Modulation of Spinal Nociceptive Excitability by Nociceptive-Visual Interaction

Pain, besides its contribution to body homeostasis, has also the function of providing information on external stimuli that can potentially harm the body. Such exteroceptive function relies on an optimally integrated multisensory representation of the body and its surrounding space, which is based on the interaction between somatic and extra-somatic stimuli occurring near the body. While the existence of such interactions between nociceptive and visual stimuli has recently been demonstrated, showing that visual stimuli outside the body can impact the perception of nociceptive stimuli and vice versa, their functional role is not clear yet. It is indeed hypothesized that one of the functions of such multisensory representations would be to optimize defensive reactions against threatening stimuli. However, the idea of this potential defensive purpose has, to date, mainly been based on a set of studies conducted in non-human primates. The aim of the present study was to investigate whether interactions between nociceptive and external visual stimuli can shape motor reactions of the stimulated limb. More specifically, we tested in 24 participants whether spinal nociceptive excitability, as measured by the spinal nociceptive withdrawal reflex (NWR) in response to noxious stimuli, can be modulated by external visual stimuli, specifically those approaching the body part on which the nociceptive stimuli are applied. NWRs were elicited by applying transcutaneous electrical stimuli in the sole of the foot of the participants. Depending on the condition, the electrical stimulus was either preceded by a dynamic visual stimulus rapidly approaching a location near the stimulated foot (NWR-visual near condition), a dynamic visual stimulus approaching a location further away from the stimulated foot (NWR-visual far condition), or was applied without any dynamic visual stimulus (NWR only condition). The electrical stimulation could be applied at one out of two possible time points of the trial, so that the NWR was either induced when the visual stimulus was perceived as still moving (early time point condition) or when it arrived at its endpoint (late time point condition). Furthermore, to avoid that the visual stimulus solely acted as a cue predicting the occurrence of the electrical stimulus, control conditions in which the dynamic visual stimuli (near or far) were presented without an electrical stimulus were also added. Trials of the different conditions were presented randomly and after each trial the participants rated the intensity of the electrical stimulus on a numerical rating scale (NRS) ranging from 0 to 10, anchored as 0: perception threshold, 5: pain threshold, 10: maximum imaginable pain. NWRs were obtained by recording the electromyographic responses in the tibialis anterior muscle of the leg and NWR size was quantified by the root-mean-square (RMS) amplitude in the 60- to 180-ms poststimulus window. For each participant, NWR amplitude and NRS rating change (in %) with regard to NWR amplitude and NRS rating in the NWR only condition (baseline) were calculated. One-sample Wilcoxon signed rank tests (to 0) were performed for all conditions to test for the presence of significant changes in NWR amplitude and NRS rating with regard to baseline and the different conditions were compared with a repeated measures ANOVA with visual condition (2) and time point (2) as within participant factors. Results show that there was a significant increase in NWR size in the NWR-visual near condition for both time points (early: M=33.5%, SD: 42.2%; late: M=30.5%, SD= 56.4%) with regard to the NWR only condition. In the NWR-visual far condition, NWR size was significantly increased for the early time point (M=30.4%, SD= 61.4%), but not for the late time point (M=22.7%, SD= 49.9%). The different conditions were not significantly different from each other. There was no significant change in NRS ratings with regard to the NWR only condition for both NWR-visual near and NWR-visual far conditions, and the different conditions were not significantly different from each other. These results suggest that spinal nociceptive excitability can be modulated by the presence of dynamic visual stimuli. Whether this modulatory effect on the spinal nociceptive reflex system is more important for near vs. far visual stimuli could however not be clearly established, and might depend on a more complex time-dependent interplay between the nociceptive and visual stimulation. This finding corroborates previous research that demonstrated supraspinal descending modulation of the NWR, for example by cognitive and emotional states, but also adds to the current literature by showing that NWR amplitude can already be modulated by external visual stimuli without any explicit emotional or task-related valence, possibly through the existence of a multisensory representation of the body and its surrounding visual space.