- Email: [email protected]
Divided Brains: the Biology and Behaviour of Brain Asymmetries
660
Book Reviews (US) / Animal Behaviour 86 (2013) 659–662
monitoring (detection of any changes in them) are discussed in detail. Quantitative results in radar biology are strongly dependent on these measures and anyone working with radar to study atmospheric fauna will need to pay close attention to the contents of this section. Regulation of radar transmission (licensing of specific frequencies so that interference does not occur) and safety issues related to radiation protection are treated in Appendix B. A very comprehensive list of references through the beginning of 2012 completes the volume. To supplement the findings in this volume, an interested reader should examine a review of more recent research by Chapman et al. (2011). Although this volume is devoted mostly to radar studies of insects, the volume has much to offer anyone interested in radar studies of the atmosphere and its inhabitants. Drake & Reynolds have done a brilliant job of detailing the technical aspects of different types of radar and summarizing nearly 40 years of findings from studies using radar techniques. Future researchers in radar biology will need to read carefully the more technical chapters and sections in the volume, and the general reader will enjoy the coverage of the biological discoveries that have been made using the technology. Sidney A. Gauthreaux Jr Department of Biological Sciences, Clemson University, Clemson, SC 29438, U.S.A. References Chapman, J. W., Drake, V. A. & Reynolds, D. R. 2011. Recent insights from radar studies of insect flight. Annual Review of Entomology, 56, 337–356. Crawford, A. B. 1949. Radar reflections in the lower atmosphere. Proceedings of the Institute of Radio Engineers, 37, 404–405. Eastwood, E. 1967. Radar Ornithology. London: Methuen. Schaefer, G. W. 1969. Radar studies of locust, moth and butterfly migration in the Sahara. Proceedings of the Royal Entomological Society of London, C, 34, 39–40. Shire, E. S. 1958. Watching migrant birds by radar. Listener, 741. 6 November.
http://dx.doi.org/10.1016/j.anbehav.2013.05.035
Evolutionary Perspectives on Pregnancy. By John C. Avise. New York, NY: Columbia University Press (2013). Pp. xvii D 326. Price $75.00 hardcover. Pregnancy is the most intimate of all intraspecific relationships. One individual lives within the body of another, sharing every breath that its mother takes and every meal that its mother eats (at least in groups with well-developed placentas). Discussion of pregnancy is not typical in the pages of Animal Behaviour, which are more concerned with events leading up to conception and parent–offspring relations after offspring are born. In my contentious moods, I have suggested that the obsession with mating behaviour and the relative neglect of pregnancy reflects the interests and concerns of male biologists who are more interested in the transient relation of copulation, the question of who gets to put his thingamajig into her whatsit, than the much more durable and complex relationship of pregnancy. This is perhaps a little unfair. Behavioural ecologists and ethologists have traditionally studied externally observable behaviour, whereas pregnancy falls into the domains of anatomy, physiology, endocrinology, and the like. The ethos of ethologists has been to observe with minimal intervention, whereas the events of pregnancy are hidden, with methods of study that are often intrusive and destructive.
