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A role for wind-up in trigeminal sensory processing: intensity coding of nociceptive stimuli in the rat.
Cephalalgia. 2008 Jun; 28(6):631-9.C

Abstract

Wind-up is a progressive, frequency-dependent increase in the excitability of trigeminal and spinal dorsal horn wide dynamic range (WDR) nociceptive neurons evoked by repetitive stimulation of primary afferent nociceptive C-fibres. The correlate of wind-up in humans is temporal summation, which is an increase in pain perception to repetitive constant nociceptive stimulation. Although wind-up is widely used as a tool for studying the processing of nociceptive information, including central sensitization, its actual role is still unknown. Here, we recorded from trigeminal WDR neurons using in vivo electrophysiological techniques in rats and assessed the wind-up phenomenon in response to stimuli of different intensities and frequencies. First, we found that the amplitude of C-evoked responses of WDR neurons to repetitive stimulation increased progressively to reach a peak, then consistently showed a stable or slightly decreasing plateau phase. Only the first phase of this time course fitted in with the wind-up description. Therefore, to assess wind-up, we measured a limited number of initial responses. Second, we showed that wind-up, i.e. the slope of the frequency-dependent increase in the response to C-fibre stimulation, was linearly correlated to the stimulus intensity. Intensities of brief C-fibre inputs were thus coded into frequencies of action potentials by second-order neurons through frequency-dependent potentiation of the evoked responses. Third, wind-up also occurred at stimulation intensities below the threshold for C-evoked responses in WDR neurons, suggesting that wind-up can amplify subthreshold C-fibre inputs to WDR neurons. This might account for the observation that sparse, subliminal, neuronal activity in nociceptors can become painful via central integration of neural responses. Altogether, the present results show that wind-up can provide trigeminal WDR neurons with the capability to encode the intensity of short-duration orofacial nociceptive stimuli and to detect subthreshold nociceptive input. Thus, not only may wind-up play a physiological role in trigeminal sensory processing, but its enhancement may also underlie the pathophysiology of chronic orofacial pain conditions.

Authors+Show Affiliations

Inserm, E216, Univ Clermontl, CHU Clermont-Ferrand, Clermont-Ferrand, F-36000 France.No affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

18422721

Citation

Coste, J, et al. "A Role for Wind-up in Trigeminal Sensory Processing: Intensity Coding of Nociceptive Stimuli in the Rat." Cephalalgia : an International Journal of Headache, vol. 28, no. 6, 2008, pp. 631-9.
Coste J, Voisin DL, Luccarini P, et al. A role for wind-up in trigeminal sensory processing: intensity coding of nociceptive stimuli in the rat. Cephalalgia. 2008;28(6):631-9.
Coste, J., Voisin, D. L., Luccarini, P., & Dallel, R. (2008). A role for wind-up in trigeminal sensory processing: intensity coding of nociceptive stimuli in the rat. Cephalalgia : an International Journal of Headache, 28(6), 631-9. https://doi.org/10.1111/j.1468-2982.2008.01568.x
Coste J, et al. A Role for Wind-up in Trigeminal Sensory Processing: Intensity Coding of Nociceptive Stimuli in the Rat. Cephalalgia. 2008;28(6):631-9. PubMed PMID: 18422721.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A role for wind-up in trigeminal sensory processing: intensity coding of nociceptive stimuli in the rat. AU - Coste,J, AU - Voisin,D L, AU - Luccarini,P, AU - Dallel,R, Y1 - 2008/04/16/ PY - 2008/4/22/pubmed PY - 2008/6/5/medline PY - 2008/4/22/entrez SP - 631 EP - 9 JF - Cephalalgia : an international journal of headache JO - Cephalalgia VL - 28 IS - 6 N2 - Wind-up is a progressive, frequency-dependent increase in the excitability of trigeminal and spinal dorsal horn wide dynamic range (WDR) nociceptive neurons evoked by repetitive stimulation of primary afferent nociceptive C-fibres. The correlate of wind-up in humans is temporal summation, which is an increase in pain perception to repetitive constant nociceptive stimulation. Although wind-up is widely used as a tool for studying the processing of nociceptive information, including central sensitization, its actual role is still unknown. Here, we recorded from trigeminal WDR neurons using in vivo electrophysiological techniques in rats and assessed the wind-up phenomenon in response to stimuli of different intensities and frequencies. First, we found that the amplitude of C-evoked responses of WDR neurons to repetitive stimulation increased progressively to reach a peak, then consistently showed a stable or slightly decreasing plateau phase. Only the first phase of this time course fitted in with the wind-up description. Therefore, to assess wind-up, we measured a limited number of initial responses. Second, we showed that wind-up, i.e. the slope of the frequency-dependent increase in the response to C-fibre stimulation, was linearly correlated to the stimulus intensity. Intensities of brief C-fibre inputs were thus coded into frequencies of action potentials by second-order neurons through frequency-dependent potentiation of the evoked responses. Third, wind-up also occurred at stimulation intensities below the threshold for C-evoked responses in WDR neurons, suggesting that wind-up can amplify subthreshold C-fibre inputs to WDR neurons. This might account for the observation that sparse, subliminal, neuronal activity in nociceptors can become painful via central integration of neural responses. Altogether, the present results show that wind-up can provide trigeminal WDR neurons with the capability to encode the intensity of short-duration orofacial nociceptive stimuli and to detect subthreshold nociceptive input. Thus, not only may wind-up play a physiological role in trigeminal sensory processing, but its enhancement may also underlie the pathophysiology of chronic orofacial pain conditions. SN - 1468-2982 UR - https://www.unboundmedicine.com/medline/citation/18422721/A_role_for_wind_up_in_trigeminal_sensory_processing:_intensity_coding_of_nociceptive_stimuli_in_the_rat_ L2 - http://journals.sagepub.com/doi/full/10.1111/j.1468-2982.2008.01568.x?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -