Sensory disturbances, but not motor disturbances, induced by sensorimotor conflicts are increased in the presence of acute pain

© 2017 Brun, Gagné, McCabe and Mercier. Incongruence between our motor intention and the sensory feedback of the action (sensorimotor conflict) induces abnormalities in sensory perception in various chronic pain populations, and to a lesser extent in pain-free individuals. The aim of this study was to simultaneously investigate sensory and motor disturbances evoked by sensorimotor conflicts, as well as to assess how they are influenced by the presence of acute pain. It was hypothesized that both sensory and motor disturbances would be increased in presence of pain, which would suggest that pain makes body representations less robust. Thirty healthy participants realized cyclic asymmetric movements of flexion-extension with both upper limbs in a robotized system combined to a 2D virtual environment. The virtual environment provided a visual feedback (VF) about movements that was either congruent or incongruent, while the robotized system precisely measured motor performance (characterized by bilateral amplitude asymmetry and medio-lateral drift). Changes in sensory perception were assessed with a questionnaire after each trial. The effect of pain (induced with capsaicin) was compared to three control conditions (no somatosensory stimulation, tactile distraction and proprioceptive masking). Results showed that while both sensory and motor disturbances were induced by sensorimotor conflicts, only sensory disturbances were enhanced during pain condition comparatively to the three control conditions. This increase did not statistically differ across VF conditions (congruent or incongruent). Interestingly however, the types of sensations evoked by the conflict in the presence of pain (changes in intensity of pain or discomfort, changes in temperature or impression of a missing limb) were different than those evoked by the conflict alone (loss of control, peculiarity and the perception of having an extra limb). Finally, results showed no relationship between the amount of motor and sensory disturbances evoked in a given individual. Contrary to what was hypothesized, acute pain does not appear to make people more sensitive to the conflict itself, but rather impacts on the type and amount of sensory disturbances that they experienced in response to that conflict.Moreover, the results suggest that some sensorimotor integration processes remain intact in presence of acute pain, allowing us to maintain adaptive motor behavior

Utilisation d'une rétroaction virtuelle altérée pour évaluer les représentations du corps en présence ou en absence de douleur

