Asymmetry from molecules to mind. Review of The Evolution of Lateral Asymmetries Language Tool Use and Intellect J. Bradshaw and L. Rogers. New York Academic Press 1993 xii + 463 pp $72код для вставкиСкачать
American Journal of Primatology 33:323-327 (1994) BOOK REVIEWS Asymmetry From Molecules to Mind Review of The Evolution of Lateral Asymmetries, Language, Tool Use, and Intellect, J. Bradshaw and L. Rogers. New York, Academic Press, 1993,xii + 463 pp, $72.00. This book seeks to integrate information about asymmetries across the animal kingdom, particularly with reference to the question of how the asymmetries present in humans are related to the characteristically human capacities of language, tool use, and intellect. The authors consider the question of asymmetries in human behavior as “one of the three great mysteries”, the other two being the origins of matter and life. They suggest that the unique characteristics of humans (consciousness,praxis, tool use, language, and art) are very recent, and that all can be related to cerebral asymmetry. Asymmetry thus looms large as a uniting concept which may allow integration of findings and thinking about the human condition from diverse fields of inquiry. The authors themselves come from quite different scientific backgrounds (Rogers in comparative behavioral and developmental psychobiology;Bradshaw in human evolution and cognition); the strengths of each author are showcased in turn in the various chapters addressing these differing perspectives on lateral asymmetry. Integrating the enormous corpus of literature and the broad sweep of topics they consider is a daunting task, and they manage it rather well, on the whole. Lateral asymmetry is receiving increasing interest from primatologists [e.g., the 1993 volume edited by Ward & Hopkinsl, in line with its increasing visibility in human cognitive neuroscience [e.g., Geschwind & Galaburda, 1987; Corballis, 19911. Comparative interests in behavioral asymmetry were given a provocative theoretical boost by MacNeilage, Studdert-Kennedy, and Lindblom [19871, in their well-known article posing postural origins for the evolution of neuromotor asymmetries in primates. This volume provides an even larger evolutionary view of the evolution of laterality than that proposed by MacNeilage et al. [19871: It looks beyond the order Primates, into molecular and organismic sources of lateral asymmetry across orders. In so doing, it provides a challenge to primatologists to clarify what aspects of asymmetry, if any, are unique to primates, and how these arise, developmentally and phylogenetically. The book opens with discussion of the sources of biological asymmetries in carbon molecules, organic molecules, RNA and amino acids, and cytoplasm. As the authors make very clear in the early chapters of the book, structural asymmetry is a condition of life; what begs explanation is not the presence of asymmetry, but rather its developmental patterns and consequences. Thus a good deal of space is given over to presenting available data on the development of asymmetries across animal phyla. To one not versed in the arcane literature of developmental morphological asymmetries in animals, the history of claw development in lobsters, or of body flattening in flatfish, class Osteichthyes, made fascinating reading. But the main focus of these authors is not on visible structural asymmetries, ubiquitous as they may be. Rather, the main focus is on behavioral asymmetries, which for the most part are mediated by the central nervous system. Thus, the 0 1994 Wiley-Liss, Inc. 324 I Fragaszy discussion quickly turns to neural asymmetries. Some of the most exciting findings regarding behavioral and neural asymmetries come from Rogers’ and colleagues’ work with chickens. The chicken turns out to be a stellar experimental system in which to investigate the development of behavioral asymmetries, particularly those mediated by vision, and their neural structural correlates. Visual pathways in birds, as in some mammals with laterally placed eyes, cross over almost completely a t the optic chiasm, so that monocular vision restricts visual input to one hemisphere of the brain. Moreover, unlike all mammals, birds have relatively few commissures connecting the two halves of the forebrain. Birds (except owls, with forward-facing eyes) frequently move the eyes independently to scan the environment, and the two eyes can focus independently. Functionally, birds have two independent eyes, and two independent visual systems that receive information from these eyes. If unihemispheric processing dominates and visual field information is essentially monocular, asymmetries in control of various behaviors are inevitable, to prevent conflict between the hemispheres. In short, the nature of the visual system set the stage for the evolution, retention, and/or elaboration of laterized brain functions in birds. Developmentally, structural and chemical asymmetries in the visual system have been shown to emerge in the chick from the organizing effects of light on the eye that is facing toward the shell, and thus is stimulated by light before hatching. Typically, the right eye faces the shell, and this population-wide positional bias, leading to differential stimulation between the two eyes, starts a cascading series of differentiating events in the nervous system. Behavioral lateralization is evident in many visually guided behaviors in chickens, such as rate of discrimination learning (better when the right