NoteCerebral petalias and their relationship to handedness in capuchin monkeys (Cebus apella)
Introduction
Neuroanatomical asymmetries of the human brain are thought to underlie a range of lateralized behavior, including language, gesture and skilled motor actions (see Toga & Thompson, 2003, for a review). In humans, one particularly prominent population-level neuroanatomical asymmetry is that of a right-frontal, left-occipital petalia (Holloway & De La Coste-Lareymondie, 1982; Lancaster, Kochunov, Thompson, Toga, & Fox, 2003; LeMay, 1976, Watkins et al., 2001). Petalias are the greater protrusion of one cerebral hemisphere relative to the other as expressed at the frontal and occipital poles of the brain. Whether nonhuman primates display cerebral petalias has been investigated using endocasts (as the petalias leave impressions on the inner table of bone of the skull), cadaver specimens, and more recently, magnetic resonance images. However, the use of these different methodologies has produced conflicting results. LeMay (1976), using data from endocasts, reported that Old and New World monkeys had only a left-occipital protrusion. Falk et al. (1991), also using endocasts, reported only a right-frontal petalia in rhesus monkeys. Cheverud et al. (1990) reported a positive correlation between the size of the left-occipital petalia and right-frontal petalia using a larger sample of rhesus endocasts. In contrast, Holloway and De La Coste-Lareymondie (1982) reported that the combination of left-occipital and right-frontal petalias was rarely present in great ape endocasts, although left-occipital petalias were fairly frequent in gorillas. Moreover, they noted that among hominin fossil endocasts, the characteristic modern human-like petalia torque pattern does not reliably occur until the emergence of Homo erectus. Others have suggested that the petalia torque is unique to Homo sapiens and is related to a genetic mutation that was critical to the evolution of novel cognitive capacities in our lineage (Crow, 2004). In contrast to these studies, Hopkins and colleagues (Hopkins & Marino, 2000; Pilcher, Hammock, & Hopkins, 2001) used magnetic resonance imaging of great ape, Old World and New World monkey brains and found that great apes followed the human pattern, showing a right-frontal and left-occipital petalia asymmetry. However, Old World and New World monkeys did not display any significant cerebral asymmetries. Thus, whether nonhuman primates show cerebral petalias remains unclear.
The relationship between petalias and handedness in humans also remains unresolved. While there is some evidence that a wider right frontal lobe combined with a wider left occipital lobe is more common in right-handed individuals than nonright-handed individuals (Kertesz, Black, Polk, & Howell, 1986; LeMay & Kido, 1978), several recent voxel-based morphometry analyses of structural asymmetries have failed to find an association between petalias and hand preference (Good et al., 2001; Herve, Crivello, Perchey, Mazoyer, & Tzourio-Mazoyer, 2006; Watkins et al., 2001).
Interestingly, no study has investigated both cerebral petalias and handedness in nonhuman primates. Here, we investigate whether capuchins display cerebral petalias and if these are related to handedness. Capuchins are noted for their high degree of skilled motor and extractive foraging habits. Additionally, capuchins express strong and consistent hand preferences during tasks that require complex bimanual coordination (e.g., Fragaszy & Mitchell, 1990; Spinozzi, Castorina, & Truppa, 1998; Westergaard and Suomi, 1993, Westergaard and Suomi, 1996). Therefore, we hypothesized that petalias would be present and their pattern would be associated with handedness.
Section snippets
Subjects
In vivo magnetic resonance images and behavioral data were collected from 13 capuchin monkeys (Cebus apella; male n = 7, female n = 6). Subjects were socially housed at Hiram College (Hiram, Ohio), Northeastern Ohio Universities College of Medicine (Rootstown, Ohio) or the College of Wooster (Wooster, Ohio). Ages ranged from 1 to 21 years (M = 10.23, S.D. = 6.61).
Behavioral measures
Hand preference was determined for each subject through a coordinated bimanual task known as the tube task (Hopkins, 1995). This task was
Results
Individual MHI values for the tube task, classification into dextral group and asymmetry quotients for all regional petalias are displayed in Table 1. Fig. 2 displays the mean (±S.E.) AQ score for each region. Data did not violate assumptions of normality; therefore, parametric statistics were used. No sex differences were found in handedness or in cerebral width asymmetry for any of the regions; therefore subsequent analyses pooled male and female data.
As some have reported that hand
Discussion
The results of this study showed that population-level left-frontal petalia asymmetry is present in capuchins. However, no relationship exists between handedness and petalias in any region.
