Organization of the Thermal Grill Illusion by Spinal Segments

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.