conference has been organized, and that human animals are ready to engage in a great “garrulity” over the merits and demerits of essentially unprovable hypotheses, is an exciting testimony to the gap between human and other animals, whether continuous or not in nature. My assigned task is to assess the paleoneurological evidence for language resulting from our rather meager fossil hominid record. This is, at least on one level, an exceedingly simple task, since there is no good paleoneurological evidence as yet from the fossil hominid record that either proves or disproves when this or that hominid acquired the capacity for language. At the level of precise unambiguity, the endocasts leave much to be desired, as I have repeatedly emphasized. 1-8 Still, these are the most proximal evidencial links we have, and when combined with the other indirect lines of evidence from the fossil record, such as stone tools made to standardized patterns of arbitrary shape, or the rest of the musculoskeletal evidence, or the remaining archaeological record of different functioning sites, the combination raises significantly, I believe, the probability that this uniquely human activity came relatively early in hominid evolution, perhaps two to three million years ago.7-9 I have tried in most of my publications to suggest that “reorganization of the brain,” i.e., the study of the quantitative changes in the various neural systems of the brain and their integrated interactions, coupled with our ever-increasing knowledge of neurofunctioning, is a profitable way of approaching the problem of human (indeed any taxa) brain evolution. Most of those earlier publications were a reaction to the views most popular during the 40s to the early 60s, in which brain mass, taken alone, by and of itself, was regarded as the level a t which human behavioral specificities would be eventually understood. Consequently, I purposely played down the role of brain size alone in the case of human evolution. Perhaps I went too far, judging by the reactions of some of my critics.“J-13 Still, I never claimed that brain size was totally meaningless; only that it was insufficient as a lone datum level from which human behavioral evolution, or even a truly comparative neurobiology, could be understood.~4-~6 In the last few years this position is being met with serious rebuke by other scientists,lO-IJ who have raised a number of issues with greater clarity than existed before. In this paper, I will address myself to certain of these criticisms as they

The Failure of the Gyrification Index (GI) to Account for Volumetric Reorganization in the Evolution of the Human Brain

The gyrification indices (GI) recently compared for chimpanzee and human brains by Armstrong et al. (1991) ignores important volumetric differences in primary visual striate cortex (area 17 of Brodmann) and the lateral geniculate body which provides the optic radiation to the visual cortex. Allometric relationships for these structures are very strong in non-human primate brains based on the data of Stephan et al. (1981). In human brains, however, their observed empirical values are over 121 % less than expected for a primate of such a brain size. The regions that show the same overlap of values between chimpanzee and human cortex of the GI are not homologous given the sharp reduction in lateral extent of primary visual striate cortex in the human brain. The GI as used by these authors ignores important reorganizational changes between chimpanzee and human despite volume differences in brain size. Thus, it is doubtful that the GI can be used to assess the position of primary visual striate cortex in the Taung hominid endocast, or to argue for the primacy of brain enlargement before brain reorganization. To assess the simultaneity of volume and reorganizational changes in early hominid evolution, it will be essential to have a better understanding of the paleoneurological evidence. Although controversial, the Hadar AL 162-28 endocast of the 3 + MY Australopithecus afarensis provides evidence for morphometric reorganization of the occipital and parietal lobes of the brain prior to any dramatic increase in overall brain volume.

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 Brocas area was investigated in extant and extinct humans. Our results do not support positive allometry for the frontal lobes 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 Brocas 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.

Cortical Orofacial Motor Representation in Old World Monkeys, Great Apes, and Humans

Social life in anthropoid primates is mediated by interindividual communication, involving movements of the orofacial muscles for the production of vocalization and gestural expression. Although phylogenetic diversity has been reported in the auditory and visual communication systems of primates, little is known about the comparative neuroanatomy that subserves orofacial movement. The current study reports results from quantitative image analysis of the region corresponding to orofacial representation of primary motor cortex (Brodmann’s area 4) in several catarrhine primate species (Macaca fascicularis, Papio anubis, Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, and Homo sapiens) using the Grey Level Index method. This cortical region has been implicated in the execution of skilled motor activities such as voluntary facial expression and human speech. Density profiles of the laminar distribution of Nissl-stained neuronal somata were acquired from high-resolution images to quantify cytoarchitectural patterns. Despite general similarity in these profiles across catarrhines, multivariate analysis showed that cytoarchitectural patterns of individuals were more similar within-species versus between-species. Compared to Old World monkeys, the orofacial representation of area 4 in great apes and humans was characterized by an increased relative thickness of layer III and overall lower cell volume densities, providing more neuropil space for interconnections. These phylogenetic differences in microstructure might provide an anatomical substrate for the evolution of greater volitional fine motor control of facial expressions in great apes and humans.

Endocast of Sambungmacan 3 (Sm 3): a new Homo erectus from Indonesia.

A new fossil calvaria, Sambungmacan 3 (Sm 3), described in New Fossil Hominid Calvaria From Indonesia—Sambungmacan 3 by Márquez et al., this volume, yields one of the most advanced and complete endocasts yet recovered from Java. This communication provides a thorough interpretation of the external anatomical landmarks observable on Sm 3. Using computer tomography (CT) and traditional morphological measurements, our comparative paleoneurological analyses show that while Sm 3 has a mosaic of features that are similar to both Indonesian and Chinese H. erectus, it also possesses significant characters reminiscent of later hominins. These include a greater degree of asymmetry characterized by a possible left‐occipital, right‐frontal petalial pattern, left‐right volumetric cerebral asymmetry, and marked asymmetry in Brocas cap. Moreover, the frontal lobe offers a more rounded, shortened appearance in contrast to the flat, elongated appearance of other Indonesian fossils (e.g., Sangiran 17). Another unique trait is exhibited in the transverse plane where the widest breadth of Sm 3 occurs more superiorly than in other Indonesian H. erectus. Thus, the endocast of Sm 3 presents a unique morphology not seen previously in the hominin fossil record. While the strong modern human characteristics in this endocast may not represent a particular ancestry, they do allow us to recognize a new dimension of the remarkable variation in Indonesian Homo erectus. Anat Rec 262:369–379, 2001.

Cortical orofacial motor representation in Old World monkeys, great apes, and humans. II. Stereologic analysis of chemoarchitecture.

This study presents a comparative stereologic investigation of neurofilament protein- and calcium-binding protein-immunoreactive neurons within the region of orofacial representation of primary motor cortex (Brodmann’s area 4) in several catarrhine primate species (Macaca fascicularis, Papio anubis, Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, and Homo sapiens). Results showed that the density of interneurons involved in vertical interlaminar processing (i.e., calbindin- and calretinin-immunoreactive neurons) as well pyramidal neurons that supply heavily-myelinated projections (i.e., neurofilament protein-immunoreactive neurons) are correlated with overall neuronal density, whereas interneurons making transcolumnar connections (i.e., parvalbumin-immunoreactive neurons) do not exhibit such a relationship. These results suggest that differential scaling rules apply to different neuronal subtypes depending on their functional role in cortical circuitry. For example, cortical columns across catarrhine species appear to involve a similar conserved network of intracolumnar inhibitory interconnections, as represented by the distribution of calbindin- and calretinin-immunoreactive neurons. The subpopulation of horizontally-oriented wide-arbor interneurons, on the other hand, increases in density relative to other interneuron subpopulations in large brains. Due to these scaling trends, the region of orofacial representation of primary motor cortex in great apes and humans is characterized by a greater proportion of neurons enriched in neurofilament protein and parvalbumin compared to the Old World monkeys examined. These modifications might contribute to the voluntary dexterous control of orofacial muscles in great ape and human communication.