Introduction: Environ 20% des adultes canadiens souffrent de douleur chronique en dépit des approches pharmacologiques disponibles. Il est donc important de développer des approches thérapeutiques complémentaires en réadaptation et de comprendre les mécanismes sous-jacents au maintien de la douleur chronique. Une des hypothèses mises en avant pour expliquer le maintien de la douleur chronique stipule que la douleur serait la conséquence d’une discordance entre les efférences motrices et la rétroaction sensorielle du mouvement (définie comme un conflit sensorimoteur), tout comme la sensation de nausée dans le mal des transports est la conséquence d’une discordance entre les informations visuelles, proprioceptives et vestibulaires. Ce conflit sensorimoteur en présence de douleur pourrait s’expliquer par une altération des représentations du corps et du contrôle moteur. Des études utilisant des conflits sensorimoteurs créés expérimentalement suggèrent que les personnes souffrant de douleur chronique sont plus sensibles à la présence de conflits (qui se traduit par une augmentation de douleur et d’autres perturbations sensorielles), ce qui pourrait contribuer à un cercle vicieux d’aggravation et de maintien de la douleur. Toutefois, la raison de cette sensibilité accrue reste encore inconnue. Ainsi, l’objectif principal de cette thèse était d’évaluer les caractéristiques cliniques et sensorimotrices expliquant une plus grande vulnérabilité au conflit sensorimoteur en présence de douleur aiguë et chronique. L’hypothèse générale était qu’une plus grande malléabilité des représentations du corps en présence de douleur explique une plus grande vulnérabilité au conflit sensorimoteur. Méthode: Les conflits sensorimoteurs ont été créés grâce à un miroir (Chapitre III, N=140 participants sains ou souffrant de fibromyalgie, syndrome de douleur régionale complexe (SDRC) ou arthrite) ou à un système robotisé de type exosquelette couplé à une interface virtuelle 2D (KINARM) (Chapitre IV, N=30 participants en santé avec ou sans douleur expérimentale; Chapitre V, N=20 participants en santé). Deux types de perturbations induites par le conflit ont été mesurées: 1) les perturbations sensorielles (mesurées par questionnaire) et 2) les perturbations motrices (déviation médio-latérale et variation d’amplitude). Le KINARM a également permis d’évaluer diverses représentations du corps chez des individus avec ou sans douleur chronique (Chapitre VI : N=26 participants en santé ou ayant un SDRC). Les variables cliniques ont été mesurées par questionnaires. Résultats: Seulement certaines perturbations sensorielles induites par le conflit sensorimoteur étaient accentuées en présence de douleur chronique (Chapitre III) et aiguë (Chapitre IV), et étaient principalement associées à l’intensité de la douleur (Chapitre III). Les autres variables cliniques (origine de la pathologie, durée de la douleur, symptômes anxieux et dépressifs) expliquaient peu la plus grande vulnérabilité au conflit sensorimoteur en présence de douleur (Chapitre III). Contrairement aux perturbations sensorielles, les perturbations motrices induites par le conflit n’étaient pas influencées par la présence de douleur aiguë (Chapitre IV). De plus, un conflit entre la vision et les efférences motrices (lors de mouvements actifs) induisait des perturbations sensorielles qui étaient plus importantes qu’un conflit entre la vision et la proprioception (mouvements passifs, Chapitre V). Enfin, la kinesthésie (sens du mouvement et de la position) était altérée chez des individus ayant un SDRC comparativement à des individus en santé, mais n’était pas reliée à la perception subjective du membre douloureux (Chapitre VI). Conclusions: La présence de douleur (aiguë ou chronique) diminue le seuil de détection du conflit sensorimoteur et contribue à maintenir une situation de conflit. Ce cercle vicieux d’aggravation de la douleur s’explique davantage par une altération de la perception du corps plutôt que par un défaut d’intégration sensorimotrice, bien que la commande motrice joue un rôle dans les perturbations sensorielles induites par le conflit. Ces résultats soutiennent la théorie des multiples représentations du corps qui suggère une dissociation entre l’image du corps et le schéma corporel. Contrairement à l’image du corps qui est altérée en présence de douleur aiguë et chronique, le schéma corporel serait perturbé seulement en présence de douleur chronique. En clinique, il serait pertinent d’évaluer et d’intervenir de manière indépendante sur l’image du corps et le schéma corporel. En recherche, il sera important d’explorer quels sont les mécanismes sous-jacents expliquant une telle dissociation.Introduction: Approximately 20% of the Canadian adults suffer from chronic pain in spite of the available pharmacological approaches. Thus, it is important to develop complementary therapeutic approaches in rehabilitation and to understand the underlying mechanisms involved in the maintenance of pain. One hypothesis that has been put forward to explain the persistence of pain postulates that pain is the consequence of a discordance between the motor efferences and the sensory feedback arising from one’s actions (defined as a sensorimotor conflict), just as the sensation of nausea in motion sickness arises from a conflict between visual, proprioceptive and vestibular information. Such sensorimotor conflicts in the presence of pain could be caused by alterations in body representations and motor control. Studies using experimental sensorimotor conflicts show that people with pain are more sensitive to the presence of conflicts (as demonstrated by an increase in painful sensations and other sensory disturbances), what could contribute to a vicious circle maintaining and aggravating pain. However, the reason why people with pain are more sensitive to sensorimotor conflicts remains unclear. Therefore, the main objective of the study was to assess the clinical and sensorimotor characteristics explaining higher sensitivity to sensorimotor conflicts in the presence of pain. The main hypothesis was that increased malleability of body representations in the presence of pain explains increased sensitivity to sensorimotor conflicts. Methods: Sensorimotor conflicts have been created using a mirror (Chapter III, N=140 participants, either healthy or with fibromyalgia, or complex regional pain syndrome (CRPS) or arthritis) or a robotic device combined with a 2D virtual reality interface (KINARM) (Chapter IV, N=30 healthy participants with or without experimental pain; Chapter V, N=20 healthy participants). Two types of disturbances were assessed: 1) sensory disturbances (measured with a questionnaire) and 2) motor disturbances (mediolateral drift and amplitude variation). The KINARM was also used to assess various body representations in participants with or without chronic pain (Chapter VI: N=26 participants, healthy or with a CRPS). Clinical outcomes were assessed with questionnaires. Results: Only some sensory disturbances induced by sensorimotor conflicts were increased in the presence of chronic (Chapter III) and acute (Chapter IV) pain, and were mainly related to pain intensity (Chapter III). The other clinical characteristics (pathology origin, duration of pain, anxious and depressive symptoms) contributed very little to the increase in sensitivity to sensorimotor conflicts in the presence of pain (Chapter III). Contrary to sensory disturbances, motor disturbances induced by sensorimotor conflicts were not influenced by the presence of acute pain (Chapter IV). Moreover, a conflict between vision and motor efferences (during active movements) induces higher sensory disturbances than a conflict between vision and proprioception (passive movements, Chapter V). Finally, kinesthesia (senses of limb position and movement) was altered in people with CRPS compared to healthy participants, but was not related to the subjective perception of the painful limb (Chapter VI). Conclusions: The presence of pain (acute or chronic) decreases the detection threshold of sensorimotor conflicts and contributes to maintain a conflict situation. This vicious circle of pain worsening is explained more by an alteration of body perception than by a perturbation in sensorimotor integration. These results support the multiple body representations theory suggesting a dissociation between the body image and the body schema. Contrary to the body image which is altered in the presence of acute and chronic pain, the body schema is altered only in the presence of chronic pain. In clinical practice, it would be relevant to assess and treat the alterations of body image and body schema separately. In research, it would be necessary to explore the underlying mechanisms of this dissociation