For almost 20 years, I have taught an undergraduate course on Vertebrate Viviparity as an effective way to teach evolutionary biology in the context of fascinating natural history, with an emphasis on inclusive fitness and evolutionary game theory. Students have often asked me if there was a good introductory book that covered the course’s content, and I have had to tell them that there was no such book and they would have to read papers scattered through the scientific literature. Now I can point them in the direction of John Avise’s engaging and beautifully illustrated book, a book that is written at a level suitable for a general audience, including college students and the interested lay reader. Avise reviews the multiple origins and diverse forms of pregnancy and pregnancy-like phenomena in vertebrates, invertebrates and even plants, although he has a particular focus on mammals and fish. I remember inspecting my leg after a boyhood tramp through the Australian bush and finding a large blood-bloated leech surrounded by a swarm of tiny leeches. Was this a litter of leeches, or had the smaller leeches merely been attracted to the scent of blood at the incision made by the larger leech? Probably the latter, because live birth is unknown among land leeches, but I learn from Avise’s book that freshwater leeches show welldeveloped parental care and that one species, Marsupiobdella africana, gives birth from an internal brood pouch. We are told about the late lamented gastric brooding frog of Australia, now sadly extinct, in which females swallowed newlyfertilized eggs and burped forth fully-formed froglets, the South American Rhinoderma darwinii (Darwin’s frog) in which males ‘gestate’ eggs and larvae in their vocal sac, monozygotic quadruplets in armadillos, and the sharing of a common blood supply by dizygotic twin marmosets. Foetal nutrition in viviparous sharks ranges from reliance on yolk deposited in an embryo’s own egg, to eating trophic eggs that a mother continues to ovulate during pregnancy, to intrauterine embryonic cannibalism. Other sharks have placentas, whereas the foetuses of rays drink ‘uterine milk’. Not only does Avise survey the taxonomic diversity of pregnancy but he also considers its evolutionary biology. Why should males become pregnant in pipefish and seahorses but females carry the offspring in other fishes? How is parent–offspring conflict and sibling rivalry expressed prenatally? What are the implications of pregnancy for paternity uncertainty (and maternity uncertainty)? I can recommend this book for a reader looking for an accessible introduction to this fascinating subject. David Haig Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, U.S.A. http://dx.doi.org/10.1016/j.anbehav.2013.06.007
Divided Brains: the Biology and Behaviour of Brain Asymmetries. By Leslie J. Rogers, Giorgio Vallortigara, Richard J. Andrew. New York: Cambridge University Press (2013). Pp. v D 229. Price $58.00 paperback. Here is a brief history of thought regarding the question of brain asymmetries in living forms and their phylogeny, the topic of this monograph. Up until about 40 years ago, nobody thought there were functional asymmetries in the brains of any animal except humans. From this anthropocentric perspective, both righthandedness and human communication, via language, jointly lateralized in the left hemisphere of the human brain, were unique evolutionary developments, and the right hemisphere was thought to have
Book Reviews (US) / Animal Behaviour 86 (2013) 659–662
subsequently evolved unique spatial functions by default. During the last 40 years, asymmetries in other animals have been reported at a gradually increasing rate. However, for the most part, these asymmetries have tended to be regarded as sporadic and unrelated to the human specializations. This monograph is momentous enough to be regarded as ushering in the next stage of this history. It provides a mountain of evidence for the radical claim that, far from the human specializations being unique, and the animal specializations being only sporadic, ‘the hemispheric specializations of humans are elaborations on a plan already present in the first vertebrates’ (page 166) and, the authors add, probably in ancestral invertebrates as well. The book consists of three parts. Chapter 1 (Introduction) presents the basic pattern of vertebrate laterality as the authors see it. The topics of chapters 2–5 (Function, Evolution, Development, Causation) derive from the four questions that Tinbergen (1963) deemed necessary to address to understand a biological trait. The sixth and final chapter considers Applications and Future Directions. The core conceptual component of the monograph consists of two basic evolutionary propositions, applying to all vertebrates and possibly extending into ancestral invertebrates: ‘.the left hemisphere became specialized for control of well established patterns of behavior under familiar circumstances, whereas the right hemisphere specialized for detection and responding to unexpected stimuli in the environment’ (page 97; MacNeilage et al. 2009). An example of provocative theorizing in this domain is Andrew’s suggestion that the left-sided mouth of the living larval form of the ancestral chordate, the lancelet, Branchiostoma (formerly known as Amphioxus) may be a clue to the origin of left-sided control of quotidian feeding in vertebrates. The major human functional asymmetries are thus to be understood as modifications of these two basic early developments. Human handedness and linguistic communication are offshoots of left-hemisphere control