eye is used), or detection of novelty (better when the left eye is used), copulatory behavior, and attack behavior (which occur more readily when the left eye is used). This is psychobiological developmental sleuthing a t its best. One lesson to be learned from birds about asymmetry is that lateralization can take many forms in addition to simple dominance of one hemisphere over another in some particular function. It can take the form of complementary specialization or differential use for the same function, or the form of different neural sites, neurochemical changes, or integration of pathways. A second lesson is that the emergence of asymmetry is epigenetic: i t is a consequence of a dynamic developmental process in which environmental conditions influence cellular metabolism. Lateral asymmetries in mammals have been most studied in rodents. Laterality in rats and mice is randomly distibuted (i.e., there is no population bias toward one side) for paw preference in reaching, direction of circling, and tail posture. This form of lateralization depends on laterality of neurotransmission, particularly that mediated by dopamine, in the nigrostriatum (not the cortex). For other characteristics, a population-wide bias is evident. The right side of the body (left hemisphere of the brain) is more involved in sequential processing and processing of species-specific vocalizations; the left side of the body (right side of the brain) for control of spatial behavior, affective behavior, and parallel processing. These asymmetries depend upon processing differences in the cortex. Control of sexual behavior is also lateralized in the population, and this is associated with asymmetries of neurotransmission in the hypothalamus. These patterns are similar in broad measures to those seen in humans, so rats and mice do make respectable models of behavioral asymmetries in humans. Therefore, we may uncover in rodents, aspects of laterality that we did not suspect existed in primates, and then find them in primates. This seems to be underway with brain modulation of the immune system. Asymmetry From Molecules to Mind I 325 Developmentally, asymmetry in rodents is influenced by sex hormones and experience (such as handling). The particular roles and extent of influence of the two hemispheres on each other appears to be influenced by the size of the corpus callosum, and the size of the corpus callosum has been shown to be sensitive to various developmental experiences. It has been shown that various stresses can induce a population-wide bias for the left eye to open before the right, which may trigger a similar cascade of developmental processes as were illustrated in chickens. Moreover, the form and extent of lateralization in the adult brain is not static-it can change. This has been shown to be true in primates, as well. As recent work cited in this volume on the topographic representation of body parts in primates illustrates, the brain is really more like software than hardware. Asymmetries in primates have been most studied in terms of motor activity (manual preferences), cognitive processes, and brain morphology. The debate in the primate community is whether there are population-wide biases in any aspect of functioning like those observed in humans. Much attention has been devoted to hand preferences, drawing upon the obvious human population bias for righthandedness, and upon MacNeilage et al.’s [19871 theory linking posture and lateral biases in prehension in primate evolution. Unfortunately for this effort, the literature on hand preferences in nonhuman primates is worse than messy for virtually every aspect of design, including numbers of subjects, nature of tasks, scoring procedures, and statistical methods [see Hopkins & Morris, 1993 for a recent review of this problem]. Although it is easy to find individual lateral biases in primates for many actions, it is extraordinarily difficult to draw clear conclusions about the origins or implications of these biases. At. present, several studies by Jeannette Ward’s group reviewed in this volume, suggest that prosimians display a population bias for left-hand reaching for prey capture, and that both age and sex influence the degree of lateral bias. Otherwise, there are controversial claims for the presence of a right-handed bias for reaching in the great apes, and no general findings for monkeys. Better luck has been had with the search for cognitive asymmetries. Perceptual processes have been one focus of this search, and in general humans and nonhuman primates appear similar in these studies. A right-hemisphere advantage has been demonstrated in a few studies of tactile discrimination and visually monitored spatial adjustments. Visual discrimination of faces appears to be mediated prinicipally by the right hemisphere, as in humans. Species-specific vocalizations are better discriminated by the left hemisphere. Work on language-proficient apes has demonstrated left-hemisphere advantage in processing “meaningful” visual stimuli, and a right hemisphere advantage in processing “nonsense” stimuli-a finding parallel to that with humans. Two chapters deal with human evolution. one concerning early human evolution and migrations, and the other concerning the rise of tool-use, art, and culture in prehistoric peoples. These were admirably comprehensive in coverage, including careful attention to the reports on lateral asymmetries in the apes, and attention to reports on tool-using and other evidence of cognitive complexity in nonhuman primates. The authors’ portrayal of the firmness of the conclusions drawn from the reports of behavior in apes and other nonhuman primates is unsettling, however. This is clearly not the literature in which they feel at home. Rather than drawing upon the comparative literature critically, as they do in the sections on studies in other taxa, human evolution, and language, they generally have accepted the conclusions of the authors of the original reports they cite, in their broadest interpretation. Consequently, they present too tidy a picture of cognitive and behavioral continuity across taxa of nonhuman primates. 