Our finding of a left-frontal and no occipital petalia contrasts with the other published studies on petalias of New World monkeys (Hopkins & Marino, 2000; LeMay, 1976, Pilcher et al., 2001). LeMay reported a left-occipital and no frontal protrusion in her sample, whereas Hopkins and Marino (2000) and Pilcher
Acknowledgements
This work was supported by the HHMI, NIH (NS-42867), NSF (BCS-0515484), the Wenner-Gren Foundation and Hiram College. The American Psychological Association's guidelines concerning the ethical treatment of animals were followed during the course of this study. We thank Dr. Claudia Thompson and Leah Michelson for collecting behavioral data on the Wooster capuchins, Courtney Buzzell and Dr. William D. Hopkins for helpful comments on a previous draft of this manuscript, and the staff of the Brain
References (23)
- et al.
Cerebral asymmetry and the effects of sex and handedness on brain structure: A voxel-based morphometric analysis of 465 normal adult human brains
NeuroImage
(2001) - et al.
Handedness and cerebral anatomical asymmetries in young adult males
NeuroImage
(2006) - et al.
Asymmetries in cerebral width in nonhuman primate brains as revealed by magnetic resonance imaging (MRI)
Neuropsychologia
(2000) - et al.
Cerebral asymmetries on magnetic resonance imaging
Cortex
(1986) - et al.
Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis)
Cognitive Brain Research
(2005) The emergence of cerebral asymmetries in early human development: A literature review and a neuroembryological model
- et al.
Heritability and association of cortical petalia in rhesus monkeys (Macaca mulatta)
Brain, Behavior, and Evolution
(1990) Directional asymmetry is the key to the origin of modern Homo sapiens (the Broca-Annett axiom). Response to Lesley Rogers
Laterality
(2004)- et al.
Cortical asymmetries in the frontal lobe of rhesus monkeys (Macaca mulatta)
Brain Research
(1991) - et al.
Hand preference and performance on unimanual and bimanual tasks in capuchin monkeys (Cebus apella)
Journal of Comparative Psychology
(1990)
Brain endocast asymmetry in pongids and hominids: Some preliminary findings of the paleontology of cerebral dominance
American Journal of Physical Anthropology
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2022, Neuroscience and Biobehavioral ReviewsBrain asymmetries and handedness in the specimens from the Sima de los Huesos site (Atapuerca, Spain)
2017, Quaternary InternationalCitation Excerpt :Contrary to these studies, Chui and Damasio (1980) results suggest that handedness and cerebral asymmetries are independent variables. Phillips and Sherwood (2007) also allude to several recent voxel-based morphometry analyses of structural asymmetries that have failed to demonstrate an association between petalias and hand preference (Good et al., 2001; Watkins et al., 2001; Herve et al., 2006). Faglioni and Scarpa (1989) also reported findings of surprisingly weak relationships between handedness and cerebral asymmetries in a sample of 160 patients (Steele, 2000).
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2013, Behavioural ProcessesCitation Excerpt :These results are in agreement with Diezinger and Anderson (1986), which found that rhesus macaques did not show a manual preference for scratching themselves in a social tense situation, but differ from previous studies on chimpanzees in which handedness emerged when performing self-directed behaviors (Dimond and Harries, 1984; Leavens et al., 2001) and subjects preferentially scratched one side of the body (Hopkins et al., 2006; Leavens et al., 2004). Since the hand and side preference for self-directed behaviors has been related to brain asymmetries that are supposed to be present in apes and humans but not in monkeys (Dimond and Harries, 1984), and yet Phillips and Sherwood (2007) have recently demonstrated in capuchins the presence of a left frontal petalia (i.e., a greater protrusion of the left cerebral hemisphere relative to the right hemisphere as expressed at the frontal pole of the brain), further studies should thorough investigate this issue in monkeys. This is one of the first studies that measured self-directed behaviors in a cognitive task.
Sex difference in squirrel monkeys' handedness for unimanual and bimanual coordinated tasks
2012, Animal BehaviourCitation Excerpt :Only females were right-handed for the unimanual task and not the males, whereas the bimanual task elicited a population-level left-hand bias approaching conventional levels of statistical significance only in males. Similar sex effects on the direction of population-level handedness have also been demonstrated not only for unimanual behaviours (e.g. in baboons, Meunier et al. 2011) but also for bimanual coordinated feeding in wild chimpanzees (Corp & Byrne 2004), in rehabilitated orang-utans (Rogers & Kaplan 1996) and somewhat in captive gorillas (i.e. borderline significance for the sex effect, Meguerditchian et al. 2010) and for the bimanual tube task in De Brazza’s monkeys (Schweitzer et al. 2007) and capuchin monkeys (Spinozzi et al. 1998; Meunier & Vauclair 2007; Phillips & Sherwood 2007). In all these studies, females were more right-handed than males or males were more left-handed than females at a group level.