of the domain of routine action. The well-known right-hemisphere spatial and attentional specializations, and the greater right-hemisphere involvement in extreme emotions, derive from the initial, bottom–up, rapid response capacity to affectively relevant stimuli. The ‘local’ left-hemisphere specialization (for detailed perception and action) is regarded as evolving from the ‘considered discrimination’ (page 13) necessary for successful feeding, while the ‘global’ or synthetic right hemisphere capacity derives from its rapid response needs. Such a claim about more than a half a billion years of precursors to human asymmetries might appear fanciful, but it is backed up by an avalanche of phylogenetic detail. This relatively short book (229 pages) has almost 1000 references, nearly half of which have asymmetry-related connotations in their titles. Notably, the authors are senior authors in over 10% of these latter papers. Rather than being highly speculative, the authors come across, for the most part, as not straying far from the facts. The primary interest of most readers will likely lie in the origin of human righthandedness and language and their associated lefthemisphere specializations. Here we find a crucial piece of spadework contributing to Corballis’s accompanying pre-publication observation that the anthropocentric view, mentioned earlier, ‘is here comprehensively buried’ (page viii). The authors point out that righthandedness for operations on the inanimate world in monkeys and apes is now well established. They even question the assumption that human righthandedness is stronger than simian handedness, and they are skeptical regarding the 90/10 assumption of right-versus lefthandedness in the so far unsuccessful attempts to genetically model human handedness. They review widespread evidence of possible precursors to righthandedness in instances of rightsidedness in other vertebrates. (An intriguing example of this tendency is that leatherback turtles, Dermochelys
661
coriacea, tend to use their rear right flipper to apparently shield their cloacas from view while laying eggs (Sieg et al. 2010).) Nonhuman rightsidedness in vertebrates is particularly widespread and typically attains humanlike levels in turning and diving preferences of whales and dolphins (MacNeilage, in press). With respect to left-hemisphere language, the authors note that righthandedness for gestural communication has been found in monkeys and apes, and several studies have shown parallels in great apes to leftward brain asymmetries in human language areas, particularly in Broca’s and Wernicke’s areas (e.g. Hopkins 2007). This conception of precursors to handedness and language, also emphasizing the importance of the primate heritage of tool use, seems quite acceptable; however, this is the only place where, in my view, the authors stray excessively from the conceptual straight and narrow. They conclude that ‘The longstanding disputes about the origin of human language thus appear to be solved by an evolutionary sequence in which initial dominance of gestural communication controlled by the left hemisphere was followed by the addition of vocal communication’ (page 97). We will not solve this problem until we understand how the form of language evolved, in particular the form of its dual combinatoric subsystems, phonology and syntax. Turning to the right hemisphere, the authors correctly conclude that ‘the overall evidence from different taxonomic groups seems to be clearly in favor of a common and shared pattern’ (page 13). Trends here include a special role of the left eye in evasive and aggressive responses to predators, a greater right-hemisphere response to stress across a number of taxonomic groups, and a more prominent role of the right hemisphere in human depression. Another finding concerns the existence of extremely large von Economo neurons in the cingulate and insular cortices of several classes of animals with relatively large ratios of brain-to-body size (humans, great apes, elephants, whales). These neurons are described here as more frequent in the right hemisphere in humans and great apes and may be associated with responses to complex negative information. The authors note also the valence hypothesis of Davidson (e.g. Davidson 1995), ‘that the right hemisphere is involved in the processing of negative information whereas the left hemisphere is involved in processing positive information’ (page 15). This perspective is supported by Craig’s (2009) conclusion from work on the phenomenon of awareness that ‘the right hemisphere of the human brain is related to sympathetic arousal and the left hemisphere to parasympathetic calming’ (page 15). The authors assert that, as with emotion and motivation, ‘cognition too has revealed a basically similar pattern of lateralization in vertebrates’ (page 7). Considerable evidence, especially in birds, is amassed for the proposition that categorization, initially in the service of feeding, is a basic left-hemisphere capability. Evidence of specializations for spatial cognition is convincingly shown, again perhaps most clearly in birds, with the left hemisphere targeting landmarks and absolute distances, while the right hemisphere is more sensitive to geometric information and relative distances. There is also much support for a deep-seated right-hemisphere specialization for social cognition, with the capability for face recognition perhaps built on the global specialization. The authors provide much evidence for the existence of asymmetries in the nervous systems of invertebrates, and even evidence for the radical possibility that vertebrate asymmetry might have roots in invertebrate asymmetry, with those roots possibly beyond their nervous systems. This information not only points to extreme phylogenetic conservatism in the natural history of brain asymmetries, but it also adds evidence of the likelihood that asymmetry is a fundamental adaptive strategy in living forms. The authors deal with the central question of what asymmetry might do for organisms in chapter 2 (Function), separately
