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Ineffectiveness of tactile gating shows cortical basis of nociceptive signaling in the Thermal Grill Illusion.

ABSTRACT: Painful burning sensations can be elicited by a spatially-alternating pattern of warm and cold stimuli applied on the skin, the so called "Thermal Grill Illusion" (TGI). Here we investigated whether the TGI percept originates spinally or centrally. Since the inhibition of nociceptive input by concomitant non-nociceptive somatosensory input has a strong spinal component, we reasoned that, if the afferent input underlying the TGI originates at spinal level, then the TGI should be inhibited by a concomitant non-nociceptive somatosensory input. Conversely, if TGI is the result of supraspinal processing, then no effect of touch on TGI would be expected. We elicited TGI sensations in a purely thermal condition without tactile input, and found no evidence that tactile input affected the TGI. These results provide further evidence against a spinal mechanism generating the afferent input producing the TGI, and indicate that the peculiar burning sensation of the TGI results from supraspinal interactions between thermoceptive and nociceptive systems.

SUBMITTER: Ferre ER

PROVIDER: S-EPMC5919908 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Ineffectiveness of tactile gating shows cortical basis of nociceptive signaling in the Thermal Grill Illusion.

Ferrè E R ER Iannetti G D GD van Dijk J A JA Haggard P P

Scientific reports 20180426 1

Painful burning sensations can be elicited by a spatially-alternating pattern of warm and cold stimuli applied on the skin, the so called "Thermal Grill Illusion" (TGI). Here we investigated whether the TGI percept originates spinally or centrally. Since the inhibition of nociceptive input by concomitant non-nociceptive somatosensory input has a strong spinal component, we reasoned that, if the afferent input underlying the TGI originates at spinal level, then the TGI should be inhibited by a co ...[more]

PMID: 29700407

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Project description: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 ?-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.

Project description:BackgroundSex-related differences in human thermal and pain sensitivity are the subject of controversial discussion. The goal of this study in a large number of subjects was to investigate sex differences in thermal and thermal pain perception and the thermal grill illusion (TGI) as a phenomenon reflecting crosstalk between the thermoreceptive and nociceptive systems. The thermal grill illusion is a sensation of strong, but not necessarily painful, heat often preceded by transient cold upon skin contact with spatially interlaced innocuous warm and cool stimuli.MethodsThe TGI was studied in a group of 78 female and 58 male undergraduate students and was evoked by placing the palm of the right hand on the thermal grill (20/40 °C interleaved stimulus). Sex-related thermal perception was investigated by a retrospective analysis of thermal detection and thermal pain threshold data that had been measured in student laboratory courses over 5 years (776 female and 476 male undergraduate students) using the method of quantitative sensory testing (QST). To analyse correlations between thermal pain sensitivity and the TGI, thermal pain threshold and the TGI were determined in a group of 20 female and 20 male undergraduate students.ResultsThe TGI was more pronounced in females than males. Females were more sensitive with respect to thermal detection and thermal pain thresholds. Independent of sex, thermal detection thresholds were dependent on the baseline temperature with a specific progression of an optimum curve for cold detection threshold versus baseline temperature. The distribution of cold pain thresholds was multi-modal and sex-dependent. The more pronounced TGI in females correlated with higher cold sensitivity and cold pain sensitivity in females than in males.ConclusionsOur finding that thermal detection threshold not only differs between the sexes but is also dependent on the baseline temperature reveals a complex processing of "cold" and "warm" inputs in thermal perception. The results of the TGI experiment support the assumption that sex differences in cold-related thermoreception are responsible for sex differences in the TGI.

Project description:AIM: The main aim of this study was to assess if the perception of thermal pain thresholds is associated with genetically inferred levels of expression of the 5-HT transporter (5-HTT). Additionally, the perception of the so-called thermal grill illusion (TGI) was assessed. Forty-four healthy individuals (27 females, 17 males) were selected a-priori based on their 5-HTTLPR/rs25531 ('tri-allelic 5-HTTLPR') genotype, with inferred high or low 5-HTT expression. Thresholds for heat- and cold-pain were determined along with the sensory and affective dimensions of the TGI. RESULTS: Thresholds to heat- and cold-pain correlated strongly (rho ?=?-0.58, p<0.001). Individuals in the low 5-HTT-expressing group were significantly less sensitive to heat-pain (p?=?0.02) and cold-pain (p?=?0.03), compared to the high-expressing group. A significant gender-by-genotype interaction also emerged for cold-pain perception (p?=?0.02); low 5-HTT-expressing females were less sensitive. The TGI was rated as significantly more unpleasant (affective-motivational dimension) than painful (sensory-discriminatory dimension), (p<0.001). Females in the low 5-HTT expressing group rated the TGI as significantly less unpleasant than high 5-HTT expressing females (p<0.05), with no such differences among men. CONCLUSION/SIGNIFICANCE: We demonstrate an association between inferred low 5-HTT expression and elevated thresholds to thermal pain in healthy non-depressed individuals. Despite the fact that reduced 5-HTT expression is a risk factor for chronic pain we found it to be related to hypoalgesia for threshold thermal pain. Low 5-HTT expression is, however, also a risk factor for depression where thermal insensitivity is often seen. Our results may thus contribute to a better understanding of the molecular underpinnings of such paradoxical hypoalgesia. The results point to a differential regulation of thermoafferent-information along the neuraxis on the basis of 5-HTT expression and gender. The TGI, suggested to rely on the central integration of thermoafferent-information, may prove a valuable tool in probing the affective-motivational dimension of these putative mechanisms.

Dataset Information

Ineffectiveness of tactile gating shows cortical basis of nociceptive signaling in the Thermal Grill Illusion.

Publications

Ineffectiveness of tactile gating shows cortical basis of nociceptive signaling in the Thermal Grill Illusion.

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