BEHAVIORAL AND BRAIN SCIENCES (2005) 28, 575–633 Printed in the United States of America Survival with an asymmetrical brain: Advantages and disadvantages of cerebral lateralization Giorgio Vallortigara Department of Psychology and B.R.A.I.N. Centre for Neuroscience, University of Trieste, 34123 Trieste, Italy. [email protected] http://psico.univ.trieste.it/labs/acn-lab/ Lesley J. Rogers Centre for Neuroscience and Animal Behaviour, School of Biological, Biomedical and Molecular Sciences, University of New England, Armidale, NSW 2351, Australia. [email protected] http://www.sciences.une.edu.au/zoology/lesleyrogers.asp Abstract: Recent evidence in natural and semi-natural settings has revealed a variety of left-right perceptual asymmetries among ver- tebrates. These include preferential use of the left or right visual hemifield during activities such as searching for food, agonistic re- sponses, or escape from predators in animals as different as fish, amphibians, reptiles, birds, and mammals. There are obvious disad- vantages in showing such directional asymmetries because relevant stimuli may be located to the animal’s left or right at rando m; there is no a priori association between the meaning of a stimulus (e.g., its being a predator or a food item) and its being located to the ani- mal’s left or right. Moreover, other organisms (e.g., predators) could exploit the predictability of behavior that arises from population- level lateral biases. It might be argued that lateralization of function enhances cognitive capacity and efficiency of the brain, thus coun- teracting the ecological disadvantages of lateral biases in behavior. However, such an increase in brain efficiency could be obtained by each individual being lateralized without any need to align the direction of the asymmetry in the majority of the individuals of the pop- ulation. Here we argue that the alignment of the direction of behavioral asymmetries at the population level arises as an “evolutionarily stable strategy” under “social” pressures occurring when individually asymmetrical organisms must coordinate their behavior with the behavior of other asymmetrical organisms of the same or different species. Keywords: asymmetry; brain evolution; brain lateralization; development; evolution of lateralization; evolutionarily stable strategy; hemispheric specialization; laterality; lateralization of behavior; social behavior; theory of games 1. The rise of a neuroethology of the dual brain havior in the natural environment of a variety of species. Though this has gone largely unnoticed among neuropsy- Research on the topic of cerebral lateralization has been chologists who study humans, we believe that such evidence characterized by periodic peaks and troughs in level of in- is going to force all of us to rethink some of the basic issues terest. For instance, the early wave of excitement raised by on the evolution of cerebral lateralization; most important, Broca’s discoveries in the 1860s waned after the turn of the it can also provide a bridge between the (once-believed) century. Similarly, the renaissance of interest induced by disparate disciplines of neuropsychology and evolutionary Sperry’s discoveries with split-brain patients in the 1960s biology, as well as between neuropsychology and develop- has shown signs of decline in recent years (Efron 1990). It mental biology. should be noted that, until very recently, virtually all re- Before considering why we should care about lateral bi- search on cerebral lateralization had been confined to the ases exhibited in naturalistic settings, let us describe some laboratories of experimental psychologists and neuropsy- examples. Consider first the response to predators. A vari- chologists and was largely centered on the human species. ety of species of different classes (see Vallortigara et al. 1999 Even after the evidence for the existence of cerebral later- and Rogers 2002b, for extensive reviews) appear to be more alization in nonhuman species had become impressive, ex- reactive to predators seen in their left, rather than right, tending from fish to primates (for recent reviews see Rogers hemifield. Toads, for instance, are more likely to react, most 2002a; 2002b; 2002c; Rogers & Andrew 2002; Vallortigara often by jumping away, when a simulated predator is intro- 2000; Vallortigara et al. 1999), the subject remained largely duced into their left monocular field than when it is intro- outside the realm of biology on account of a focus on the duced into their right monocular field (Lippolis et al. 2002), causal mechanisms rather than on its function. In the past and recently the same result has been obtained in dunnarts, few years, however, something really new has appeared: Sminthopsis macroura (Lippolis et al. 2005) and chicks namely, evidence for lateral biases affecting everyday be- (Lippolis & Rogers, in preparation). These findings suggest © 2005 Cambridge University Press 0140-525X/05 $12.50 575 Vallortigara & Rogers: Survival with an asymmetrical brain that predator-escape and associated fear responses are con- In contrast to their leftward responses to predators, toads trolled by the right side of the brain. Some evidence indi- strike preferentially at prey to their right side (Vallortigara cates that also in rats the right hemisphere controls fear re- et al. 1998). The rightward bias for feeding responses has sponses: lesions of various types, including infarcts, in the also been documented in a variety of species of birds right hemisphere elevate activity in the open field (Robin- (chicks: Andrew et al. 1982; Mench & Andrew 1986; Rogers son 1985), presumably because the fear response of freez- 1997; Vallortigara et al. 1996; pigeons: Güntürkün 1997; ing is suppressed. Robinson and Downhill (1995) have Güntürkün & Kesch 1987; parids and corvids: Clayton & drawn attention to the similarity between these effects of Krebs 1994; zebrafinch: Alonso 1988; quails: Valenti et al. right hemisphere infarct in rats and the heightened anxiety 2003; black-winged stilts: Ventolini et al. 2005) and has that occurs in humans following damage to the right hemi- been traced back to an appearance during evolution as early sphere. Neurochemical changes, apparently associated as teleost fish (Miklosi & Andrew 1999; Miklosi et al. 1998). with long-term alterations of neurotransmission, are also in- These rightward biases for prey catching and foraging re- duced in the right, but not the left, hemisphere by preda- sponses are apparent when the prey or food has to be dis- tor stress, as shown in rats and cats (Adamec et al. 2003). criminated from similar targets: for example, toads show a In some circumstances, an approach towards, rather than right hemifield preference for directing tongue strikes at avoidance of, a potential predator is needed. Some fish prey that has to be recognized precisely and “handled” with leave their school in groups of two or three to approach a care (e.g., crickets) but not for simplified prey models, such predator and examine it more closely. By placing a mirror as a rectangular silhouette moving along its longitudinal axis on the left or right side of a tank, Bisazza et al. (1999) found (Robins & Rogers 2004). Similarly, chicks show the right- that the test fish approached a predator more closely in or- ward bias for pecking at grain (controlled by inputs from the der to inspect it when the mirror was on its left side than right eye) that has to be discriminated against a distracting when the mirror was on its right side. Such a preference for background or uncovered by removing a lid from a bowl a fish to position itself so that the image of a conspecific is (Andrew et al. 2000). These findings indicate that the left on its left side has been reported, even in the absence of hemisphere, which primarily processes input from the right predators, in eight different species of teleosts (Sovrano et eye, controls responses that require considered discrimina- al. 1999; 2001; see also Sovrano 2004). Similarly, the pref- tion between stimuli and manipulation of objects. To some erence for a fish to position itself so that the image of a degree this particular specialization of the left hemisphere predator being inspected is on its right side has been ob- is manifested in hand preferences in primates (discussed served in the absence of other conspecifics in several spe- later). As the left hemisphere controls the right hand, cies of teleosts (De Santi et al. 2000; 2001). Even tadpoles planned use of the right hand for fine manipulation of ob- have been shown to prefer to position themselves so that jects, as in writing by humans, may have arisen from this an- the image of a conspecific is on their left side (Bisazza et al. cient evolutionary specialization. 2002; Dadda et al. 2003). Aggressive responses also seem to be strongly lateralized in intraspecific agonistic settings: toads (Robins & Rogers 2004; Robins et al. 1998; Vallortigara et al. 1998), lizards Giorgio Vallortigara, Professor of Behavioural (Deckel 1995; 1997; Hews & Worthington 2001; Hews et Neuroscience and Animal Cognition at the University al. 2004), chicks (Vallortigara et al. 2001), adult hens of Trieste, Italy, is the author of over 150 scientific pa- (Rogers 1991), and gelada baboons (Casperd & Dunbar pers, most in the area of animal cognition and compar- 1996) direct more aggressive responses to conspecifics on ative neuroscience. He discovered the first evidence of their left side than they do to those on their right side.