Chimpanzee (Pan troglodytes) Precentral Corticospinal System Asymmetry and Handedness: A Diffusion Magnetic Resonance Imaging Study

Li, Longchuan; Preuss, Todd M.; Rilling, James K.; Hopkins, William D.; Glasser, Matthew F.; Kumar, B.S. Hemanth; Nana, Roger; Zhang, Xiaodong; Hu, Xiaoping

doi:10.1371/journal.pone.0012886

Cited by 37 publications

(28 citation statements)

References 90 publications

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“…In chimpanzees, a positron emission tomography study showed activation in the KNOB region in the hemisphere contralateral to the hand used during a reach-and-grasp task [Hopkins et al 2010b], suggesting that the KNOB may similarly represent the cortical substrate of the hand in this species. Finally, in both humans and chimpanzees, anatomical asymmetries in the KNOB have been linked to individual differences in hand preference and skill at the level of gross morphology [Amunts et al 1996; Foundas et al 1998; Hopkins and Cantalupo 2004; Kloppel et al 2010; Li et al 2009] and histology [Sherwood et al 2010; Sherwood et al 2007]. These findings reinforce the view that the motor hand area of the precentral gyrus may represent the neural substrate of the hand and possibly handedness.…”

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confidence: 76%

Evolution of the Central Sulcus Morphology in Primates

Hopkins¹,

Meguerditchian²,

Coulon³

et al. 2014

Brain Behav Evol

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The central sulcus (CS) divides the pre- and postcentral gyri along the dorsal-ventral plane of which all motor and sensory functions are topographically organized. The motor-hand area of the precentral gyrus or KNOB has been described as the anatomical substrate of the hand in humans. Given the importance of the hand in primate evolution, here we examine the evolution of the motor-hand area by comparing the relative size and pattern of cortical folding of the CS surface area from magnetic resonance images in 131 primates, including Old World monkeys, apes and humans. We found that humans and great apes have a well-formed motor-hand area that can be seen in the variation in depth of the CS along the dorsal-ventral plane. We further found that great apes have relatively large CS surface areas compared to Old World monkeys. However, relative to great apes, humans have a small motor-hand area in terms of both adjusted and absolute surface areas.

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confidence: 76%

Evolution of the Central Sulcus Morphology in Primates

Hopkins¹,

Meguerditchian²,

Coulon³

et al. 2014

Brain Behav Evol

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“…In addition to behavioral studies, advances in neuroimaging have identified links between brain structure and hand preferences measured by the TUBE task in capuchin monkeys and chimpanzees [e.g., Dadda et al, 2006;Hopkins & Cantalupo, 2004;Li et al, 2010;Phillips & Hopkins, 2007;Phillips & Sherwood, 2005]. Recent work in A. geoffroyi using diffusion-tensor imaging found that the structural fibers of the corpus callosum were similar to that of chimpanzees and humans, but differed from that of rhesus monkeys, Macaca mulatta [Platas-Neri et al, 2015].…”

Section: Discussionmentioning

confidence: 99%

Precise digit use increases the expression of handedness in Colombian spider monkeys (Ateles fusciceps rufiventris)

Nelson

Boeving

2015

American J Primatol

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Decades of research on the hand use patterns of nonhuman primates can be aptly summarized by the following phrase: measurement matters. There is a general consensus that simple reaching is a poor indicator of handedness in most species, while tasks that constrain how the hands are used elicit individual, and in some cases, population-level biases. The TUBE task has become a popular measure of handedness, although there is variability in its administration across studies. The goal of this study was to investigate whether TUBE performance is affected by tube diameter, with the hypothesis that decreasing tube diameter would increase task complexity, and therefore the expression of handedness. We predicted that hand preference strength, but not direction, would be affected by tube diameter. We administered the TUBE task using a 1.3 cm tube to Colombian spider monkeys, and compared their performance to a previous study using a larger 2.5 cm diameter tube. Hand preference strength increased significantly on the smaller diameter tube. Hand preference direction was not affected. Notably, spider monkeys performed the TUBE task using a single digit, despite the longstanding view that this species has poor dexterity. We encourage investigators who use the TUBE task to carefully consider the diameter of the tube used in testing, and to report digit use consistently across studies. In addition, we recommend that researchers who cannot use the TUBE task try to incorporate the key features from this task into their own species appropriate measures: bimanual coordination and precise digit use.

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“…This is a relatively crude measure of WM organization. Ideally, studies comparing THROWþ and THROW2 apes using more sensitive measures of WM connectivity, such as DTI, would be more informative of the possible changes in cortical connectivity between the IFG and KNOB in these cohorts of apes [58,59].…”

Section: Discussionmentioning

confidence: 99%

The neural and cognitive correlates of aimed throwing in chimpanzees: a magnetic resonance image and behavioural study on a unique form of social tool use

Hopkins

Russell²,

Schaeffer³

2012

Phil. Trans. R. Soc. B

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It has been hypothesized that neurological adaptations associated with evolutionary selection for throwing may have served as a precursor for the emergence of language and speech in early hominins. Although there are reports of individual differences in aimed throwing in wild and captive apes, to date there has not been a single study that has examined the potential neuroanatomical correlates of this very unique tool-use behaviour in non-human primates. In this study, we examined whether differences in the ratio of white (WM) to grey matter (GM) were evident in the homologue to Broca's area as well as the motor-hand area of the precentral gyrus (termed the KNOB) in chimpanzees that reliably throw compared with those that do not. We found that the proportion of WM in Broca's homologue and the KNOB was significantly higher in subjects that reliably throw compared with those that do not. We further found that asymmetries in WM within both brain regions were larger in the hemisphere contralateral to the chimpanzee's preferred throwing hand. We also found that chimpanzees that reliably throw show significantly better communication abilities than chimpanzees that do not. These results suggest that chimpanzees that have learned to throw have developed greater cortical connectivity between primary motor cortex and the Broca's area homologue. It is suggested that during hominin evolution, after the split between the lines leading to chimpanzees and humans, there was intense selection on increased motor skills associated with throwing and that this potentially formed the foundation for left hemisphere specialization associated with language and speech found in modern humans.

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Chimpanzee (Pan troglodytes) Precentral Corticospinal System Asymmetry and Handedness: A Diffusion Magnetic Resonance Imaging Study

Cited by 37 publications

References 90 publications

Evolution of the Central Sulcus Morphology in Primates

Evolution of the Central Sulcus Morphology in Primates

Precise digit use increases the expression of handedness in Colombian spider monkeys (Ateles fusciceps rufiventris)

The neural and cognitive correlates of aimed throwing in chimpanzees: a magnetic resonance image and behavioural study on a unique form of social tool use

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