This study examined hand preference in baboons in a sample of 94 subjects for a unimanual task and in a sample of 104 subjects for a bimanual task. For the unimanual task, handedness was assessed by observing simple reaching for grains. For the bimanual task, tubes lined with peanut butter inside were presented to the baboons. The hand and the finger used to remove peanut butter were recorded. Population-level right-handedness was found for the bimanual but not the unimanual task. In addition, test-retest correlations showed consistency in hand use across time for the coordinated bimanual task but not the simple reaching task. No significant effects of age and sex on the direction and strength of hand preferences were found for either task. These are the first evidences of population-level handedness in baboons and the results are discussed in the context of evolutionary theories of cerebral dominance.
Within the evolutionary framework about the origin of human handedness and hemispheric specialization for language, the question of expression of population-level manual biases in nonhuman primates and their potential continuities with humans remains controversial. Nevertheless, there is a growing body of evidence showing consistent population-level handedness particularly for complex manual behaviors in both monkeys and apes. In the present article, within a large comparative approach among primates, we will review our contribution to the field and the handedness literature related to two particular sophisticated manual behaviors regarding their potential and specific implications for the origins of hemispheric specialization in humans: bimanual coordinated actions and gestural communication. Whereas bimanual coordinated actions seem to elicit predominance of left-handedness in arboreal primates and of right-handedness in terrestrial primates, all handedness studies that have investigated gestural communication in several primate species have reported stronger degree of population-level right-handedness compared to noncommunicative actions. Communicative gestures and bimanual actions seem to affect differently manual asymmetries in both human and nonhuman primates and to be related to different lateralized brain substrates. We will discuss (1) how the data of hand preferences for bimanual coordinated actions highlight the role of ecological factors in the evolution of handedness and provide additional support the postural origin theory of handedness proposed by MacNeilage [MacNeilage [2007]. Present status of the postural origins theory. In W. D. Hopkins (Ed.), The evolution of hemispheric specialization in primates (pp. 59-91). London: Elsevier/Academic Press] and (2) the hypothesis that the emergence of gestural communication might have affected lateralization in our ancestor and may constitute the precursors of the hemispheric specialization for language.
Although the relative expansion of the frontal cortex in primate evolution is generally accepted, the nature of the human uniqueness, if any, and between-species anatomo-functional comparisons of the frontal areas remain controversial. To provide a novel interpretation of the evolution of primate brains, sulcal morphological variability of the medial frontal cortex was assessed in Old World monkeys (macaque/baboon) and Hominoidea (chimpanzee/human). We show that both Hominoidea possess a paracingulate sulcus, which was previously thought to be unique to the human brain and linked to higher cognitive functions, such as mentalizing. Also, we show systematic sulcal morphological organization of the medial frontal cortex that can be traced from Old World monkeys to Hominoidea species, demonstrating an evolutionarily conserved organizational principle. These data provide a new framework to compare sulcal morphology, cytoarchitectonic areal distribution, connectivity, and function across the primate order, leading to clear predictions about how other primate brains might be anatomo-functionally organized.
Predominance of right-handedness has historically been considered as a hallmark of human evolution. Whether nonhuman primates exhibit population-level manual bias remains a controversial topic. Here we investigated the hypothesis that bimanual coordinated activities may be a key-behavior in our ancestors for the emergence and evolution of human population-level right-handedness. To this end, we collected data on hand preferences in 35 captive gorillas (Gorilla gorilla) during simple unimanual reaching and for bimanual coordinated feeding. Unimanual reaching consisted of grasping food on the ground while bimanual feeding consisted of using one hand for holding a food and processing the food item by the opposite hand. No population-level manual bias was found for unimanual actions but, in contrast, gorillas exhibited a significant population-level right-handedness for the bimanual actions. Moreover, the degree of right-handedness for bimanual feeding exceeds any other known reports of hand use in primates, suggesting that lateralization for bimanual feeding is robust in captive gorillas. The collective evidence is discussed in the context of potential continuity of handedness between human and nonhuman primates. Keywordshandedness; hemispheric specialization; unimanual reaching; bimanual coordination; primates A universal human behavioral trait is right-handedness (Perelle and Ehrman, 1994;Annett, 2002;Raymond and Pontier, 2004). Although there is some variation between different cultures, all human populations studied to date have been shown to display right hand preferences, particularly for complex motor actions (e.g., Fagard, 2001). Moreover, the archeological data suggest that right-handedness in tool use can be dated back at least 2.5 millions years ago (Corballis, 1991;Bradshaw and Rogers, 1993). Whether evidence of handedness can be dated back even further in Hominid evolution, particularly in our closest living relative, the great apes, remains a topic of intense debate (McGrew and Marchant, 1997;Hopkins, 2006 Whereas historically population-level behavioral and hemispheric specialization have been considered hallmarks of human evolution (Warren, 1980;Ettlinger, 1988;Crow, 2004), there is a growing body of evidence of population-level behavioral and brain asymmetries in a host of vertebrates (Rogers and Andrew, 2002;Vallortigara and Rogers, 2005;Hopkins, 2007). For example, population-level limb preferences for motor actions have been found in some species of toads, rats and dogs, suggesting some phylogenetic continuity between animal species (Hook, 2004 for review). However, not all species show the same patterns and some have been critical of both the methods and interpretation of results in nonprimate species with respect to evolutionary models of handedness (MacNeilage et al., 1987;Crow, 2004). It is in this regard that studies of handedness in nonhuman primates have become increasingly important for testing and evaluating different evolutionary and genetic models of handedness (Hopkins, 2004(...
