Neuroanatomical asymmetries and handedness in chimpanzees (Pan troglodytes): a case for continuity in the evolution of hemispheric specialization

Abstract

Many historical and contemporary theorists have proposed that population-level behavioral and brain asymmetries are unique to humans and evolved as a consequence of human-specific adaptations such as language, tool manufacture and use, and bipedalism. Recent studies in nonhuman animals, notably primates, have begun to challenge this view. Here, I summarize comparative data on neuroanatomical asymmetries in the planum temporale (PT) and inferior frontal gyrus (IFG) of humans and chimpanzees, regions considered the morphological equivalents to Broca's and Wernicke's areas. I also review evidence of population-level handedness in captive and wild chimpanzees. When similar methods and landmarks are used to define the PT and IFG, humans and chimpanzees show similar patterns of asymmetry in both cortical regions, though humans show more pronounced directional biases. Similarly, there is good evidence that chimpanzees show population-level handedness, though, again, the expression of handedness is less robust compared to humans. These results stand in contrast to reported claims of significant differences in the distribution of handedness in humans and chimpanzees, and I discuss some possible explanations for the discrepancies in the neuroanatomical and behavioral data.

Figure 1

Distribution of asymmetries in humans and chimpanzees for (a) the planum temporale (PT) and (b) posterior superior temporal gyrus (pSTG).

Figure 2

3D reconstruction of a chimpanzee brain with the sylvian fissure (SF) and superior temporal sulcus (STS) identified on the lateral surface. (a-c) are the points along the posterior superior temporal gyrus that have been rotated into the coronal plane to show the landmarks used to delineate the pSTG.

Figure 3

(A) Location of the FO and PCI sulci in relation to the curvature of the frontal cortex as seen in an axial view of the chimpanzee brain template. (B) Orientation of the para-sagittal planes of cutting for the right (R) and left (L) POP. (C) Example of a para-sagittal slice showing the borders defining the POP region. (D) Manual tracing of the POP on the same para-sagittal slice. FO = Fronto-Orbital Sulcus; PCI = Pre-Central Inferior Sulcus; POP = Pars Opercularis; A–P = Anterior-Posterior Axis; SF = Sylvian Fissure

Figure 4

Distribution of handedness in a sample of 300 chimpanzees based on consistency in hand use across four different measures. SR = strongly right-handed, MR = moderately right-handed, A = ambidextrous, ML = moderately left-handed, SL = strongly left-handed.

Figure 5

Mean HI scores (+/− s.e.) for the TUBE tasks for five separate chimpanzee samples. MONO = Mono Foundation Santuary and Chimfunshi Wildlife Orphanage, PFA= Primate foundation of Arizona, YNPRC = Yerkes National Primate Research Center, UTMDACC = University of Texas M. D. Anderson Cancer Center, APF = Alamogordo Primate Facility.

Figure 6

(a) Midsagittal view of the corpus callosum in a chimpanzee MRI scans. Different colors indicate different regions of the corpus callosum. Green = genu, cyan = anterior midbody, blue = central midbody, red = isthmus, yellow = splenium. (b) Mean ratio (+/− s.e.) in corpus callosum size to total brain volume in different primate families (data regraphed from Rilling et al.).