662
Book Reviews (US) / Animal Behaviour 86 (2013) 659–662
considering the two kinds of asymmetries: individual asymmetries without a predominant overall direction and population-level asymmetries favoring a particular direction. The authors contend that, when individual animals have asymmetries but there is no overall direction of asymmetry in the population, the advantage might accrue in either greater overall processing capability or more efficient separation of (and therefore less interference between) different stages of memory processing. An example of the advantage of greater processing capability comes from Rogers’ finding that chickens with normally developing asymmetries show a greater ability to separately monitor for predators and eat efficiently than do chickens that do not develop normal asymmetries. Population-level lateralization is considered to arise as an evolutionarily stable strategy whereby ‘what is advantageous for an (asymmetrical) animal to do depends on what the other (asymmetrical) individuals of the group do’ (page 52). A particular merit of the present approach to the question of function is that the authors use both game-theoretical mathematical modeling and testing of predictions to take them well beyond the ‘just-so story’ approach of unconstrained post hoc rationalization. An example of a successful test of a prediction is the finding by Vallortigara and colleagues that schooling fish, which would have an advantage in predator evasion if they had uniform turning preferences, in fact tend to have such preferences, while nonschooling fish tend not to have them. Chapter 5 (Causation) is mainly devoted to the question of how the actions of the two sides of the brain relate to each other, as they normally do. The modal state is considered to be one in which the left hemisphere, with its ability to categorize, focus attention, and make sustained responses under routine conditions, tends to inhibit the right hemisphere’s more generalized novelty-oriented bias, while remaining capable of providing access to its more immediate survival-oriented information. Although the authors are not specialists in human biology, they provide an incisive review of a wide range of human asymmetries, for example those relating to insight, planning, creativity, autism and gender differences, among others. A particularly fascinating assertion is that there is a common neurological substrate for the ventral attentional system of the right hemisphere and left hemisphere speech-related substrates including Broca’s and Wernicke’s areas, suggesting that the evolving organization of speech might have required the creation of an internal attentional analog to the externally directed right-hemisphere attentional system.
One puzzling aspect of the monograph is that one looks in vain for a mention of Darwin. It is puzzling because the authors present a classic example of a proposal regarding descent with modification, via natural selection, of what turns out to be a general property of animals, which is a worthy addition to Neo-Darwinian treatments of organismic evolution in general. Space forbids the coverage of a number of important parts of this book, including treatment of chapter 4 (Development) and chapter 6 (Applications and Future Directions). I have focused primarily on material related to chapter 2 (Evolution), because I find this the most important part of the book. It is impossible to do justice to the extraordinarily high quality of this book in the space available here. The authors have produced a monograph of astonishing scope, without sacrifice of rigor. The book is a landmark contribution to comparative neurobiology and cognitive neuroscience. I have no doubt that it will constitute the gold standard for attempts to synthesize knowledge on animal brain asymmetry for the foreseeable future. This remarkable book will make obsolete the typical introductory psychology textbook, with a single chapter on hemispheric specialization, unrelated to the content of the rest of the book. Peter MacNeilage Department of Psychology, University of Texas, Austin, Texas 78712, U.S.A. References Craig, A. D. 2009. How do you feeldnow? The anterior insula and human awareness. Nature Reviews Neuroscience, 10, 59–70. Davidson, R. J. 1995. Cerebral asymmetry, emotion, and affective style. In: Brain Asymmetry (Ed. by R. J. Davidson & K. Hugdahl), pp. 361–387. Cambridge, MA: MIT Press. Hopkins, W. D. (Eds). 2007. The Evolution of Hemispheric Specialization in Primates. Oxford: Oxford University Press. MacNeilage, P. F., Rogers, L. J. & Vallortigara, G. 2009. Origins of the left and right brain. Scientific American, 301, 60–67. MacNeilage, P. F. Evolution of the strongest vertebrate rightward action asymmetries: marine mammals and humans. Psychological Bulletin, In press. Sieg, A. E., Zandona, E., Izzo, V. M., Paladino, F. V. & Spotila, J. R. 2010. Populationlevel “flipperedness” in the eastern Pacific leatherback turtle. Behavioural Brain Research, 206, 135–138. Tinbergen, N. 1963. On aims and methods in ethology. Zeitschrift für Tierpsychology, 20, 410–433.
http://dx.doi.org/10.1016/j.anbehav.2013.06.001
Book Reviews (US) / Animal Behaviour 86 (2013) 659–662
monitoring (detection of any changes in them) are discussed in detail. Quantitative results in radar biology are strongly dependent on these measures and anyone working with radar to study atmospheric fauna will need to pay close attention to the contents of this section. Regulation of radar transmission (licensing of specific frequencies so that interference does not occur) and safety issues related to radiation protection are treated in Appendix B. A very comprehensive list of references through the beginning of 2012 completes the volume. To supplement the findings in this volume, an interested reader should examine a review of more recent research by Chapman et al. (2011). Although this volume is devoted mostly to radar studies of insects, the volume has much to offer anyone interested in radar studies of the atmosphere and its inhabitants. Drake & Reynolds have done a brilliant job of detailing the technical aspects of different types of radar and summarizing nearly 40 years of findings from studies using radar techniques. Future researchers in radar biology will need to read carefully the more technical chapters and sections in the volume, and the general reader will enjoy the coverage of the biological discoveries that have been made using the technology. Sidney A. Gauthreaux Jr Department of Biological Sciences, Clemson University, Clemson, SC 29438, U.S.A. References Chapman, J. W., Drake, V. A. & Reynolds, D. R. 2011. Recent insights from radar studies of insect flight. Annual Review of Entomology, 56, 337–356. Crawford, A. B. 1949. Radar reflections in the lower atmosphere. Proceedings of the Institute of Radio Engineers, 37, 404–405. Eastwood, E. 1967. Radar Ornithology. London: Methuen. Schaefer, G. W. 1969. Radar studies of locust, moth and butterfly migration in the Sahara. Proceedings of the Royal Entomological Society of London, C, 34, 39–40. Shire, E. S. 1958. Watching migrant birds by radar. Listener, 741. 6 November.
http://dx.doi.org/10.1016/j.anbehav.2013.05.035
Evolutionary Perspectives on Pregnancy. By John C. Avise. New York, NY: Columbia University Press (2013). Pp. xvii D 326. Price $75.00 hardcover. Pregnancy is the most intimate of all intraspecific relationships. One individual lives within the body of another, sharing every breath that its mother takes and every meal that its mother eats (at least in groups with well-developed placentas). Discussion of pregnancy is not typical in the pages of Animal Behaviour, which are more concerned with events leading up to conception and parent–offspring relations after offspring are born. In my contentious moods, I have suggested that the obsession with mating behaviour and the relative neglect of pregnancy reflects the interests and concerns of male biologists who are more interested in the transient relation of copulation, the question of who gets to put his thingamajig into her whatsit, than the much more durable and complex relationship of pregnancy. This is perhaps a little unfair. Behavioural ecologists and ethologists have traditionally studied externally observable behaviour, whereas pregnancy falls into the domains of anatomy, physiology, endocrinology, and the like. The ethos of ethologists has been to observe with minimal intervention, whereas the events of pregnancy are hidden, with methods of study that are often intrusive and destructive.
