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. 2013 Aug 28;33(35):14117-34.
doi: 10.1523/JNEUROSCI.2172-13.2013.

Differences in Neural Activation for Object-Directed Grasping in Chimpanzees and Humans

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Free PMC article

Differences in Neural Activation for Object-Directed Grasping in Chimpanzees and Humans

Erin E Hecht et al. J Neurosci. .
Free PMC article

Abstract

The human faculty for object-mediated action, including tool use and imitation, exceeds that of even our closest primate relatives and is a key foundation of human cognitive and cultural uniqueness. In humans and macaques, observing object-directed grasping actions activates a network of frontal, parietal, and occipitotemporal brain regions, but differences in human and macaque activation suggest that this system has been a focus of selection in the primate lineage. To study the evolution of this system, we performed functional neuroimaging in humans' closest living relatives, chimpanzees. We compare activations during performance of an object-directed manual grasping action, observation of the same action, and observation of a mimed version of the action that consisted of only movements without results. Performance and observation of the same action activated a distributed frontoparietal network similar to that reported in macaques and humans. Like humans and unlike macaques, these regions were also activated by observing movements without results. However, in a direct chimpanzee/human comparison, we also identified unique aspects of human neural responses to observed grasping. Chimpanzee activation showed a prefrontal bias, including significantly more activity in ventrolateral prefrontal cortex, whereas human activation was more evenly distributed across more posterior regions, including significantly more activation in ventral premotor cortex, inferior parietal cortex, and inferotemporal cortex. This indicates a more "bottom-up" representation of observed action in the human brain and suggests that the evolution of tool use, social learning, and cumulative culture may have involved modifications of frontoparietal interactions.

