Organization of the Thermal Grill Illusion by Spinal Segments

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

Beyond labeled lines: A population coding account of the thermal grill illusion

“…When pain is experienced, its intensity is typically mild to moderate (Bouhassira et al, 2005a;Craig and Bushnell, 1994;Leung et al, 2005). However, similar heat and painful percepts can be elicited using different experimental apparatuses, such as alternating cold and warm spiral tubes (Bach et al, 2011;Thunberg, 1896), warm-cold-warm patterns using three thermodes (Kammers et al, 2010;Marotta et al, 2015), or one single cold and one single warm thermode, even at large distances on the skin (Defrin et al, 2008;Fardo et al, 2018). Overall these experiments suggest that the TGI depends primarily upon the spatial pattern of thermal stimulation, while other factors such as the size of the affected area, the number of stimulated afferents, or the distances between component stimuli exert minor influences on the quality and intensity of the illusion (Li et al, 2009).…”

“…Thus, although the generation of TGI percepts is conserved across a variety of spatial configurations, the difference between the cold and warm components does exert a large influence on the perceived thermo-nociceptive quality and intensity of the illusion. TGI phenomena have been investigated using qualitative reports -for example by requiring participants to select from a variety of descriptors relating to the subjective qualities of temperature and pain (e.g., Li et al 2009;Bach et al 2011) -as well as quantitative approaches, such as verbal numerical scales (Scheuren et al, 2014), visual analogue scales (Adam et al, 2014;Craig and Bushnell, 1994;Kern et al, 2008aKern et al, , 2008bLeung et al, 2005) or temperature matching (Fardo et al, 2018;Ferrè et al, 2018;Kammers et al, 2010;Leung et al, 2005;Marotta et al, 2015). From this variety of qualitative and quantitative measures, it emerged that TGI sensations vary from innocuous to painful heat percepts, and can be felt as an intermediate sensation between innocuous and noxious perception (Bach et al, 2011).…”

“…As such, the debate has focused on the distinction between supraspinal (thalamus or cortex; Craig and Bushnell 1994) and spinal mechanisms (Bouhassira et al, 2005;Green, 2002). However, experimental data do not support this categorical approach, and indicate that we cannot exclude either spinal (Fardo et al, 2018;Harper and Hollins, 2017) or supraspinal contributions (Ferrè et al, 2018;Lindstedt et al, 2011;Marotta et al, 2015) as contributing to the TGI phenomenon. In the next paragraphs, we will review the two main TGI theories and their assumptions in more detail.…”

The Arm’s Blind Line: Anisotropic Distortion in Perceived Orientation of Stimuli on the Arm

“…Though a previous study reported a minor effect of dermatomes during intensity discrimination task on the arm [9], the orientation (spatial relationship) might be calculated differently depending on whether the stimuli are presented within or across dermatomes. It seems that our inwardly and outwardly inclined stimuli were presented to the same degree over two dermatomes (C6 and T1) [10]; however, roll rotation of the arm actually non-uniformly stretches and rotates skin, and this uniformity remains unclear. In addition, the differences in cortical representation of each skin area (i.e., cortical magnification) may be related to the observed distortion on the arm, since the correlation with acuity of shape perception on the finger has been reported [11].…”

Thermonociceptive interaction: interchannel pain modulation occurs before intrachannel convergence of warmth

“…Therefore, further studies could address whether thermo -nociceptive interactions also occur on a larger scale and on both glabrous and hairy skin. Given the different innervation territories and segmental projections of the median and ulnar nerves, one may expect that warmth delivered on the index vs the ring finger might show different interactions with pain delivered on the middle finger (Fardo et al 2018). However, while this hypothesis would predict a significant difference in pain ratings and/or LEPs between our condition 2 (warmth on the index finger) and condition 4 (warmth on the ring finger), we found no evidence for any difference in sensory ratings or LEPs (p > 0.200 in all cases).…”