International audienceAlthough nonhuman primates' gestural communication is often considered to be a likely precursor of human language, the intentional properties in this communicative system have not yet been entirely elucidated. In particular, little is known about the intentional nature of monkeys' gestural signalling and related social understanding. We investigated whether olive baboons can (1) adjust their requesting gestures to the visual attention of the experimenter with special emphasis on the state of the eyes (open versus closed), and (2) flexibly tailor visual and auditory-based gestures to elaborate their communication as a function of whether or not the experimenter can see them. Using a food-requesting paradigm, we found monkeys able to favour either visual or auditory-based requesting gestures to match the experimenter's visual attention. Crucially, when the human was not visually attending, they silenced visual gestures to some extent but performed more attention-getting gestures. This is, to our knowledge, the first report of monkeys elaborating attention-getting signals to compensate for communication breakdown. Gestural communication was also supported by gaze alternation between the experimenter's face and the food, especially when the human was visually attending. These findings offer evidence that olive baboons understand the state of the eyes in others' visual attention and use requesting gestures intentionally. They emphasize that Old World monkeys shift to acoustic communication when the recipient is not visually attending. In contrast to that of human infants and great apes, this acoustic communication is purely gestural, not vocal
Determination of whether nonhuman primates exhibit neuroanatomical asymmetries would inform our understanding of the evolution of traits in humans that show functional hemispheric dominance, including language and handedness. Here we report the first evidence of population-level asymmetries in the chimpanzee neocortex using voxel-based morphology (VBM). MRI scans of the brain were collected in a sample of 31 chimpanzees including 9 males and 22 females, and the resulting images were segmented into gray matter, white matter and CSF. Gray matter images were then co-registered to a template and these normally oriented volumes were flipped on the left-right axis to create mirror volumes. In total, significant asymmetries were found in 13 regions including several that have been described previously in great apes using traditional region-of-interest approaches. The results from this VBM analysis support previous reports of hemispheric lateralization in chimpanzees and reinforce the view that asymmetries in the central nervous system are not uniquely human.Dating back to the time of Dax, Broca and Wernicke, it has been well documented that the human brain is asymmetrically organized, particularly for regions associated with handedness and language functions. For example, the planum temporale (PT) and frontal operculum (FO), regions corresponding to the classically-defined language centers of the human cerebral cortex, tend to be larger in the left compared to right hemisphere, particularly among right-handed individuals (Beaton, 1997;Foundas et al., 1998;Shapleske et al., 1999). Historically, the presence of behavioral and neuroanatomical asymmetries has been considered unique to hominin evolution (Corballis, 1992;Ettlinger, 1988;Warren, 1980); however, recent studies in nonhuman animals, and particularly nonhuman primates, have challenged this view (Hopkins, 2007;Rogers and Andrew, 2002). For instance, post-mortem and in vivo imaging studies have revealed population-level leftward asymmetries in the PT and FO of great ape brains (Cantalupo and Hopkins, 2001;Cantalupo et al., 2003; Gannon et al., 1998), suggesting Correspondence and reprint requests should be addressed to Dr. William D. Hopkins, Division of Psychobiology, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia 30322. E-mail: whopkin@emory.edu or whopkins@agnesscott.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. that neuroanatomical asymmetries are not uniquely human but rather reflect a shared trait that was present in the last common ancestor of humans and great apes. These...
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