Functional lateralization of face, hand, and trunk representation in anatomically defined human somatosensory areas

Abstract

We used functional magnetic resonance imaging (fMRI) and cytoarchitectonic probability maps to investigate the responsiveness of individual areas in the human primary and secondary somatosensory cortices to hand, face, or trunk stimulation of either body-side. A Bayesian modeling approach to quantify the probability of ipsilateral activations revealed that areas OP 1, OP 4, and OP 3 of the SII cortex as well as the trunk and face representations within all SI subareas (areas 3b, 1, and 2) show robust bilateral responses to unilateral stimulation. Such bilateral response properties are in good agreement with the transcallosal projections demonstrated for these areas in nonhuman primates and other mammals. In contrast, the SI hand region showed a different pattern. Whereas ipsilateral areas 3b and 1 were deactivated by tactile hand stimulation, particularly on the left, there was strong evidence for ipsilateral processing of information from the right hand in area 2. These results demonstrate not only the behavioral importance of the hand representation, but also suggest that area 2 may have particularly evolved to form the cortical substrate of these specialized demands, in line with recent studies on cortical evolution hypothesizing that area 2 has developed with increasing manual abilities in anthropoid primates featuring opposable thumbs.

Figure 1.

Schematic overview on the skin surface stimulated for each of the different body part conditions. Face and trunk were stimulated with a sponge rubbed in a back-and-forth motion in a rostrocaudal direction, for stimulation of the hands the sponge was rubbed in a back-and-forth motion from proximal to distal.

Figure 2.

Inference on the Bayesian model estimated in this study for every voxel of the primary and somatosensory cortex was performed by computing the area under the posterior probability density function. The posterior probability for an activation was given by the portion of the density function which was located to the right of the positive gamma threshold (background noise level as given by the prior standard deviation, i.e., variance across voxels), that for deactivation by the part of the density function which was upper-bounded by the negative gamma threshold.

Figure 3.

The location of the defined ROIs (given by their anatomical location within the SI respectively SII subareas, a posterior probability for activation following stimulation of the respective body part on either side of > 95% and a probability of > 90% for showing stronger activation than both of the 2 other examined body parts) reveals the somatotopic organization of the human primary (A) and secondary (B) somatosensory cortices. For the display of the somatotopic ROIs in the secondary somatosensory cortex, the temporal lobes have been removed from the template brain in order to allow an unobstructed view on the parietal operculum. Note that the respective ROIs are mutually exclusive in 3-dimensional space but may overlap in the projection of their location to the cortical surface.

Figure 4.

Mean posterior probabilities for activation (green) and deactivation (red) following ipsilateral trunk stimulation as well as those for activation following contralateral trunk stimulation are given for each of the 3 analyzed areas of the primary and secondary somatosensory cortex on either side of the brain. All cortical areas within the SI and SII region show a strong bilateral response to tactile stimulation of the trunk, as the probabilities for ipsilateral activation were no lower than those following contralateral stimulation.

Figure 5.

Mean posterior probabilities for activation (green) and deactivation (red) following ipsilateral face stimulation as well as those for activation following contralateral face stimulation are given for each of the 3 analyzed areas of the primary and secondary somatosensory cortex on either side. Similar to the trunk regions within SI and SII (Fig. 4), also the head representations within the analyzed areas showed a pronounced ipsilateral response. However, the posterior probabilities for ipsilateral activation within these regions were slightly lower as compared with those observed within the trunk representations.

Figure 6.

Mean posterior probabilities for activation (green) and deactivation (red) following ipsilateral hand stimulation as well as those for activation following contralateral hand stimulation are given for each of the 3 analyzed areas of the primary and secondary somatosensory cortex on either side of the brain. All subareas of the secondary somatosensory cortex responded well to ipsilateral tactile stimulation of the hands, although the mean probabilities for activation were considerably lower as compared with those observed within the trunk and face regions (Figs 4 and 5). In contrast, areas 3b and 1 of the primary somatosensory cortex showed a deactivation following ipsilateral hand stimulation, which was more pronounced in the left hemisphere. Left area 2 finally was also deactivated by ipsilateral stimuli, whereas right area 2 was the only part of the primary somatosensory cortex showing a substantial positive response to ipsilateral tactile stimulation.

Figure 7.

Mean (±SEM) of the individual effect size estimates (beta-values) for each condition extracted from the single-subject analyses. The close correspondence between the patterns emerging from this mean individual effect size plots and those from the posterior probabilities as derived from the Bayesian group analysis confirmed that the observed effects were indeed stable across subjects.