A few years ago, I engaged in a somewhat acerbic debate with Crow on the existence of lateralization in non-human animals (Crow 2004
; Rogers 2004
; see comments by Corballis 2007
). Crow firmly adhered to the earlier, widely held notion that directional asymmetry is unique to modern Homo sapiens
and saw it, in association with right-handedness, as the pivotal event in hominid evolution that determined the emergence of language. I, on the other hand, pointed out the now extensive literature on lateralization in a wide range of vertebrate species and argued that there was no such discontinuity in the evolution of lateralization that coincided with the appearance of human language and so placed humans apart from other species on this particular characteristic. As far as I know, we still hold these differences of opinion, although others, such as Corballis (2005
), who once also defined humans as the lopsided ape (Corballis 1991
) and unique in terms of their asymmetrical brains, have now embraced the evidence for lateralization in other vertebrate species and reached the conclusion that it is very unlikely that Crow is correct.
Handedness has been important in this continuity/discontinuity debate, largely because right-handedness in humans is associated with the left hemisphere's specialization for language and speech production. Not surprisingly, the first attempts to see whether animals other than humans might be lateralized focused on measuring hand preferences in primates. The first conclusion drawn from these investigations was that non-human primates lacked any species-typical, directional bias for using a preferred hand, although individuals of some species often had hand preferences, left and right in approximately equal numbers, which were seen to be the result of learning through practice (see Warren 1977
). Furthermore, it was concluded that non-human primates preferred to use different hands for different tasks. Later, MacNeilage et al. (1987)
re-examined the research on hand preferences in primates and concluded that there was evidence of preferences at the species level and, moreover, that this bias was for use of the right hand and arm to support the body while employing the left hand for snatching at and grasping insects, as seen in the early primates, prosimians (Ward et al. 1993
). This specialization of the left hand to grab moving targets has been retained in higher primates, including humans (MacNeilage et al. 1987
). As adoption of an upright body posture freed the right hand from its role of supporting the body, the right hand was used to perform fine manipulation of objects and, as evolution proceeded, this hand was adopted for tool using. Recent studies of hand preferences in chimpanzees have supported this hypothesis; chimpanzees show consistent and significant right-hand preferences in tool using (captive chimpanzees: Hopkins et al. 2004
; wild chimpanzees: Lonsdorf & Hopkins 2005
) and in throwing (Hopkins et al. 2005
The theory of MacNeilage and colleagues has become known as the Postural Origins Theory, meaning that postural changes were instrumental in the origin of the hemispheric asymmetries present in humans (MacNeilage 1998
). Hence, the emphasis is on motor functions, rather than sensory functions.
Meanwhile, during the 1970s and 1980s, evidence of lateralization in non-primate species was coming to light, and in these cases, it had nothing to do with manifested hand or limb preferences but rather with hemispheric differences in sensory processing and/or motor control. Nottebohm (1971)
showed that, in the male chaffinch, the motor control of song production is lateralized to the left syringeal nerve and, as he showed later, in the canary, it is lateralized to the vocal centre in the left hemisphere (Nottebohm et al. 1976
). By injecting cycloheximide into the left or right hemisphere of the domestic chick, I showed that the left and right hemispheres control different patterns of behaviour (Rogers & Anson 1979
). Using ablation of one or other hemisphere, Denenberg (1981)
demonstrated differential functioning of the left and right hemispheres of the rat. Since the time of these initial discoveries of lateralization in non-human species, a growing number of examples have accumulated (summarized by Rogers 2002a
; Rogers & Andrew 2002
; Vallortigara & Rogers 2005
The finding of hemispheric specialization in the rat was important for the main point that I am discussing here, because it was not associated with the paw preferences of the rats. Although the rats that Deneberg tested exhibited individual paw preferences to use either the left or right paw to reach into a tube to obtain food, there was no population bias for a preferred paw, whereas the lateralization of hemispheric function was present at a population level, as confirmed many times subsequently (Cowell et al. 1997
; summarized by Bradshaw & Rogers (1993)
). In other words, a brain can be lateralized without that lateralization being manifested as a paw or hand preference.
This lack of concordance between hand preference and hemispheric lateralization might have alerted those seeking to find evidence of lateralization in primates by measuring hand preferences, but it did not, probably because the hands of primates are considered to be special and of no comparison with hand/paw use by non-primates. Although I recognize the complexity of some primate hands and their ability to perform fine manipulations, I am not sure whether an absolute distinction between primate hands and non-primate paws is correct. The complexity of hand use, and hand structure, along with the presence or absence of claws, varies enormously across primate species and the whole-hand snatch-grab use of the hands by prosimians may not be qualitatively very different from the rat's use of its paws to grasp small objects (Whishaw & Gorny 1994
; Whishaw et al. 1998a
) or the cockatoo's use of its foot to hold food objects and manipulate them by coordinated use of the foot and beak (Rogers 2007
). Internal control of the hand, which enables processing of food, evolved only in some primates. Hence, I am suggesting that hand/paw preferences in non-primate species might be compared with those of primate species to gain a broader picture of the relationship, or lack thereof, of hand preference with hemispheric specialization.
Directional bias to use a preferred paw has now been found in some species: toads use the right paw preferentially to wipe objects from their head and to push against a substrate in order to right their body posture (Bisazza et al. 1996
), and parrots show preferred use of a foot, the left foot in most species, to hold food (Rogers 1980
; Harris 1989
). In fact, it has now been found that some strains of laboratory rats express directional biases to use a preferred paw (Tang & Verstynen 2002
; Güven et al. 2003
These examples demonstrate that species-typical hand/paw preferences are present in some primates and non-primates. Even right-hand preference is not exclusive to humans and did not evolve solely in the hominid line in association with language, as postulated by McManus (1999)
, Annett (2002)
and Crow (2002)
. This does not mean that the right-handedness of humans is unrelated to specialization of the left hemisphere for language, but rather that we cannot consider language as the sole reason for adopting preferred use of a particular hand or limb, or vice versa. In other words, there was no single genetic mutation, no ‘speciation event’ as Crow (2002)
hypothesized, that caused hemispheric asymmetry and handedness, and in so doing, brought about the evolution of H. sapiens
The question to be addressed now is what does determine the preferred use of a hand/paw in different species and to what extent is it related to other aspects of brain lateralization?