Figures

Figure 1.
Figure 1.
Chimpanzee behavioral tasks. A, Reach-to-grasp action used in tasks. The ball is fed into a downward-slanting chute. The chimpanzee reaches toward and grasps the ball, navigates around the internal divider, and places the ball into another chute, where it rolls back to the experimenter. B, Action execution condition. The chimpanzee performed the reach-to-grasp action while an experimenter passed the ball through the chutes. This experimenter was hidden behind an opaque screen, but a second, inactive experimenter was visible. This controlled for the presence of a visible human in the observation condition and also allowed the chimpanzee's behavior to be monitored. All sides of the box were opaque, so the chimpanzee could not see his own hand movements. C, Transitive and intransitive observation conditions. The top and 1 side of the box were replaced with clear Plexiglas. The experimenter performing the actions was visible, but the second experimenter was hidden. In the transitive observation condition, the experimenter performed the actions as in A. In the intransitive observation condition, the experimenter mimed these same actions without touching any object. D, Control for the perception of object movement in the intransitive observation condition. The ball was slid in and out of the box along a transparent thread, interspersed with the experimenter's mimed grasping actions. The chimpanzee was unable to see the experimenter's hand moving the thread.
Figure 2.
Figure 2.
Transitive grasping stimuli observed by chimpanzees and humans. A, Screenshots from human video stimuli (Peeters et al., 2009). B, Photograph of chimpanzee live-action demonstration.
Figure 3.
Figure 3.
Chimpanzee cortical anatomy and ROIs. Left hemispheres appear on the left. A, Chimpanzee cortical anatomy. Architectonic areas (top) and surface morphology of cerebral cortex (bottom). The nomenclature for sulci and gyri is based on Bailey et al. (1950), although our abbreviations follow more modern conventions. Cortical areas are denoted according to the system of Bailey et al. (1950) and Bailey (1948) based on Economo's system in humans (Economo and Parker, 1929). For most areas, there is a fairly straightforward correspondence between the Bailey et al. (1950) areas and their counterparts in Brodmannn's human map (Brodmannn, 1909; Von Bonin, 1948), and we have added Brodmannn numbers in parentheses below the Bailey et al. (1950) symbols. Areas thought to be homologous to BA 44 and BA 45 of humans occupy the posterior inferior frontal gyrus and adjacent part of the inferior frontal sulcus in chimpanzees, as discussed by Schenker et al. (2010). B, ROIs in FCBm and PFD/PF in each subject. CS, central sulcus; FOS, frontoorbital sulcus; IFG, inferior frontal gyrus; IFS, inferior frontal sulcus; IPL, inferior parietal lobule; IPS, intraparietal sulcus; LCaS, lateral calcarine sulcus; LOTS, lateral occipitotemporal sulcus; LS, lateral sulcus; LuS, lunate sulcus; MFG, middle frontal gyrus; MTG, middle temporal gyrus; MTS, middle temporal sulcus; PoCG, postcentral gyrus; PoCS, postcentral sulcus; PrCG, precentral gyrus; PrCS, precentral sulcus; SFG, superior frontal gyrus; SFS, superior frontal sulcus; SPL, superior parietal lobule.
Figure 4.
Figure 4.
3D surface renderings of group-level SPM statistical comparisons between conditions. Left hemispheres appear on the left. SPM5 analysis thresholded at p < 0.05. A, Execution > Rest. B, Transitive Observation > Rest. C, Intransitive Observation > Rest. D, Execution > Transitive Observation. E, Execution > Intransitive Observation. F, Transitive Observation > Execution. G, Intransitive Observation > Execution. H, Transitive Observation > Intransitive Observation. I, Intransitive Observation > Transitive Observation.
Figure 5.
Figure 5.
Coronal slices of group-level SPM statistical comparisons between conditions. Left hemispheres appear on the left. SPM5 analysis thresholded at p < 0.05.
Figure 6.
Figure 6.
3D surface renderings of top 1% of activity in chimpanzee subjects during each individual condition and in conjunction analyses. Left hemispheres appear on the left.
Figure 7.
Figure 7.
3D surface renderings of overlap of above-threshold activation across chimpanzee subjects in individual conditions and in conjunction analyses. Left hemispheres appear on the left. A, Execution. B, Transitive Observation. C, Intransitive Observation. D, Voxels activated above threshold in both Execution and Transitive Observation. E, Voxels activated above threshold in both Execution and Intransitive Observation.
Figure 8.
Figure 8.
Cortical slices of overlap of above-threshold activation across chimpanzee subjects in individual conditions and in conjunction analyses. Left hemispheres appear on the left. A, Execution. B, Transitive Observation. C, Intransitive Observation. D, Voxels activated above threshold in both Execution and Transitive Observation. E, Voxels activated above threshold in both Execution and Intransitive Observation.
Figure 9.
Figure 9.
Quantification of activity in chimpanzee regions homologous to those that contain mirror neurons in macaques. A, ROI activation in individual conditions. Percentage of ROIs active in each condition were averaged across subjects. An initial repeated-measures ANOVA showed no effect of hemisphere, so data were averaged bilaterally for each ROI. Activation was greater in execution, transitive observation, and intransitive observation relative to rest, as measured with a repeated-measures ANOVA (main effect of task condition, F(3,9) = 14.185, p < 0.001; individual comparisons, p = 0.004, 0.007, and 0.026, respectively). In addition, the FCBm was more active than PFD/PF (main effect of region, F(1,3) = 17.386, p = 0.014). B, ROI activation in conjunction analyses. Percentage of voxels in top 1% of execution condition which were also in top 1% of transitive observation or intransitive observation conditions in FCMb and PF, averaged across subjects. A repeated-measures ANOVA revealed no effect of condition, but a main effect of region (F(1,3) = 16.076, p = 0.028); the frontal ROI was more active than the parietal ROI.
Figure 10.
Figure 10.
Human activation during transitive grasping observation. Left hemispheres appear on the left. A, Top 1% of activity in individual subjects. B, Overlap of above-threshold activation across subjects.
Figure 11.
Figure 11.
Quantitative comparison of chimpanzee and human activation during transitive grasping observation. A, ROIs. B, Percentage of total above-threshold activation that fell into each ROI. Inferior parietal lobule (IPL), inferotemporal cortex (IT), and PMv accounted for a significantly greater proportion of overall activation in humans than in chimpanzees (p = 0.036, p < 0.001, and p < 0.001, respectively; independent samples t test). Ventrolateral prefrontal cortex (VLPFC) accounted for a significantly greater proportion of overall activation in chimpanzees than in humans (p = 0.033, independent samples t test). Error bars, ±1 SEM. DLPFC, dorsolateral prefrontal cortex; PMd, dorsal premotor cortex; PMv, ventral premotor cortex; M1, primary motor cortex; S1–S2, primary and secondary somatosensory cortex; LOC, lateral occipital cortex; STS, superior temporal sulcus.

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