Noxious mechanical heterotopic stimulation induces inhibition of the spinal dorsal horn neuronal network: analysis of spinal somatosensory-evoked potentials

Abstract

Most of the endogenous pain modulation (EPM) involves the spinal dorsal horn (SDH). EPM including diffuse noxious inhibitory controls have been extensively described in oligoneuronal electrophysiological recordings but less attention had been paid to responses of the SDH neuronal population to heterotopic noxious stimulation (HNS). Spinal somatosensory-evoked potentials (SEP) offer the possibility to evaluate the neuronal network behavior, reflecting the incoming afferent volleys along the entry root, SDH interneuron activities and the primary afferent depolarization. SEP from de lumbar cord dorsum were evaluated during mechanical heterotopic noxious stimuli. Sprague-Dawley rats (n = 12) were Laminectomized (T10-L3). The sural nerve of the left hind paw was electrically stimulated (5 mA, 0.5 ms, 0.05 Hz) to induce lumbar SEP. The HNS (mechanic clamp) was applied sequentially to the tail, right hind paw, right forepaw, muzzle and left forepaw during sural stimulation. N wave amplitude decreases (-16.6 %) compared to control conditions when HNS was applied to all areas of stimulation. This effect was more intense for muzzle stimulation (-23.5 %). N wave duration also decreased by -23.6 %. HNS did not change neither the amplitude nor the duration of the P wave but dramatically increases the dispersion of these two parameters. The results of the present study strongly suggest that a HNS applied to different parts of the body is able to reduce the integrated electrical response of the SDH, suggesting that not only wide dynamic range neurons but many others in the SDH are modulated by the EPM.

Thermo-dependence of noxious mechanical heterotopic stimulation-dependent modulation of the spinal dorsal horn response to somatosensory stimulation

“…In agreement with a recent report [11], HNS applied to different body sites activated endogenous pain modulation systems that then exerted an inhibitory effect by reducing N-wave amplitude and du-ration. This process showed an inverse thermo-dependence, i.e.…”

“…The DNIC system has a whole body receptive field [20,21], but not every body site activates the DNIC system with the same intensity [11]. The present report goes further by describing that muzzle and tail were body sites with significantly higher and lower thermo-dependency, respectively, than hind-and fore-paws during HNS.…”

“…Tissue differences of sensory receptor density at these body areas, i.e. intense trigeminal skin innervation of the muzzle [11,20], trigeminal bilateral brainstem inputs and poly-synaptic connections between trigeminal caudal nuclei and SRD, the main supraspinal structure involved in DNIC [11,20], should be considered to explain a more intense response for muzzle HNS. Reduction of the inhibition of N-wave induced by HNS in the tail was lower than that of other body sites, presumably due to its lower temperature changes, as the location is more environmentally dependent because of its greater distance from the body core.…”

“…Thereafter, maintaining sural nerve stimulation, HNS was applied for five minutes sequentially in the tail, right hind paw, right forepaw, muzzle, and left forepaw, with five minutes of CC recording after each HNS application. This duration has been reported sufficient for recovery of basal activity in SDH neurons [4,11]. The HNS body site sequence was applied randomly clockwise or anticlockwise to every subject for each temperature (34; 37 and 40 • C), which was also randomly increased or decreased prior to each application.…”

“…The N-wave is followed by a positive wave (P-wave), the result of a complex process of SDH activation induced by descending pathways from supraspinal structures which primary consist of a combination of afferent depolarization and local neuronal network interactions [7,8]. Recent experimental evidence supports the proposition that a large and heterogeneous cell population, which includes excitatory and inhibitory neurons but also different sensory neurons and primary afferents within the SDH, could be modulated by a heterotopic noxious stimulus (HNS) applied distal to a spinal segment [11].…”