For almost 20 years, I have taught an undergraduate course on Vertebrate Viviparity as an effective way to teach evolutionary biology in the context of fascinating natural history, with an emphasis on inclusive fitness and evolutionary game theory. Students have often asked me if there was a good introductory book that covered the course’s content, and I have had to tell them that there was no such book and they would have to read papers scattered through the scientific literature. Now I can point them in the direction of John Avise’s engaging and beautifully illustrated book, a book that is written at a level suitable for a general audience, including college students and the interested lay reader. Avise reviews the multiple origins and diverse forms of pregnancy and pregnancy-like phenomena in vertebrates, invertebrates and even plants, although he has a particular focus on mammals and fish. I remember inspecting my leg after a boyhood tramp through the Australian bush and finding a large blood-bloated leech surrounded by a swarm of tiny leeches. Was this a litter of leeches, or had the smaller leeches merely been attracted to the scent of blood at the incision made by the larger leech? Probably the latter, because live birth is unknown among land leeches, but I learn from Avise’s book that freshwater leeches show welldeveloped parental care and that one species, Marsupiobdella africana, gives birth from an internal brood pouch. We are told about the late lamented gastric brooding frog of Australia, now sadly extinct, in which females swallowed newlyfertilized eggs and burped forth fully-formed froglets, the South American Rhinoderma darwinii (Darwin’s frog) in which males ‘gestate’ eggs and larvae in their vocal sac, monozygotic quadruplets in armadillos, and the sharing of a common blood supply by dizygotic twin marmosets. Foetal nutrition in viviparous sharks ranges from reliance on yolk deposited in an embryo’s own egg, to eating trophic eggs that a mother continues to ovulate during pregnancy, to intrauterine embryonic cannibalism. Other sharks have placentas, whereas the foetuses of rays drink ‘uterine milk’. Not only does Avise survey the taxonomic diversity of pregnancy but he also considers its evolutionary biology. Why should males become pregnant in pipefish and seahorses but females carry the offspring in other fishes? How is parent–offspring conflict and sibling rivalry expressed prenatally? What are the implications of pregnancy for paternity uncertainty (and maternity uncertainty)? I can recommend this book for a reader looking for an accessible introduction to this fascinating subject. David Haig Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, U.S.A. http://dx.doi.org/10.1016/j.anbehav.2013.06.007
Divided Brains: the Biology and Behaviour of Brain Asymmetries. By Leslie J. Rogers, Giorgio Vallortigara, Richard J. Andrew. New York: Cambridge University Press (2013). Pp. v D 229. Price $58.00 paperback. Here is a brief history of thought regarding the question of brain asymmetries in living forms and their phylogeny, the topic of this monograph. Up until about 40 years ago, nobody thought there were functional asymmetries in the brains of any animal except humans. From this anthropocentric perspective, both righthandedness and human communication, via language, jointly lateralized in the left hemisphere of the human brain, were unique evolutionary developments, and the right hemisphere was thought to have
Book Reviews (US) / Animal Behaviour 86 (2013) 659–662
subsequently evolved unique spatial functions by default. During the last 40 years, asymmetries in other animals have been reported at a gradually increasing rate. However, for the most part, these asymmetries have tended to be regarded as sporadic and unrelated to the human specializations. This monograph is momentous enough to be regarded as ushering in the next stage of this history. It provides a mountain of evidence for the radical claim that, far from the human specializations being unique, and the animal specializations being only sporadic, ‘the hemispheric specializations of humans are elaborations on a plan already present in the first vertebrates’ (page 166) and, the authors add, probably in ancestral invertebrates as well. The book consists of three parts. Chapter 1 (Introduction) presents the basic pattern of vertebrate laterality as the authors see it. The topics of chapters 2–5 (Function, Evolution, Development, Causation) derive from the four questions that Tinbergen (1963) deemed necessary to address to understand a biological trait. The sixth and final chapter considers Applications and Future Directions. The core conceptual component of the monograph consists of two basic evolutionary propositions, applying to all vertebrates and possibly extending into ancestral invertebrates: ‘.the left hemisphere became specialized for control of well established patterns of behavior under familiar circumstances, whereas the right hemisphere specialized for detection and responding to unexpected stimuli in the environment’ (page 97; MacNeilage et al. 2009). An example of provocative theorizing in this domain is Andrew’s suggestion that the left-sided mouth of the living larval form of the ancestral chordate, the lancelet, Branchiostoma (formerly known as Amphioxus) may be a clue to the origin of left-sided control of quotidian feeding in vertebrates. The major human functional asymmetries are thus to be understood as modifications of these two basic early developments. Human handedness and linguistic communication are offshoots of left-hemisphere control of the domain