When proprioceptive feedback enhances visual perception of self-body movement: rehabilitation perspectives.

Introduction: Rehabilitation approaches take advantage of vision's important role in kinesthesia, using the mirror paradigm as a means to reduce phantom limb pain or to promote recovery from hemiparesis. Notably, it is currently applied to provide a visual reafferentation of the missing limb to relieve amputees' pain. However, the efficiency of this method is still debated, possibly due to the absence of concomitant coherent proprioceptive feedback. We know that combining congruent visuo-proprioceptive signals at the hand level enhances movement perception in healthy people. However, much less is known about lower limbs, for which actions are far less visually controlled in everyday life than upper limbs. Therefore, the present study aimed to explore, with the mirror paradigm, the benefit of combined visuo-proprioceptive feedback from the lower limbs of healthy participants. Methods: We compared the movement illusions driven by visual or proprioceptive afferents and tested the extent to which adding proprioceptive input to the visual reflection of the leg improved the resulting movement illusion. To this end, 23 healthy adults were exposed to mirror or proprioceptive stimulation and concomitant visuo-proprioceptive stimulation. In the visual conditions, participants were asked to voluntarily move their left leg in extension and look at its reflection in the mirror. In the proprioceptive conditions, a mechanical vibration was applied to the hamstring muscle of the leg hidden behind the mirror to simulate an extension of the leg, either exclusively or concomitantly, to the visual reflection of the leg in the mirror. Results: (i) Visual stimulation evoked leg movement illusions but with a lower velocity than the actual movement reflection on the mirror; (ii) proprioceptive stimulation alone provided more salient illusions than the mirror illusion; and (iii) adding a congruent proprioceptive stimulation improved the saliency, amplitude, and velocity of the illusion. Conclusion: The present findings confirm that visuo-proprioceptive integration occurs efficiently when the mirror paradigm is coupled with mechanical vibration at the lower limbs, thus providing promising new perspectives for rehabilitation.

Investigating the human spinal sensorimotor pathways through functional magnetic resonance imaging.

Most of our knowledge about the human spinal ascending (sensory) and descending (motor) pathways comes from non-invasive electrophysiological investigations. However, recent methodological advances in acquisition and analyses of functional magnetic resonance imaging (fMRI) data from the spinal cord, either alone or in combination with the brain, have allowed us to gain further insights into the organization of this structure. In the current review, we conducted a systematic search to produced somatotopic maps of the spinal fMRI activity observed through different somatosensory, motor and resting-state paradigms. By cross-referencing these human neuroimaging findings with knowledge acquired through neurophysiological recordings, our review demonstrates that spinal fMRI is a powerful tool for exploring, in vivo, the human spinal cord pathways. We report strong cross-validation between task-related and resting-state fMRI in accordance with well-known hemicord, postero-anterior and rostro-caudal organization of these pathways. We also highlight the specific advantages of using spinal fMRI in clinical settings to characterize better spinal-related impairments, predict disease progression, and guide the implementation of therapeutic interventions.

The impact of movement sonification on haptic perception changes with aging.

Combining multisensory sources is crucial to interact with our environment, especially for older people who are facing sensory declines. Here, we examined the influence of textured sounds on haptic exploration of artificial textures in healthy younger and older adults by combining a tactile device (ultrasonic display) with synthetized textured sounds. Participants had to discriminate simulated textures with their right index while they were distracted by three disturbing, more or less textured sounds. These sounds were presented as a real-time auditory feedback based on finger movement sonification and thus gave the sensation that the sounds were produced by the haptic exploration. Finger movement velocity increased across both groups in presence of textured sounds (Rubbing or Squeaking) compared to a non-textured (Neutral) sound. While young adults had the same discrimination threshold, regardless of the sound added, the older adults were more disturbed by the presence of the textured sounds with respect to the Neutral sound. Overall, these findings suggest that irrelevant auditory information was taken into account by all participants, but was appropriately segregated from tactile information by young adults. Older adults failed to segregate auditory information, supporting the hypothesis of general facilitation of multisensory integration with aging.

Functional properties of extended body representations in the context of kinesthesia.

A person's internal representation of his/her body is not fixed. It can be substantially modified by neurological injuries and can also be extended (in healthy participants) to incorporate objects that have a corporeal appearance (such as fake body segments, e.g. a rubber hand), virtual whole bodies (e.g. avatars), and even objects that do not have a corporeal appearance (e.g. tools). Here, we report data from patients and healthy participants that emphasize the flexible nature of body representation and question the extent to which incorporated objects have the same functional properties as biological body parts. Our data shed new light by highlighting the involvement of visual motion information from incorporated objects (rubber hands, full body avatars and hand-held tools) in the perception of one's own movement (kinesthesia). On the basis of these findings, we argue that incorporated objects can be treated as body parts, especially when kinesthesia is involved.

The aging brain: A set of functional MRI data acquired at rest and during exposure to tactile or muscle proprioceptive stimulation in healthy young and older volunteers.

There is a growing interest in understanding functional brain decline with aging. The dataset provides raw anatomical and functional images recorded in a group of 20 young volunteers and in another group of 19 older volunteers during a 10-minute period of resting state followed by four consecutive task-related runs. During each task-related run, the participants were exposed to two types of sensory stimulation: a tactile stimulation consisting in a textured-disk rotation under the palm of their right hand or a muscle proprioceptive stimulation consisting in a mechanical vibration applied to the muscle tendon of their wrist abductor. These two stimulations are known to evoke illusory sensations of hand movement, while the hand remains actually still. Therefore, the dataset is meant to be used to assess age-related functional brain changes during the perception of hand movements based on muscle proprioception or touch individually. It also allows to explore any structural changes or functional resting connectivity alteration with aging. The dataset is a supplement to the research findings in the paper 'Functional brain changes in the elderly for the perception of hand movements: a greater impairment occurs in proprioception than touch published in NeuroImage.

