The evolution and genetics of cerebral asymmetry

Michael C. Corballis * 0 0 Department of Psychology, University of Auckland , Private Bag 92019, Auckland 1142 , New Zealand Handedness and cerebral asymmetry are commonly assumed to be uniquely human, and even defining characteristics of our species. This is increasingly refuted by the evidence of behavioural asymmetries in non-human species. Although complex manual skill and language are indeed unique to our species and are represented asymmetrically in the brain, some non-human asymmetries appear to be precursors, and others are shared between humans and non-humans. In all behavioural and cerebral asymmetries so far investigated, a minority of individuals reverse or negate the dominant asymmetry, suggesting that such asymmetries are best understood in the context of the overriding bilateral symmetry of the brain and body, and a trade-off between the relative advantages and disadvantages of symmetry and asymmetry. Genetic models of handedness, for example, typically postulate a gene with two alleles, one disposing towards right-handedness and the other imposing no directional influence. There is as yet no convincing evidence as to the location of this putative gene, suggesting that several genes may be involved, or that the gene may be monomorphic with variations due to environmental or epigenetic influences. Nevertheless, it is suggested that, in behavioural, neurological and evolutionary terms, it may be more profitable to examine the degree rather than the direction of asymmetry. 1. INTRODUCTION The asymmetry of the brain raises something of a paradox, since, in most respects, the brains and bodies of most organisms, including humans, are strikingly bilaterally symmetrical. As Palmer (2004) put it, bilateral symmetry is the default condition. The midplane of the developing organism is defined by two axes, the anteroposterior and dorsoventral axes, but there is no leftright axis. Instead, the left and right halves of the organism are constructed from separate mediolateral axes. Since these axes are mirror images, the resulting organism will be bilaterally symmetrical, unless there is some symmetry-breaking step. Indeed, most organisms, including humans, belong to the phylum known as Bilateria, which goes back some 600 million years (Chen et al. 2004). Nevertheless, bilateral symmetry is not restricted to the Bilateria, and has arisen independently in different lineages. It may even precede the Bilateria, since it is also present in some species of the phylum Cnidaria, which is outside the Bilateria. In the sea anemone Nematostella vectensis, for example, bilateral symmetry is dependent on the expression of homologous Hox genes much as it is in the Bilateria, suggesting that bilateral symmetry arose even before the evolutionary split between the Cnidaria and the Bilateria ( Finnerty et al. 2004). For animals that move freely in the natural world, bilateral symmetry is adaptive, because symmetrically placed limbs, be they legs, wings or flippers, provide for linear movement, which is more efficient than motion in an arc. Directional motion creates a backfront asymmetry, so that eyes and mouth are placed forward, but asymmetry tends to be preserved with respect to left and right. Any sensory asymmetry would create an increased risk of predation from the weaker side. In a world in which leftright parity is largely conserved, then, bilateral symmetry is a natural adaptation. Against this strong background of bilateral symmetry, our brains and bodies exhibit some striking leftright asymmetries. Indeed, asymmetries are widespread in nature, albeit superimposed on a body plan that is fundamentally bilaterally symmetrical. Many asymmetries are so-called fluctuating asymmetries, which are random variations from symmetry, usually slight, and these are not of concern here. Rather, my focus is on cerebral and behavioural asymmetries in which the direction of asymmetry in the majority of individuals in a population is in the same direction. Such asymmetries suggest that bilateral symmetry is readily and systematically broken if asymmetry proves more adaptive. This is true of the internal organs, including the heart, lungs, stomach and liver, which are arranged asymmetrically, presumably in the interests of more efficient packaging, and perhaps also of more effective function. Automobiles, for example, have evolved to be outwardly bilaterally symmetrical, but their engines are arranged asymmetricallya matter of efficiency in both packaging and performance. Internal organs, moreover, are relatively independent of the organisms interactions with the spatial world, so the pressure to symmetry is eased. The brain and nervous system, on the other hand, are more directly concerned with sensorimotor activity, and are, for the most part, organized symmetrically. Superimposed on the fundamental symmetry of the brain, though, are a number of systematic asymmetries. In humans, at least, the most obvious asymmetry is handedness. In the great majority of the human population, one hand is clearly dominant in activities such as writing and throwing, and, in approximately 90 per cent of the population, the dominant hand is the right hand. This asymmetry is not at all obvious in the actual structure of the hands themselves, although there are some differences in muscle strength and bone density favouring the dominant hand; at least some of these are a consequence rather than a cause of greater use of the dominant hand (see Steele & Uomini 2005, for review). Handedness is much more obviously a matter of differential skill and activity between the hands, reflecting a cerebral asymmetry rather than a mechanical one. Since the pioneering discoveries of Broca (1861), it is well established that the left hemisphere of the brain is also dominant for language, especially those aspects of language concerned with production. It is also clear that there are complementary specializations of the right hemisphere (Sperry 1982; Corballis 1991; Mort et al. 2003). It is widely held that these asymmetries are uniquely human, and perhaps even a defining characteristic of our species. It is often suggested that handedness and cerebral asymmetry resulted from some genetic mutation at some point after the split of the hominins from the other great apes (e.g. Corballis 1991; Annett 2002; McManus 2002), and Crow (2002) has gone so far as to suggest that this mutation was the speciation event that created Homo sapiens and other putatively human characteristics such as language, theory of mind and a susceptibility to psychosis. It is probably true that some functions that are lateralized in the human brain, such as language and specialized manual functions, are unique to our species, but it is becoming increasingly clear that cerebral asymmetry itself is not. Furthermore, many of the lateralized functions documented in non-humans are probably precursors to those functions we regard as uniquely human (e.g. Rogers & (...truncated)