The encoding of the thermal grill illusion in the human spinal cord

Abstract

Abstract Aims The spatial alternation of innocuous cold and warm stimuli on the skin can paradoxically provoke a hot, burning sensation, known as the thermal-grill illusion (TGI). Whether the TGI depends on spinal or supraspinal integration mechanisms is still debated. To assess whether the TGI can be accounted by integration of cold and warm afferent signals in the spinal cord, we leveraged anatomical knowledge on the spatial arrangement of dermatomes and spinal segmental projections. Methods We stimulated a series of skin locations on the right arm using one cold (∼20 °C) and one warm thermode (∼40°C). The two stimulus locations had identical physical distance on the skin. However, the distance between the cold and heat projection signals in the spinal cord varied across three conditions. Cold and warm inputs were delivered (1) within the same dermatome (e.g., C5–C5); (2) across the dermatome boundary of two adjacent spinal segments (e.g., C5–C6); (3) across the dermatome boundary of two non-adjacent spinal segments (e.g., C5–T1). In two experiments, we obtained an estimate of the strength of the TGI by asking 32 healthy participants to complete a temperature matching task. Results Participants overestimated the actual average temperature of the two thermodes (Exp. 1) and the cold temperature of one of the two thermodes (Exp. 2). However, this effect was significantly larger when cold and heat stimuli were delivered within the same dermatome (+6.57 ± 3.99°C and +9.88 ± 5.60 °C) or between dermatomes projecting to adjacent spinal segments (+6.26 ±4.44°C and +9.48 ± 5.83 °C), compared to when cold and heat stimuli projected to non-adjacent spinal segments (+3.46 ± 4.46 °C and +4.80 ± 3.21 °C). Conclusions These results demonstrate that the strength of the illusion is modulated by the segmental distance between cold and heat spinal signals, and show that the perceived quality and intensity of thermal stimuli depends upon low-level spatial summation mechanisms in the spinal cord.