Evidence for Thalamic Involvement in the Thermal Grill Illusion: An fMRI Study

Abstract

BackgroundPerceptual illusions play an important role in untangling neural mechanisms underlying conscious phenomena. The thermal grill illusion (TGI) has been suggested as a promising model for exploring percepts involved in neuropathic pain, such as cold-allodynia (pain arising from contact with innocuous cold). The TGI is an unpleasant/painful sensation from touching juxtapositioned bars of cold and warm innocuous temperatures.AimTo develop an MRI-compatible TGI-unit and explore the supraspinal correlates of the illusion, using fMRI, in a group of healthy volunteers.MethodsWe constructed a TGI-thermode allowing the rapid presentation of warm(41°C), cold(18°C) and interleaved(41°C+18°C = TGI) temperatures in an fMRI-environment. Twenty volunteers were tested. The affective-motivational (“unpleasantness”) and sensory-disciminatory (“pain-intensity”) dimensions of each respective stimulus were rated. Functional images were analyzed at a corrected α-level <0.05.ResultsThe TGI was rated as significantly more unpleasant and painful than stimulation with each of its constituent temperatures. Also, the TGI was rated as significantly more unpleasant than painful. Thermal stimulation versus neutral baseline revealed bilateral activations of the anterior insulae and fronto-parietal regions. Unlike its constituent temperatures the TGI displayed a strong activation of the right (contralateral) thalamus. Exploratory contrasts at a slightly more liberal threshold-level also revealed a TGI-activation of the right mid/anterior insula, correlating with ratings of unpleasantness(rho = 0.31).Conclusion/SignificanceTo the best of our knowledge, this is the first fMRI-study of the TGI. The activation of the anterior insula is consistent with this region's putative role in processing of homeostatically relevant feeling-states. Our results constitute the first neurophysiologic evidence of thalamic involvement in the TGI. Similar thalamic activity has previously been observed during evoked cold-allodynia in patients with central neuropathic pain. Our results further the understanding of the supraspinal correlates of the TGI-phenomenon and pave the way for future inquiries into if and how it may relate to neuropathic pain.

Reduced Response to the Thermal Grill Illusion in Chronic Pain Patients

“…Although the largest pain response to the TGI was reported when the thermal grill configuration was 18°C/42°C, the thermal grill did not produce a very painful stimulus in pain‐free participants (median 2 on an 11‐point NRS, interquartile range 1 to 5), being below 4 (out of 10), which is generally accepted as the minimum for clinically relevant pain [55]. The reported pain intensity in our study is similar to previous studies investigating the TGI in pain‐free participants, where similar thermal grill configurations produced pain intensity ratings between 7 mm and 47 mm on a 100‐mm VAS [6,8–11,15,16,18,20,21]. Instead, the thermal grill produced an altered sensory experience in our study that manifested as an aversive heat stimulus (approx.…”

Neurophysiology of Skin Thermal Sensations

“…Along with recent advances in neuroimaging techniques, which have allowed the investigation of the cortical projections of third order thermo-sensory neurons, these studies have provided novel insights on the central processing sub-serving conscious thermal sensation in humans (60,62,68,78,80,92,198,213,251).…”

Ionic mechanisms of spinal neuronal cold hypersensitivity in ciguatera

“…Although not directly related to this study, perceptually the A‐fibre nerve block, thermal grill and menthol‐induced hyperalgesia model all evoke sensations of paradoxical burning during cooling (Wahren et al ., ; Craig & Bushnell, ; Binder et al ., ), and functional magnetic resonance imaging analysis also reveals various degrees of activation within the lateral and medial thalamic nuclei in these models (Binder et al ., ; Lindstedt et al ., ). Similarly, in post‐stroke patients, damage to a cool‐signalling lateral thalamic pathway that causes a disinhibition of a medial thalamic nociceptive channel has been proposed to underlie observed burning cold, ongoing pain and cold allodynia in these patients (Greenspan et al ., ).…”