Abstract
ObjectiveA 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.MethodsWe 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.ResultsParticipants 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.InterpretationThese 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
Highlights
We found that temperature overestimation was strong if cold and warm afferent signals were most likely located within the same spinal segment or across adjacent segments
In 4 experiments, we showed that a cardinal feature of the thermal grill illusion (TGI)—misperception of cold—is influenced by low-level integration mechanisms in the spinal cord
Overestimation of TGI stimuli was greater when cold and warm afferents were at a short distance within the spinal cord, but was drastically reduced when cold and warm afferents corresponded to nonadjacent spinal segments
Summary
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. When innocuous warm and cold stimuli are alternated on the skin, spatial summation generates a sensation that is seemingly unrelated to the constituent temperatures In this case, participants often report paradoxical heat sensations,[3,4] coupled with an intense burning pain.[5,6,7] These paradoxical heat and pain sensations are commonly known as the thermal grill illusion (TGI), and are key features of sensory integration between simultaneous cold and warm signals. A preliminary report of the results was given at the Scandinavian Association for the Study of Pain meeting.[14]
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