Laterality effect for faces in chimpanzees (Pan troglodytes)

Abstract

Face perception in humans is governed more by right-hemispheric than left-hemispheric neural correlate. Some but not all neurophysiological studies depict a right-side dominance for face responsive neurons in the brains of macaques. Hence, it is an open question whether and to what extent a right-hemisphere preference of processing faces exists across primate brains. We investigated chimpanzees discriminating chimeric faces of chimpanzees and humans, i.e., the combination of either left or right sides of a face vertically flipped and merged into a whole face. We found an effect of choosing the left-chimeric face more often than the right-chimeric face as being the one of the two that is closer to the original face, reflecting an advantage for the right side of the brain to process faces, as reported in humans. Moreover, we found a modulation by age of the participants, suggesting that the exposure history with a particular category shapes the right-hemispheric neural correlate to a configural/holistic processing strategy. In other words, the findings in chimpanzee participants parallel those in human participants and are suggestive for similar neural machineries in the occipital-temporal cortices in both species.

Figure 1.

Laterality effect. A, Example stimuli of chimpanzee and human original and chimeric faces. B, Left-chimeric face bias for chimpanzee participants. Colored lines indicate the participants' responses plotted as a cumulative function of left–right decisions (x-axis) over time (y-axis, trials). The light red bar distribution around the zero line shows an iterative randomization procedure of left–right decisions indicating the significance level of 5%. C, Left-chimeric face bias for human participants. Gray lines indicate the participants' responses plotted as a cumulative function of left–right decisions (x-axis) over time (y-axis, trials) for chimpanzee (dark) and human (light) faces. D, Correlation of laterality biases and classification performance indices of chimpanzee participants. The x-axis shows the discrimination bias, i.e., the subtraction of performance scores for chimpanzee faces from those for human faces. Positive values indicate better performance for chimpanzee than human faces. The y-axis indicates the left chimeric face bias, i.e., the subtraction of the left-chimeric face biases for chimpanzee faces from those for human faces. Positive values indicate a stronger bias for chimpanzee than human faces. Individual participants are marked by a colored circle. E, Distributions of p values for chimpanzee participants. Binominal tests were conducted for each point in time to determine the effect of left-chimeric face biases. The color lines represent the participants, the dashed line represents the significance level of 5%, while the arrowheads mark the individual significance level of 5% (black) and 6.5% (gray, Y1 for human faces). F, Distributions of p values for human participants. Binomial tests were conducted similar to chimpanzee participants. G, Negative correlation between the left-chimeric face biases for chimpanzee and human face stimuli. Colored lines indicate the participants; the gray-yellow background indicates the level of significance (while black circles mark p < 0.05). H, Level of expertise. The performances of chimpanzee-novice and chimpanzee-expert human participants were contrasted for chimpanzee and human chimeric faces.