of routine action. The well-known right-hemisphere spatial and attentional specializations, and the greater right-hemisphere involvement in extreme emotions, derive from the initial, bottom–up, rapid response capacity to affectively relevant stimuli. The ‘local’ left-hemisphere specialization (for detailed perception and action) is regarded as evolving from the ‘considered discrimination’ (page 13) necessary for successful feeding, while the ‘global’ or synthetic right hemisphere capacity derives from its rapid response needs. Such a claim about more than a half a billion years of precursors to human asymmetries might appear fanciful, but it is backed up by an avalanche of phylogenetic detail. This relatively short book (229 pages) has almost 1000 references, nearly half of which have asymmetry-related connotations in their titles. Notably, the authors are senior authors in over 10% of these latter papers. Rather than being highly speculative, the authors come across, for the most part, as not straying far from the facts. The primary interest of most readers will likely lie in the origin of human righthandedness and language and their associated lefthemisphere specializations. Here we find a crucial piece of spadework contributing to Corballis’s accompanying pre-publication observation that the anthropocentric view, mentioned earlier, ‘is here comprehensively buried’ (page viii). The authors point out that righthandedness for operations on the inanimate world in monkeys and apes is now well established. They even question the assumption that human righthandedness is stronger than simian handedness, and they are skeptical regarding the 90/10 assumption of right-versus lefthandedness in the so far unsuccessful attempts to genetically model human handedness. They review widespread evidence of possible precursors to righthandedness in instances of rightsidedness in other vertebrates. (An intriguing example of this tendency is that leatherback turtles, Dermochelys
661
coriacea, tend to use their rear right flipper to apparently shield their cloacas from view while laying eggs (Sieg et al. 2010).) Nonhuman rightsidedness in vertebrates is particularly widespread and typically attains humanlike levels in turning and diving preferences of whales and dolphins (MacNeilage, in press). With respect to left-hemisphere language, the authors note that righthandedness for gestural communication has been found in monkeys and apes, and several studies have shown parallels in great apes to leftward brain asymmetries in human language areas, particularly in Broca’s and Wernicke’s areas (e.g. Hopkins 2007). This conception of precursors to handedness and language, also emphasizing the importance of the primate heritage of tool use, seems quite acceptable; however, this is the only place where, in my view, the authors stray excessively from the conceptual straight and narrow. They conclude that ‘The longstanding disputes about the origin of human language thus appear to be solved by an evolutionary sequence in which initial dominance of gestural communication controlled by the left hemisphere was followed by the addition of vocal communication’ (page 97). We will not solve this problem until we understand how the form of language evolved, in particular the form of its dual combinatoric subsystems, phonology and syntax. Turning to the right hemisphere, the authors correctly conclude that ‘the overall evidence from different taxonomic groups seems to be clearly in favor of a common and shared pattern’ (page 13). Trends here include a special role of the left eye in evasive and aggressive responses to predators, a greater right-hemisphere response to stress across a number of taxonomic groups, and a more prominent role of the right hemisphere in human depression. Another finding concerns the existence of extremely large von Economo neurons in the cingulate and insular cortices of several classes of animals with relatively large ratios of brain-to-body size (humans, great apes, elephants, whales). These neurons are described here as more frequent in the right hemisphere in humans and great apes and may be associated with responses to complex negative information. The authors note also the valence hypothesis of Davidson (e.g. Davidson 1995), ‘that the right hemisphere is involved in the processing of negative information whereas the left hemisphere is involved in processing positive information’ (page 15). This perspective is supported by Craig’s (2009) conclusion from work on the phenomenon of awareness that ‘the right hemisphere of the human brain is related to sympathetic arousal and the left hemisphere to parasympathetic calming’ (page 15). The authors assert that, as with emotion and motivation, ‘cognition too has revealed a basically similar pattern of lateralization in vertebrates’ (page 7). Considerable evidence, especially in birds, is amassed for the proposition that categorization, initially in the service of feeding, is a basic left-hemisphere capability. Evidence of specializations for spatial cognition is convincingly shown, again perhaps most clearly in birds, with the left hemisphere targeting landmarks and absolute distances, while the right hemisphere is more sensitive to geometric information and relative distances. There is also much support for a deep-seated right-hemisphere specialization for social cognition, with the capability for face recognition perhaps built on the global specialization. The authors provide much evidence for the existence of asymmetries in the nervous systems of invertebrates, and even evidence for the radical possibility that vertebrate asymmetry might have roots in invertebrate asymmetry, with those roots possibly beyond their nervous systems. This information not only points to extreme phylogenetic conservatism in the natural history of brain asymmetries, but it also adds evidence of the likelihood that asymmetry is a fundamental adaptive strategy in living forms. The authors deal with the central question of what asymmetry might do for organisms in chapter 2 (Function), separately
