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. 2016 May 25;36(21):5850-60.
doi: 10.1523/JNEUROSCI.1130-15.2016.

Encoding of Touch Intensity But Not Pleasantness in Human Primary Somatosensory Cortex

Laura K Case  1 , Claire M Laubacher  2 , Håkan Olausson  3 , Binquan Wang  2 , Primavera A Spagnolo  4 , M Catherine Bushnell  2
Affiliations

Encoding of Touch Intensity But Not Pleasantness in Human Primary Somatosensory Cortex

Laura K Case et al. J Neurosci. .

Abstract

Growing interest in affective touch has delineated a neural network that bypasses primary somatosensory cortex (S1). Several recent studies, however, have cast doubt on the segregation of touch discrimination and affect, suggesting that S1 also encodes affective qualities. We used functional magnetic resonance imaging (fMRI) and repetitive transcranial magnetic stimulation (rTMS) to examine the role of S1 in processing touch intensity and pleasantness. Twenty-six healthy human adults rated brushing on the hand during fMRI. Intensity ratings significantly predicted activation in S1, whereas pleasantness ratings predicted activation only in the anterior cingulate cortex. Nineteen subjects also received inhibitory rTMS over right hemisphere S1 and the vertex (control). After S1 rTMS, but not after vertex rTMS, sensory discrimination was reduced and subjects with reduced sensory discrimination rated touch as more intense. In contrast, rTMS did not alter ratings of touch pleasantness. Our findings support divergent neural processing of touch intensity and pleasantness, with affective touch encoded outside of S1.

Significance statement: Growing interest in affective touch has identified a neural network that bypasses primary somatosensory cortex (S1). Several recent studies, however, cast doubt on the separation of touch discrimination and affect. We used functional magnetic resonance imaging and repetitive transcranial magnetic stimulation to demonstrate the representation of touch discrimination and intensity in S1, but the representation of pleasantness in the anterior cingulate cortex, not S1. Our findings support divergent neural processing of touch intensity and pleasantness, with affective touch encoded outside of S1. Our study contributes to growing delineation of the affective touch system, a crucial step in understanding its dysregulation in numerous clinical conditions such as autism, eating disorders, depression, and chronic pain.

Keywords: affect; c-tactile fibers; pleasantness; rTMS; somatosensory cortex; touch discrimination.

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Figures

Figure 1.
Figure 1.
fMRI design. Brushing stimuli were delivered during two runs: one brushing the palm and one brushing the back of the hand. Each run contained 4 blocks: 2 fast brushing blocks (30 cm/s) and 2 slow brushing blocks (3 cm/s). Each block had 8 6 s periods of brushing with rest periods jittered around 15 s. Each block was followed by a 16 s rating period: 8 s for rating intensity and 8 s for rating pleasantness. The order of the two runs was counterbalanced across subjects and the order of the four blocks was randomized within each run.
Figure 2.
Figure 2.
rTMS target placement. Each point represents an individual subject's right hemisphere primary somatosensory cortex S1 target (red) transformed into MNI space. The S1 target was individually selected based on the peak of the subject's Z-statistic map of brushing > rest. The coil was aligned in the posterior-anterior direction at ∼45° to the right of midline in the S1 condition. In the vertex condition, the coil was placed directly above the interhemispheric fissure in the same coronal plane as individual subject's S1 target. The coil was aligned in the posterior-anterior direction at 0° to the midline. Each target is displayed at the section representing the group average y-coordinate (coronal) in MNI space.
Figure 3.
Figure 3.
Slow > fast brushing. The contrast of BOLD response to slow > fast brushing was thresholded at Z > 3 with whole-brain correction for multiple comparisons at the cluster level (p < 0.01). A, On the back of the hand, the left ACC, left motor cortex, and right somatosensory cortex had a greater response to slow than fast brushing. B, No regions showed a significantly greater response to slow than fast brushing on the palm. x, y, and z are MNI coordinates corresponding to the left–right, anterior–posterior, and inferior–superior axes, respectively; R = L.
Figure 4.
Figure 4.
Brushing ratings. During the fMRI task, slow (3 cm/s) and fast brushing (30 cm/s) stimuli were delivered to the palm and back of the left hand. Each block of 8 stimuli was rated on a visual analog scale for intensity (0 = “no sensation”; 100 = “the most intense sensation imaginable”) and for pleasantness (0 = “the most unpleasant imaginable”; 100 = “the most pleasant imaginable”). Error bars indicate ± SEM.
Figure 5.
Figure 5.
Whole-brain positive correlates of intensity and pleasantness. BOLD activation predicted by intensity and pleasantness ratings were thresholded at Z > 3 with whole-brain correction for multiple comparisons at the cluster level (p < 0.01). A, Intensity ratings collected during the fMRI brushing task significantly predicted BOLD response in right S1, right posterior insula, and bilateral S2. B, Pleasantness ratings significantly predicted BOLD response in the ACC. x, y, and z refer to the MNI coordinates corresponding to the left–right, anterior–posterior, and inferior–superior axes, respectively; R = L.
Figure 6.
Figure 6.
Effect of rTMS on 2PD accuracy. Participants were tested on 2PD before and after 20 min of inhibitory 1 Hz rTMS on 2 separate days. During the active session, rTMS was directed to S1 and, during the control session, rTMS was directed to the vertex. The 2PD task was administered as 2 descending series of blocks at tip distances of 2–10 mm (see Materials and Methods for details). Each block contained 5 trials of 2-point stimulation and 5 trials of 1-point stimulation. 2PD accuracy was reduced significantly more after rTMS to S1 than after rTMS to the vertex. In addition, there was a marginally significant interaction between rTMS session and distance. Post hoc tests showed that 2PD accuracy was significantly reduced after rTMS to S1 at the smallest distance tested. S1 before, M = 58.1, SD = 11.1; S1 after, M = 50.8, SD = 9.7; vertex before, M = 56.3, SD = 9.4; vertex after, M = 58.6, SD = 9.2. *One-tailed p < 0.05. Error bars indicate ± SEM.
Figure 7.
Figure 7.
Perception of intensity and pleasantness after S1 rTMS. A, Subjects rated the intensity and pleasantness of fast and slow brushing on the palm and back of the hand before and after 20 min of 1 Hz rTMS. The subjects who showed a drop in 2PD performance after rTMS to S1 (n = 14) also showed an increase in intensity ratings but not in pleasantness ratings (averaged across brushing types) after rTMS to S1. Five subjects who did not show a drop in 2PD accuracy are not included in graph. *Single-sample t test, p < 0.05. Error bars indicate ± SEM. Intensity: S1 before, M = 41.9, SD = 26.0; S1 after, M = 46.1, SD = 27.5; vertex before, M = 45.6, SD = 23.2; vertex after, M = 43.4, SD = 24.7; pleasantness: S1 before, M = 64.6, SD = 14.7; S1 after, M = 65.9, SD = 15.9; vertex before, M = 64.5, SD = 15.2; vertex after, M = 64.3, SD = 15.3. B, Changes in 2PD accuracy from before to after rTMS significantly predicted changes in ratings of brushing intensity.
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