The contribution of motor commands to the perturbations induced by sensorimotor conflicts in fibromyalgia

Individuals with pain report higher sensory disturbances during sensorimotor conflicts compared to pain-free individuals. In the pain field, it is frequently assumed that disturbances arise from a discordance between sensory and efference copies (defined as sensory-motor conflict), while in the sensorimotor control field they are considered to result from the incongruence between sensory modalities (defined as sensory-sensory conflict). The general aim of this study was to disentangle the relative contribution of motor efferences and sensory afferences to the increased sensitivity to sensorimotor conflicts in individual with fibromyalgia (n = 20) compared to controls (n = 20). We assessed sensory and motor disturbances during sensory-sensory and sensory-motor conflicts using a robotized exoskeleton interfaced with a 2D virtual environment. There was a significant interaction between the group and the type of conflict (p = 0.03). Moreover, the increase in conflict sensitivity from sensory-sensory to sensory-motor conflicts in fibromyalgia was related to conflict-induced motor disturbances (r = 0.57; p < 0.01), but did not result from a poorer proprioception (r = 0.12; p = 0.61). Therefore, it appears that higher conflict sensitivity in fibromyalgia is mainly explained by a sensory-motor conflict rather by a sensory-sensory conflict. We suggest this arises due to a deficit in updating predicted sensory feedback rather than in selecting appropriate motor commands

Motor and sensory disturbances induced by sensorimotor conflicts during passive and active movements in healthy participants

© 2018 Brun et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Sensorimotor conflict induces both sensory and motor disturbances, but the specific factors playing a role in conflict-induced disturbances are still misunderstood. For example, we still do not know the role played by motor intention (vs. a purely visuo-proprioceptive conflict) or the influence of specific types of incongruent visual feedback. The objective of this study was threefold: 1- to compare the effect of passive and active movement during sensorimotor conflict on sensory disturbances measured with a questionnaire; 2- to compare the effect of three incongruent visual feedback conditions on sensory and motor (mediolateral drift and movement amplitude) disturbances; 3- to test whether conflict-induced sensory and motor disturbances were stable over time. 20 healthy participants realized active or passive cyclic upper limb movements while viewing either congruent or incongruent visual feedback about their movement using a robotized exoskeleton combined with 2D virtual reality interface. First, results showed that in condition of conflict, participants reported higher sensory disturbances during active movements compared to passive movements (p = 0.034), suggesting that the efference copy reinforces the conflict between vision and proprioception. Second, the three conditions of incongruence in the active condition induced similar sensory (all p>0.45) and motor disturbances (medio-lateral drift: all p>0.59 and amplitude: all p>0.25), suggesting that conflict induced motor disturbances could be related more to the observation of another movement rather than to a detection of conflict between motor intention and sensory feedback. Finally, both sensory and motor disturbances were stable over time (all ICCs between 0.76 and 0.87), demonstrating low variability within participants. Overall, our results suggest that the efference copy is more involved in sensory disturbances than in motor disturbances, suggesting that they might rely on independent processes

