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. 2018 Sep;84(3):463-472.
doi: 10.1002/ana.25307. Epub 2018 Sep 3.

Organization of the Thermal Grill Illusion by Spinal Segments

Francesca Fardo  1   2   3 , Nanna Brix Finnerup  2 , Patrick Haggard  1
Affiliations

Organization of the Thermal Grill Illusion by Spinal Segments

Francesca Fardo et al. Ann Neurol. 2018 Sep.

Abstract

Objective: A common symptom of neuropathy is the misperception of heat and pain from cold stimuli. Similar cold allodynic sensations can be experimentally induced using the thermal grill illusion (TGI) in humans. It is currently unclear whether this interaction between thermosensory and nociceptive signals depends on spinal or supraspinal integration mechanisms. To address this issue, we developed a noninvasive protocol to assess thermosensory integration across spinal segments.

Methods: We leveraged anatomical knowledge regarding dermatomes and their spinal projections to investigate potential contributions of spinal integration to the TGI. We simultaneously stimulated a pair of skin locations on the arm or lower back using 1 cold (∼20°C) and 1 warm thermode (∼40°C). The 2 thermodes were always separated by a fixed physical distance on the skin, but elicited neural activity across a varying number of spinal segments, depending on which dermatomal boundaries the 2 stimuli spanned.

Results: Participants consistently overestimated the actual cold temperature on the skin during combined cold and warm stimulation, confirming the TGI effect. The TGI was present when cold and warm stimuli were delivered within the same dermatome, or across dermatomes corresponding to adjacent spinal segments. In striking contrast, no TGI effect was found when cold and warm stimuli projected to nonadjacent spinal segments.

Interpretation: These results demonstrate that the strength of the illusion is modulated by the segmental distance between cold and warm afferents. This suggests that both temperature perception and thermal-nociceptive interactions depend upon low-level convergence mechanisms operating within a single spinal segment and its immediate neighbors. Ann Neurol 2018;84:463-472.

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Figures

Figure 1
Figure 1
Method. We developed a quantitative approach to measure thermal grill illusion (TGI) perception elicited by cold and warm stimulation delivered by 2 thermodes on the right arm (Experiments 1–3, A–D) or on the right side of the lower back (Experiment 4, E–G). To test whether the TGI is mediated by spinal mechanisms, we varied the configuration of cold and warm stimuli to activate cold and warm afferents at distinct segmental distances. We hypothesized that the strength of the TGI illusion decreased with increased segmental distance between cold and warm afferents. (A) 8 possible locations stimulated with cold and warm thermodes within and across dermatomes on the right arm (TGI stimulation) and approximate location of the matching thermode on the left forearm (TGI matching). The distance between the 2 thermodes was ∼5cm in all conditions. This setup was used in Experiments 1 to 3. (B) Example of within‐dermatome stimulation in Experiments 1 to 3. Cold and warm spinal afferents were most likely within the same spinal segment (ie, ∼0 segments distance). (C) Example of across‐dermatomes stimulation in Experiments 1 and 2. Cold and warm afferents were most likely across 2 adjacent spinal segments (ie, ∼1 segment distance). (D) Example of across‐dermatomes stimulation in Experiments 1 to 3. Cold and warm afferents were most likely across 2 nonadjacent spinal segments (ie, ∼2–4 segments distance). (E) 9 possible locations stimulated with cold and/or warm thermodes within and across dermatomes on the right side of the lower back (TGI stimulation) and approximate location of the matching thermode on the left forearm (TGI matching). The distance between the 2 thermodes was either ∼5 or ∼10cm. This setup was used in Experiment 4. (F) Example of within‐dermatome stimulation in Experiment 4. Cold and/or warm afferents were most likely within the same spinal segment (ie, ∼0 segments distance). (G) Example of across‐dermatomes stimulation in Experiment 4. Cold and warm afferents were most likely across 2 nonadjacent spinal segments (ie, ∼2–4 segments distance). [Color figure can be viewed at http://www.annalsofneurology.org]
Figure 2
Figure 2
Results. Boxplots show the difference between judged and actual temperature at the matching tasks. (A) In Experiment 1, participants received thermal grill illusion (TGI; ie, cold–warm) stimulation and matched the overall temperature sensation from both thermodes. (B) In Experiment 2, participants received TGI (ie, cold–warm) stimulation and matched the sensation from the cold thermode. In both Experiments 1 and 2, participants systematically overestimated the overall or cold temperature across all conditions; however, in both experiments, overestimation was significantly reduced (ie, closer to the veridical temperature) when the segmental distance spanned 2 nonadjacent segments. (C, D) In Experiments 3 and 4, participants received TGI and non‐TGI stimulation consisting of 4 different temperature combinations (cold–cold, cold–warm, warm–cold, warm–warm) either on the forearm (Experiment 3, C) or on the lower back (Experiment 4, D). They matched either the cold thermode (cold–cold and cold–warm combinations) or the warm thermode (warm–cold and warm–warm combinations). In both Experiments 3 and 4, participants systematically overestimated the cold temperature; however, overestimation was larger for TGI versus non‐TGI combinations when the stimuli were applied within the same dermatome. No significant difference was found between TGI and non‐TGI combinations when the segmental distance spanned 2 nonadjacent spinal segments. Asterisks indicate statistical significance (p < 0.05) for the comparisons within vs across‐dermatomes. For simplicity, statistical significance is not depicted for comparisons across temperature combinations. [Color figure can be viewed at http://www.annalsofneurology.org]
Figure 3
Figure 3
Meta‐analytic effect size. (A) Raincloud plot of the pooled data across experiments (N = 64) for the 2 key segmental conditions: short segmental distance (∼0 spinal segments) and long segmental distance (∼2–4 spinal segments). Each single‐subject value corresponds to the difference between judged and actual temperature at the matching tasks, separately for the minimal and maximal segmental distance conditions. Positive values correspond to cold overestimation, whereas negative values correspond to cold underestimation. The half violin plots depict the probability density of the data at different values and contain 95% confidence intervals (CIs) of the mean for the 2 conditions. (B) Ninety‐five percent CIs of the difference between the 2 key segmental conditions. Positive values correspond to a larger thermal grill illusion (TGI) effect for short versus long segmental distance. The differential TGI segmental effect is plotted for each experiment (n = 16), as well as the pooled data across experiments (N = 64). [Color figure can be viewed at http://www.annalsofneurology.org]
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