Spinal signalling of C-fiber mediated pleasant touch in humans

Abstract

C-tactile afferents form a distinct channel that encodes pleasant tactile stimulation. Prevailing views indicate they project, as with other unmyelinated afferents, in lamina I-spinothalamic pathways. However, we found that spinothalamic ablation in humans, whilst profoundly impairing pain, temperature and itch, had no effect on pleasant touch perception. Only discriminative touch deficits were seen. These findings preclude privileged C-tactile-lamina I-spinothalamic projections and imply integrated hedonic and discriminative spinal processing from the body.

Keywords: C-tactile; anterolateral cordotomy; human; human biology; medicine; neuroscience; pain; spinothalamic tract; touch.

Figure 1.. Anterolateral cordotomy induces marked deficits in canonical Lamina I spinothalamic tract modalities.

Myelogram (a) and schematic (b) showing the anterolateral cordotomy procedure. Following dural puncture contrast is injected to document the position of the dentate ligament. Radiofrequency lesions are given through the cordotomy probe within the anterolateral funiculus. Dot plots showing changes in pre-cordotomy to post-cordotomy thermal detection and pain thresholds are shown in (c) and (d) respectively. Data are presented as median and interquartile range. Significant differences (Related-Samples Wilcoxon Signed Rank Test) between the pain affected and control sides are marked with asterisks and show ****p<0.0005. Abbreviations: CDT, Cold Detection Threshold; WDT, Warm Detection Threshold CPT, Cold Pain Threshold; HPT, Heat Pain Threshold.

Figure 2.. The preference for C-Tactile targeted touch and overall touch pleasantness are unaffected by anterolateral cordotomy.

(a) Raw touch pleasantness rating data for the pain-affected and control sides in the pre-cordotomy as well as post-cordotomy states. Group data for the pain affected side pre-cordotomy and post-cordotomy are shown in (b). Group data for the control side pre-cordotomy and post-cordotomy are shown in (c). Ratings of touch pleasantness are not significantly affected by anterolateral cordotomy. Dot plots of the mean individual ratings for touch pleasantness on the pain-affected side in the pre-cordotomy and post-cordotomy state are shown in (d). The lines of best fit with 95% confidence intervals are shown. The vertical dotted line indicates the position of a velocity of 1 cm s-1 on the logarithmic scale. Intercept values were defined as the value of where this 1 cm s-1 line is crossed by the line of best fit. The equations for the fitted curves, R² as well as F-test results for the pre-cordotomy and post-cordotomy states are (y = -2.07x² + 1.88x + 6.22; R² = 0.22; F_{2, 56} = 7.432, p=0.001) and (y = -1.95x² + 1.75x + 6.34; R² = 0.19; F_{2, 56} = 6.211, p=0.004) respectively. F-test results for a linear fit were not statistically significant (p=0.756 and p=0.749 for pre-cordotomy and post-cordotomy states respectively). Dot plots of individual values for β₂ and intercept pre-cordotomy and post-cordotomy states for both the pain-affected and control side are shown in (e) and (f). Group data are presented as mean + standard error mean.

Figure 3.. Anterolateral cordotomy induces a reduction in perceived touch intensity on the pain-affected side.

(a) Raw touch intensity rating data for the pain-affected and control sides in the pre-cordotomy as well as post-cordotomy states. Group touch intensity rating data for the pain affected side pre-cordotomy and post-cordotomy are shown in (b). Group data for the control side pre-cordotomy and post-cordotomy are shown in (c). Group data are presented as mean + standard error mean. Significant differences (Post-hoc analysis) between the pre-cordotomy and post-cordotomy states are marked with asterisks and show **P_s <0.01, **** P_s <0.0005.

Figure 4.. Descriptor ratings and factor scores for sensory and emotional terms in the Touch Perception Task.

Radar plots showing the mean ratings for sensory and affective descriptor terms in the pre-cordotomy (blue line) and post-cordotomy (orange line) states on the pain affected side are shown in (a). Pleasant and unpleasant touch stimulation was delivered on the forearm using fake fur and sandpaper respectively. Note that the blue and orange lines are almost superimposed for stroking with a pleasant stimulus for both emotional and sensory descriptors. In contrast both sensory and emotional descriptor ratings for an unpleasant stimulus are clearly altered by spinothalamic tract lesioning. Markedly lower mean ratings for dry, hard, prickly, rough and sharp are seen post-cordotomy. A clear divergence in the pattern of ratings is seen for emotional descriptors: ratings for negative descriptors are higher than positive descriptors in the pre-cordotomy state but the opposite pattern is seen post-cordotomy. Radar plots for descriptor ratings to stimulation with fur and sandpaper on the control side (not shown) were superimposable for respective pre-cordotomy and post-cordotomy states as well as for the equivalent material in the pre-cordotomy state on the pain affected side. The absolute change in the factor score between the pre-cordotomy and post-cordotomy states for stimulation with fur and sandpaper on the pain-affected and control sides are shown in the dot plots for sensory (b - e) and emotional (f - g) factors. Factor scores for stroking with sandpaper are significantly affected by cordotomy with evidence of a marked reduction in ratings for the texture group (b) and a more modest reduction in ratings for heat terms (d). There are small but significant increases in ratings for descriptor terms in the pile (c) and slip (e) group. Only heat (d) is significantly altered for stimulation with fur. For stroking with an unpleasant stimulus highly significant increases and decreases in emotional factor scores were seen for positive (f) and negative (g) terms respectively. These are unaffected for stroking with fur. No significant change in the emotional factor ‘arousal’ was seen (data not shown). Bars depicting median and interquartile ranges are shown. Significant differences (Related-Samples Wilcoxon Signed Rank Test) between the pain-affected and control sides are marked with asterisks and show *p<0.05, **p<0.01, ***p<0.001, ****p<0.0005. Abbreviation: SP, sandpaper.