Exploring the Relationships Between Altered Body Perception, Limb Position Sense, and Limb Movement Sense in Complex Regional Pain Syndrome

© 2018 The Authors Chronic pain is often accompanied by patient-reported distorted body perception and an altered kinesthesia (referring to the senses of limb position and limb movement), but the association between these deficits is unknown. The objectives of this study were to assess body perception and the senses of limb position and limb movement in complex regional pain syndrome (CRPS) and to test whether these variables are related to each other and to pain intensity. Thirteen patients with upper limb CRPS (mean pain intensity, 4.2 ± 2.4 out of 10) and 13 controls were recruited. Body perception was self-reported with a questionnaire, and the senses of limb position (task 1) and of limb movement (task 2) were assessed with a robotic system combined with a 2D virtual reality display. The results showed altered kinesthesia in the patients with CRPS compared with controls (all

Virtual reality-induced sensorimotor conflict evokes limb-specific sensory disturbances in complex regional pain syndrome

Sensory disturbances are frequently observed in complex regional pain syndrome (CRPS). They are characterized by changes in the perception of limb weight and temperature, a distorted mental image of the affected limb, feeling the limb as a foreign body part, etc. However, the origin of such disturbances remains unclear. It has been hypothesized that such disturbances are due to attentional effects and/or sensorimotor integration deficits. If sensory disturbances are explained by sensorimotor integration deficits rather than by attentional factors (as hypervigilance toward pain and pain-related sensations), they would be expected to be specific in terms of the type of sensation evoked and in terms of localization.Objectives: The first objective was to test whether sensory disturbances evoked by a unilateral sensorimotor conflict are specific to the painful limb and differ according to the type of sensory disturbances in individuals with a unilateral CRPS compared to healthy controls (HC). The second objective was to assess the association between clinical characteristics and sensory disturbances evoked by a unilateral sensorimotor conflict. The third objective was to assess motor disturbances induced by a unilateral sensorimotor conflict.Methods: Ten adults with upper limb (UL) CRPS and 23 HC were recruited. Sensorimotor conflict was elicited with a KINARM robotized exoskeleton interfaced with a 2D virtual environment allowing the projection of a virtual UL that was moving in either a congruent or incongruent manner relative to the actual UL movement. Participants were required to rate the sensory disturbances evoked from 0 (no change) to 3 (high change) on a questionnaire (8 items). According to a previous study, items were categorized in two Types (Type 1: pain, discomfort, the feeling of losing a limb, change in weight and temperature; Type 2: feelings of peculiarity, the impression of gaining a limb and losing control). Motor disturbances were quantified as mediolateral drift and changes in amplitude of UL movement. Recorded clinical characteristics included the intensity and duration of pain, proprioception deficits, and body perception disturbances.Results and conclusion: CRPS participants report higher Type 1 than Type 2 disturbances for the Affected limb (while the reverse was observed for HC and for the Unaffected limb). In addition, no difference was observed between the Unaffected limb in CRPS and the Dominant limb in HC for Type 2 disturbances, while higher conflict sensitivity was observed for Type 1 disturbances. Conflict sensitivity was related to higher pain (but not to other clinical characteristics) only for Type 1 disturbances in the Affected limb. Finally, no difference in motor disturbances was observed between CRPS and HC. While this does not completely rule out the attentional hypothesis, these results are in line with the hypothesis that sensory disturbances in CRPS are due to deficits in sensorimotor integration

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The kinaesthetic mirror illusion: How much does the mirror matter?

