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 (eg, its being a predator or a food item) and its being located to the ani- mal's left or right Moreover, other organisms (eg, 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

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Survival with an asymmetrical brain: Advantages and disadvantages of cerebral lateralization

The last decade has seen a resurgence of interest in laterality of function in primates, especially in hand use as it links to handedness and language in Homo sapiens. Manual lateralization of behavior in humans reflects asymmetry in cerebral structure, which must have evolved from nonhuman progenitors. To what extent is hand function lateralized in our nearest living relations? First, we address current issues of theory and methodology: statistics, measurement, variables, setting, sensory modality, and sample size. Specific topics include preference vs. performance, posture, bimanuality, inheritance, and arm asymmetry. We categorize the published literature in a descriptive, classificatory framework of five levels that range from Level 1, ambilaterality, to Level 5, human-like handedness. In a meta-analysis we put 241 published data-sets to a methodological test of seven criteria and code the 48 survivors onto the levels framework, by taxonomic grouping (prosimian, New World monkey, Old World monkey, ape, chimpanzee). Primates at Level 1 are mostly wild or naturalistic populations performing spontaneous species-typical behavior patterns. Most primates are at Levels 2 and 3, that is, individually lateralized to either side, especially on complex, demanding or practiced tasks, usually as devised in captive settings. Only chimpanzees show signs of population-level bias (Levels 4 and 5) to the right, but only in captivity and only incompletely. We conclude that nonhu- man primate hand function has not been shown to be lateralized at the species level—it is not the norm for any species, task, or setting, and so offers no easy model for the evolution of human handedness. Yrbk Phys Anthropol 40:201- 232, 1997. r 1997 Wiley-Liss, Inc.

On the Other Hand: Current Issues in and Meta-Analysis of the Behavioral Laterality of Hand Function in Nonhuman Primates

This article examines individual and group manual lateralization in nonhuman primates as a function of task's demands. It is suggested to distinguish low- from high-level manual activities with respect to the novelty variable and to the spatiotemporal scale of the movements. This review shows that low-level tasks lead to (a) symmetrical distributions of hand biases for the group and (b) manual preferences that are not indicative of the specialization of the contralateral hemisphere. In contrast, behaviors expressed in high-level tasks (a) show asymmetrical distribution of hand biases for the group and (b) seem to be related to a specialization of the contralateral hemisphere. Two types of lateralization, handedness and manual specialization, correspond to the 2 levels of tasks that are distinguished.

/pdf/manual-laterality-in-nonhuman-primates-a-distinction-between-2gdjto9yhv.pdf

Manual laterality in nonhuman primates : a distinction between handedness and manual specialization

Variability in the functional topography of area 4 was examined in adult squirrel monkeys Conventional intracortical microstimulation techniques were used to derive detailed maps (250 microns interpenetration distances) of distal forelimb movement representations in both hemispheres of six monkeys Spatial features of these representational maps were then compared to the hand preferred by the individual animals during a motor task requiring skilled digit use Beyond a few broad generalizations common to all area 4 motor maps, the local mosaic-like topography of individual distal forelimb representations was highly idiosyncratic Using statistical procedures to determine the independent contributions of individual, side, and movement category to the total variation in motor maps, the results demonstrate statistically significant variation in representational topography among individuals as well as between hemispheres of the same individuals In the dominant hemisphere (ie, the hemisphere opposite the preferred hand), the distal forelimb representations generally were greater in number and larger in total area, and displayed a longer total boundary length and a greater index of spatial complexity Because of the direct relationship between interhemispheric asymmetry and behavioral asymmetry, these studies suggest that a large source of variability found in the topography of motor maps in this and other studies derives from differences in the way particular movements and/or movement combinations are performed by individual animals

https://www.jneurosci.org/content/jneuro/12/8/2918.full.pdf

Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys

Summary A pattern of hemispheric specialization common to all vertebrates has been presented (summarized in Fig. 6 ). It has been considered, as far as possible, in terms of behavior patterns that are important in the natural environment. Responses in foraging and prey capture are typical specializations of the left hemisphere and they are often apparent as rightward-directed responses. Responses to novel stimuli and potential predators are specializations of the right hemisphere and responses to these stimuli are directed preferentially to the animal's left side. The right hemisphere is also specialized for the expression of fear and aggression, and to process and memorize topographical information, essential in association with predator-escape responses. The baseline differences between the hemispheres are (1) rapid and species-typical responses being under the control of the right hemisphere and (2) responses requiring considered decision making being under control of the left hemisphere. Download : Download full-size image Fig. 6 . Summary of the general pattern of lateralization of the hemispheres. Side biases in responding to prey to the right side and agonistic responses delivered to conspecifics on the left side occur not only in species with eyes placed on the sides of their head and with only a small binocular field of vision, but also in species with smaller lateral fields and with a large binocular overlap. At least in one case, that of prey striking in toads, there is clear evidence that the side bias occurs within the binocular field and manifests itself as a hemifield neglect of prey to the left side of the toad's midline. Chicks also, provided they have been hatched from eggs incubated in the dark, have a bias within the binocular field: They show a preference to fixate with the right half of the binocular field before delivering an aggressive peck. It should be noted, however, that the majority of aggressive pecks made by chicks are delivered after use of the left, monocular field of vision in dark-incubated chicks as well as those exposed to light before hatching. Lateralized use of the visual hemifields deserves further investigation in a range of species. Side biases in responding are not easily associated with any evolutionary advantage but they may be balanced against other advantages of lateralization. Lateralization may enhance cognitive abilities and more efficient responding in some species and contexts. It may also be associated with specialized functioning of the immune system selected on the basis of past experience of the species in terms of physiological demand on the immune system, although this hypothesis has yet to be tested. Finally, population bias for the majority of individuals to be lateralized in the same direction is considered as a potential benefit to group cohesion, as in schooling fish, and a mechanism by which individuals can interact in predictable ways within a social group. For example, the bias for directing attack responses leftward may be used by an approaching animal to avoid an aggressive encounter; approach on the potential aggressor's right side would minimize the chances of attack. Until now, most examples of lateralization have come from experimentation in the laboratory or using captive animals. There are relatively few examples demonstrating lateralization in wild populations, despite the obvious implications of lateralization for survival of species and individuals. Those lateralizations found in species in their natural habitat have been mentioned. They highlight the promise of gaining a better understanding of behavior of animals in the wild if lateralization is taken into account as a characteristic of all vertebrates.

Lateralization in vertebrates: Its early evolution, general pattern, and development

A population of 194 lemurs (Lemur spp.), 116 males and 78 females, from 1 to 30 years of age, was assessed for lateralized hand use in simple food reaching with a minimum of 100 reaches per animal. A hand preference was present in 80% of the population with a bias for use of the left hand that was most characteristic of male lemurs and young lemurs. The results confirm the presence of lateralization in prosimians, and we interpret the sex and age differences in relation to current theories of neural lateralization.

Michelle Wallace

Papers

Handedness as a function of sex and age in a large population of Lemur