662
Book Reviews (US) / Animal Behaviour 86 (2013) 659–662
considering the two kinds of asymmetries: individual asymmetries without a predominant overall direction and population-level asymmetries favoring a particular direction. The authors contend that, when individual animals have asymmetries but there is no overall direction of asymmetry in the population, the advantage might accrue in either greater overall processing capability or more efficient separation of (and therefore less interference between) different stages of memory processing. An example of the advantage of greater processing capability comes from Rogers’ finding that chickens with normally developing asymmetries show a greater ability to separately monitor for predators and eat efficiently than do chickens that do not develop normal asymmetries. Population-level lateralization is considered to arise as an evolutionarily stable strategy whereby ‘what is advantageous for an (asymmetrical) animal to do depends on what the other (asymmetrical) individuals of the group do’ (page 52). A particular merit of the present approach to the question of function is that the authors use both game-theoretical mathematical modeling and testing of predictions to take them well beyond the ‘just-so story’ approach of unconstrained post hoc rationalization. An example of a successful test of a prediction is the finding by Vallortigara and colleagues that schooling fish, which would have an advantage in predator evasion if they had uniform turning preferences, in fact tend to have such preferences, while nonschooling fish tend not to have them. Chapter 5 (Causation) is mainly devoted to the question of how the actions of the two sides of the brain relate to each other, as they normally do. The modal state is considered to be one in which the left hemisphere, with its ability to categorize, focus attention, and make sustained responses under routine conditions, tends to inhibit the right hemisphere’s more generalized novelty-oriented bias, while remaining capable of providing access to its more immediate survival-oriented information. Although the authors are not specialists in human biology, they provide an incisive review of a wide range of human asymmetries, for example those relating to insight, planning, creativity, autism and gender differences, among others. A particularly fascinating assertion is that there is a common neurological substrate for the ventral attentional system of the right hemisphere and left hemisphere speech-related substrates including Broca’s and Wernicke’s areas, suggesting that the evolving organization of speech might have required the creation of an internal attentional analog to the externally directed right-hemisphere attentional system.
One puzzling aspect of the monograph is that one looks in vain for a mention of Darwin. It is puzzling because the authors present a classic example of a proposal regarding descent with modification, via natural selection, of what turns out to be a general property of animals, which is a worthy addition to Neo-Darwinian treatments of organismic evolution in general. Space forbids the coverage of a number of important parts of this book, including treatment of chapter 4 (Development) and chapter 6 (Applications and Future Directions). I have focused primarily on material related to chapter 2 (Evolution), because I find this the most important part of the book. It is impossible to do justice to the extraordinarily high quality of this book in the space available here. The authors have produced a monograph of astonishing scope, without sacrifice of rigor. The book is a landmark contribution to comparative neurobiology and cognitive neuroscience. I have no doubt that it will constitute the gold standard for attempts to synthesize knowledge on animal brain asymmetry for the foreseeable future. This remarkable book will make obsolete the typical introductory psychology textbook, with a single chapter on hemispheric specialization, unrelated to the content of the rest of the book. Peter MacNeilage Department of Psychology, University of Texas, Austin, Texas 78712, U.S.A. References Craig, A. D. 2009. How do you feeldnow? The anterior insula and human awareness. Nature Reviews Neuroscience, 10, 59–70. Davidson, R. J. 1995. Cerebral asymmetry, emotion, and affective style. In: Brain Asymmetry (Ed. by R. J. Davidson & K. Hugdahl), pp. 361–387. Cambridge, MA: MIT Press. Hopkins, W. D. (Eds). 2007. The Evolution of Hemispheric Specialization in Primates. Oxford: Oxford University Press. MacNeilage, P. F., Rogers, L. J. & Vallortigara, G. 2009. Origins of the left and right brain. Scientific American, 301, 60–67. MacNeilage, P. F. Evolution of the strongest vertebrate rightward action asymmetries: marine mammals and humans. Psychological Bulletin, In press. Sieg, A. E., Zandona, E., Izzo, V. M., Paladino, F. V. & Spotila, J. R. 2010. Populationlevel “flipperedness” in the eastern Pacific leatherback turtle. Behavioural Brain Research, 206, 135–138. Tinbergen, N. 1963. On aims and methods in ethology. Zeitschrift für Tierpsychology, 20, 410–433.
http://dx.doi.org/10.1016/j.anbehav.2013.06.001