The sound of one-hand clapping: handedness and perisylvian neural correlates of a communicative gesture in chimpanzees

Abstract

Whether lateralization of communicative signalling in non-human primates might constitute prerequisites of hemispheric specialization for language is unclear. In the present study, we examined (i) hand preference for a communicative gesture (clapping in 94 captive chimpanzees from two research facilities) and (ii) the in vivo magnetic resonance imaging brain scans of 40 of these individuals. The preferred hand for clapping was defined as the one in the upper position when the two hands came together. Using computer manual tracing of regions of interest, we measured the neuroanatomical asymmetries for the homologues of key language areas, including the inferior frontal gyrus (IFG) and planum temporale (PT). When considering the entire sample, there was a predominance of right-handedness for clapping and the distribution of right-and left-handed individuals did not differ between the two facilities. The direction of hand preference (right-versus left-handed subjects) for clapping explained a significant portion of variability in asymmetries of the PT and IFG. The results are consistent with the view that gestural communication in the common ancestor may have been a precursor of language and its cerebral substrates in modern humans.

From Grasping to Grooming to Gossip: Innovative Use of Chimpanzee Signals in Novel Environments Supports Both Vocal and Gestural Theories of Language Origins

“…Hopkins and his colleagues (Cantalupo and Hopkins 2001;) and others (e.g., Gannon et al 1998) have demonstrated that these "language" areas can be identified in the brains of great apes, and they are also asymmetrically larger, on average, in the left cerebral hemispheres of these close human relatives, although not every study of Broca's area homologues in great ape brains finds this asymmetry, suggesting that the degree of asymmetry, here, is less robust in great apes than in humans (e.g., Meguerditchian et al 2012;Schenker et al 2010). In related work, there is some evidence that chimpanzees display a weak but significant right-hand bias for bimanual grooming, implicating a left-hemisphere dominance for this activity (e.g., Hopkins et al 2007a).…”

Human handedness: An inherited evolutionary trait

“…[52][53][54][55][56][57], others have reported right-hand biases in chimpanzees (Pan troglodytes) for: bimanual feeding, coordinated bimanual actions, bipedal reaching and throwing [for reviews, see 58,59], in captive gorillas for bimanual feeding [60] and 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 7 for communicative gesture in chimpanzees [e.g. 10,61,62]. Alternatively, it has been noted that orangutans a exhibited a significant left-hand preference for scratching and for fine manipulation of parts of the face in rehabilitated orangutans [63], while chimpanzees exhibited a significant increase in left-handed self-directed behaviors with increased in task complexity [64] contending that self-directed behaviors may be influenced by motivational factors underpinned by a right hemisphere dominance within both social and nonsocial contexts.…”

What can atypical language hemispheric specialization tell us about cognitive functions?

“…Furthermore, the direction of hand preference for clapping explains a significant portion of the variability in asymmetries of the planum temporale and inferior frontal gyrus [30] . In contrast, no signifi cant population-level cerebral structural asymmetries have been reported in the macaque, except for the surface area of the superior temporal sulcus [31] .…”

“…Chimpanzees, our closest relatives, show both a bias towards right-handedness at the population-level [30] and brain structural asymmetries in regions homologous with human language-relevant regions [31] . Furthermore, the direction of hand preference for clapping explains a significant portion of the variability in asymmetries of the planum temporale and inferior frontal gyrus [30] .…”

“…Although the hemispheric lateralization of language is a specifi c cortical feature of the human brain, it is now clear that asymmetries of brain and behavior exist not only in humans but also in vertebrates and invertebrates [30][31][32][33] .…”