A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping

Abstract

Although lesion and functional imaging studies have broadly implicated the right hemisphere in the recognition of emotion, neither the underlying processes nor the precise anatomical correlates are well understood. We addressed these two issues in a quantitative study of 108 subjects with focal brain lesions, using three different tasks that assessed the recognition and naming of six basic emotions from facial expressions. Lesions were analyzed as a function of task performance by coregistration in a common brain space, and statistical analyses of their joint volumetric density revealed specific regions in which damage was significantly associated with impairment. We show that recognizing emotions from visually presented facial expressions requires right somatosensory-related cortices. The findings are consistent with the idea that we recognize another individual's emotional state by internally generating somatosensory representations that simulate how the other individual would feel when displaying a certain facial expression. Follow-up experiments revealed that conceptual knowledge and knowledge of the name of the emotion draw on neuroanatomically separable systems. Right somatosensory-related cortices thus constitute an additional critical component that functions together with structures such as the amygdala and right visual cortices in retrieving socially relevant information from faces.

Fig. 1.

Histograms of performances in Experiment 1. Shown are the number of subjects with a given correlation score for each emotion category. The subjects' ratings of 36 emotional facial expressions were correlated with the mean ratings from 18 normal controls for each face stimulus and then averaged for each emotion category. The number of subjects is encoded by the gray scale value (scale at top). Red lines,Division into the 54 subjects with the lowest and the 54 with the highest scores. Blue areas, Means (circles) and 2 SDs (error bars) of correlations among the 18 normal controls. These correlations were calculated between each normal individual and the remaining 17. disg, Disgusted;surpr, surprised.

Fig. 2.

Distribution of lesions as a function of mean emotion recognition (Experiment 1). a, Lesion overlaps from all 108 subjects. Color (scale attop) encodes the difference in the density of lesions between the subjects with the lowest and those with the highest scores. Thus, redregions correspond to locations at which lesions resulted in impairment more often than not, andblueregions correspond to locations at which lesions resulted in normal performance more often than not.p values indicating statistical significance are shown in white for voxels in four regions (white squares) on coronal cuts (bottom) that correspond to the whiteverticallines in the three-dimensional reconstructions (top). Because adjacent voxels cannot be considered independent, we analyzed the significance of six specific separate voxels, determined a priori from the density distribution of all 108 lesions, as follows. We selected contiguous regions within which at least nine subjects had lesions and picked the voxel at the centroid of each of these regions. The voxels (white squares shown in the coronal cuts at the bottom; the two in the temporal lobe not shown because lesions there did not result in impaired emotion recognition) were located in six regions; details are given in Table 2. Voxels were chosen by one of us (G.C.) who was blind to the outcome of the task data. The central sulcus is shown ingreen. b, Three examples of individual subjects' lesions in the right frontoparietal cortex. Two lesions (left, middle) are from subjects in the bottom partition who had the smallest lesions; the other lesion (right)is from a subject in the top partition. The data from these three subjects provide further evidence, at the individual subject level, that lesions in somatosensory cortices impair the recognition of facial emotion. The central sulcus is shown in green.

Fig. 3.

Distribution of lesion overlaps from the most-impaired and the least-impaired 25% of subjects. Subjects were again partitioned using the mean emotion correlation from Experiment 1. Lesion overlaps from the 27 least-impaired subjects were subtracted from those of the 27 most-impaired subjects; data from the middle 54 subjects were not used. The resulting images are directly comparable with those in Figure 2 but show more focused regions of difference because of the extremes of performances that are being compared. Coronal cuts are shown on the left, and three-dimensional reconstructions of brains that are rendered partially transparent are shown on the right, indicating the level of the coronal cuts (whiteverticallines) and the location of the central sulcus (green).

Fig. 4.

Neuroanatomical regions critical for naming or for sorting emotions. Images were calculated as described in Figure2a. a, Neuroanatomical regions critically involved in choosing the name of an emotion (Experiment 2).b, Neuroanatomical regions critically involved in sorting emotions into categories without requiring naming (Experiment 3).