326 I Fragaszy But keeping the overall scope of the book in mind, this is a picky criticism from a primatologist sensitized to the interpretation of these kinds of observational data. In the main, these chapters did not deal with the comparative data; they dealt with the emergence of uniquely human activities of using fire, burial rituals, and art. A dextral bias is already evident in the manufacture of tools in the Oldowan period, and becomes more widespread in more modern peoples. As the authors note, (a) tool-using behaviors are not uniquely human, and (b) humanmade tools remained very simple in design and manufacture for a very long time, even while brain size was changing rather dramatically. They conclude that selective advantage afforded by tool-using behaviors was certainly not the only influence on human evolution during this era, and in fact probably not even an important one. The emergence of more advanced tools appears to have happened rather suddenly, in what ;he authors term the “cultural explosion’’ of the upper Paleolithic period in Europe, which they suggest happened when anatomically modern humans met up with, and eventually outlasted, the extant Neanderthal population. In a concluding chapter, an integrated view of the nature and evolution of language and speech is attempted. The neurological substrates of language partly involve those cortical areas of the parietal lobe in the left hemisphere that in the right hemisphere are given over to spatial processing and that support visuoperceptual pattern recognition. The authors argue that language cannot be linked too tightly to art through common evolutionary origins or neural mechanisms of symbolism, categorization, and referencing. Similarly, it cannot be linked too tightly to tool construction and use, or other behaviors that involve sequential and syntactic elements. In short they argue that the popular scenario of upright posture freeing the hands, leading to tool-use, and subsequently leading to language, should be discarded. Gestures appear phylogenetically either independently of tool-use, or well before-shared gestures are quite apparent in chimpanzees and humans, but shared tool-use is much less apparent. The authors conceive of the evolution of intelligence and encephalization in terms of mosaic changes in tool-use and technology, social interchange and society, consciousness and understanding, and intellect. Thus, there is no single causative factor responsible for the emergence of language. The authors conclude, very humbly after 387 pages of text on the subject, that “It is easy to overemphasize the role of cerebral asymmetry and behavioral lateralities in human evolution . . . Cerebral asymmetry is just one dichotomy among, for example, cortical-subcortical, anterior-posterior, and so on. However, it is a neat and clear division, . . . and the functions so divided do seem to address some so-called uniquely human characteristics . . . On the one hand, we have tried to show that these characteristics may not be nearly so uniquely human after all; on the other hand, we have also tried to show that . . . neither are we so unique as previously thought in being overtly o r covertly asymmetrical. . . . Behavioral asymmetries are common in all genera, being evident even half a billion years ago. We have not crossed a Rubicon, linguistic or otherwise; we are merely rather further out on a number of evolutionary limbs . . .” (pp. 387-388). Given that they started the volume by claiming human asymmetries to be one of the three “great mysteries of life”, it seems that the authors could find life rather dull from here on, unless, of course, they recognize the remaining fundamental questions about asymmetries (of development, of integration, of function) as holding equivalent interest. We still have a long way to go before we fully understand asymmetries in our order. We would be wise to consider the ubiquity of the phe- Asymmetry From Molecules to Mind I 327 nomena across orders, as these authors have ably done, before investing too m u c h effort in creating primate-specific explanations for the varied asymmetries found in our own order. Dorothy M. Fragaszy Department of Psychology University of Georgia Athens, Georgia REFERENCES Corballis, M. C. THE LOPSIDED APE. New York, Oxford University Press, 1991. Geschwind, N.; Galaburda, A. M. CEREBRAL LATERALIZATION: BIOLOGICAL MECHANISMS, ASSOCIATIONS, AND PATHOLOGY. Cambridge, Bradford/MIT Press, 1987. Hopkins, W. D.; Morris, R. Handedness in great apes: A review of findings. INTERNATIONAL JOURNAL OF PRIMATOLOGY 14:l-25, 1993. MacNeilage, P. F.; Studdert-Kennedy, M. G.; Lindblom, B. Primate handedness reconsidered. BEHAVIORAL AND BRAIN SCIENCES 101247-303,1987. Ward, J. P.; Hopkins, W. D. PRIMATE LATERALITY. CURRENT BEHAVIORAL EVIDENCE OF PRIMATE ASYMMETRIES. New York, Springer Verlag, 1993.