International audienceThe reflection of a moving hand in a mirror positioned in the sagittal plane can create an illusion of symmetrical, bimanual movement. This illusion is implicitly presumed to be of visual origin. However, muscle proprioceptive afferents of the arm reflected in the mirror might also affect the perceived position and movement of the other arm. We characterized the relative contributions of visual and proprioceptive cues by performing two experiments. In Experiment 1, we sought to establish whether kinaesthetic illusions induced using the mirror paradigm would survive marked visual impoverishment (obtained by covering between 0% and 100% of the mirror in 16% steps). We found that the mirror illusion was only significantly influenced when the visual degradation was 84% or more. In Experiment 2, we masked the muscle proprioceptive afferents of the arm reflected in the mirror by co-vibrating antagonistic muscles. We found that masking the proprioceptive afferents reduced the velocity of the illusory displacement of the other arm. These results confirm that the mirror illusion is not a purely visual illusion but emerges from a combination of congruent signals from the two arms, i.e. visual afferents from the virtually moving arm and proprioceptive afferents from the contralateral, moving arm

Impact of Experimental Tonic Pain on Corrective Motor Responses to Mechanical Perturbations

Movement is altered by pain, but the underlying mechanisms remain unclear. Assessing corrective muscle responses following mechanical perturbations can help clarify these underlying mechanisms, as these responses involve spinal (short-latency response, 20-50 ms), transcortical (long-latency response, 50-100 ms), and cortical (early voluntary response, 100-150 ms) mechanisms. Pairing mechanical (proprioceptive) perturbations with different conditions of visual feedback can also offer insight into how pain impacts on sensorimotor integration. The general aim of this study was to examine the impact of experimental tonic pain on corrective muscle responses evoked by mechanical and/or visual perturbations in healthy adults. Two sessions (Pain (induced with capsaicin) and No pain) were performed using a robotic exoskeleton combined with a 2D virtual environment. Participants were instructed to maintain their index in a target despite the application of perturbations under four conditions of sensory feedback: (1) proprioceptive only, (2) visuoproprioceptive congruent, (3) visuoproprioceptive incongruent, and (4) visual only. Perturbations were induced in either flexion or extension, with an amplitude of 2 or 3 Nm. Surface electromyography was recorded from Biceps and Triceps muscles. Results demonstrated no significant effect of the type of sensory feedback on corrective muscle responses, no matter whether pain was present or not. When looking at the effect of pain on corrective responses across muscles, a significant interaction was found, but for the early voluntary responses only. These results suggest that the effect of cutaneous tonic pain on motor control arises mainly at the cortical (rather than spinal) level and that proprioception dominates vision for responses to perturbations, even in the presence of pain. The observation of a muscle-specific modulation using a cutaneous pain model highlights the fact that the impacts of pain on the motor system are not only driven by the need to unload structures from which the nociceptive signal is arising

Do nociceptive stimulation intensity and temporal predictability influence pain-induced corticospinal excitability modulation?

International audienceTemporal predictability and intensity of an impending nociceptive input both shape pain experience and modulate laser-evoked potentials (LEPs) amplitude. However, it remains unclear whether and how these two factors could influence pain-induced corticospinal excitability modulation. The current study investigated the influence of nociceptive stimulation intensity and temporal predictability on motor-evoked potentials (MEPs) modulation, in parallel to their effect on pain perception and LEPs amplitude. Twenty participants completed electroencephalographic and transcranial magnetic stimulation experiments during which two laser nociceptive stimulation intensities (high and low) were either unpredictably delivered (random delay) or preceded by a fixed-timing cue (fixed delay). The amplitude of the conditioned MEPs was significantly reduced only for the high nociceptive stimulation and was not affected by the temporal predictability of pain (despite the fact that temporal predictability modulated the amplitude of P2 LEP component amplitude). However, a posteriori analyses based on patterns of pain-induced MEPs modulation revealed that participants in which nociceptive stimulation resulted in an increase in corticospinal excitability were more affected by the predictability of pain (i.e. increasing corticospinal excitability even more when pain occurrence was predictable), regardless of the nociceptive stimulation intensity; whereas participants in which nociceptive stimulation resulted in a decrease in corticospinal excitability were sensitive to the intensity of the stimulation but not its predictability. These results suggest a potential influence of cognitive factors such as temporal predictability on the response of the motor system in the presence of pain for some participants, contributing to explain, at least in part, the high variability highlighted in a number of previous studies