Neuronal Encoding of Multisensory Motion Features in the Rat Associative Parietal Cortex.

Motion perception is facilitated by the interplay of various sensory channels. In rodents, the cortical areas involved in multisensory motion coding remain to be identified. Using voltage-sensitive-dye imaging, we revealed a visuo-tactile convergent region that anatomically corresponds to the associative parietal cortex (APC). Single unit responses to moving visual gratings or whiskers deflections revealed a specific coding of motion characteristics strikingly found in both sensory modalities. The heteromodality of this region was further supported by a large proportion of bimodal neurons and by a classification procedure revealing that APC carries information about motion features, sensory origin and multisensory direction-congruency. Altogether, the results point to a central role of APC in multisensory integration for motion perception.

Functional brain changes in the elderly for the perception of hand movements: A greater impairment occurs in proprioception than touch.

Unlike age-related brain changes linked to motor activity, neural alterations related to self-motion perception remain unknown. Using fMRI data, we investigated age-related changes in the central processing of somatosensory information by inducing illusions of right-hand rotations with specific proprioceptive and tactile stimulation. Functional connectivity during resting-state (rs-FC) was also compared between younger and older participants. Results showed common sensorimotor activations in younger and older adults during proprioceptive and tactile illusions, but less deactivation in various right frontal regions and the precuneus were found in the elderly. Older participants exhibited a less-lateralized pattern of activity across the primary sensorimotor cortices (SM1) in the proprioceptive condition only. This alteration of the interhemispheric balance correlated with declining individual performance in illusion velocity perception from a proprioceptive, but not a tactile, origin. By combining task-related data, rs-FC and behavioral performance, this study provided consistent results showing that hand movement perception was altered in the elderly, with a more pronounced deterioration of the proprioceptive system, likely due to the breakdown of inhibitory processes with aging. Nevertheless, older people could benefit from an increase in internetwork connectivity to overcome this kinesthetic decline.

Functional Connectivity in Chronic Nonbothersome Tinnitus Following Acoustic Trauma: A Seed-Based Resting-State Functional Magnetic Resonance Imaging Study.

Background: Tinnitus and its mechanisms are an ongoing subject of interrogation in the neuroscientific community. Although most current models agree that it encompasses multiple structures within and outside the auditory system, evidence provided in the literature suffers from a lack of convergence. To further our understanding of contributions to tinnitus lying outside the auditory system, we explored a new model based on a proprioceptive hypothesis specifically in subjects experiencing chronic nonbothersome tinnitus due to acoustic trauma. The present study addresses the role of the right operculum 3 (OP3) involved in this model. It also investigates classical models of tinnitus. Methods: A seed-based resting-state magnetic resonance imaging study explored the functional connectivity in an acoustic trauma group presenting slight to mild nonbothersome chronic tinnitus and compared it with a control group. Results: Group differences were found with two networks: with the sensorimotor-auditory and the frontoparietal, but not with the default mode network nor the limbic regions. In the auditory pathway, the inferior colliculus displayed group differences in connectivity with the right superior parietal lobule. Exploratory analysis elicited a significant increase in connectivity between two seeds in the right OP3 and two mirror regions of the dorsal prefrontal cortex, thought to correspond to the human homologue of the premotor ear-eye field bilaterally and the inferior parietal lobule involved in proprioception, in the tinnitus group. Conclusions: These new findings support the view that acoustic trauma tinnitus could bear a proprioceptive contribution and that a permanent cognitive control is required to filter out this chronic phantom percept.

Seeing Your Foot Move Changes Muscle Proprioceptive Feedback.

Multisensory effects are found when the input from single senses combines, and this has been well researched in the brain. Presently, we examined in humans the potential impact of visuo-proprioceptive interactions at the peripheral level, using microneurography, and compared it with a similar behavioral task. We used a paradigm where participants had either proprioceptive information only (no vision) or combined visual and proprioceptive signals (vision). We moved the foot to measure changes in the sensitivity of single muscle afferents, which can be altered by the descending fusimotor drive. Visual information interacted with proprioceptive information, where we found that for the same passive movement, the response of muscle afferents increased when the proprioceptive channel was the only source of information, as compared with when visual cues were added, regardless of the attentional level. Behaviorally, when participants looked at their foot moving, they more accurately judged differences between movement amplitudes, than in the absence of visual cues. These results impact our understanding of multisensory interactions throughout the nervous system, where the information from different senses can modify the sensitivity of peripheral receptors. This has clinical implications, where future strategies may modulate such visual signals during sensorimotor rehabilitation.

Contribution of Visual Motion Cues from a Held Tool to Kinesthesia.

Incorporation of a tool into the body schema is well established. Here, we assessed whether visual signals originating from the tool provide relevant cues for the perception of arm movements, as would signals originating from the arm holding it. Kinesthetic illusions were investigated by passively moving one arm (via a robotized manipulandum) and therefore the tool (a rake), using the mirror paradigm, with the reflected part being limited to the tool, the arm, or both. Illusory movements concerned the other arm, remaining static and hidden behind the mirror. In Experiments 1 and 3, participants held the same tools in their hands. Results showed that seeing the displacement of the reflected tool in the mirror induced kinesthetic mirror illusions in the hidden arm, similarly to seeing the reflected arm itself, though slightly reduced in terms of strength and occurrence frequency. In Experiment 2, participants held either the same objects in their hands (the rakes) or different ones (a rake, the image of which was reflected in the mirror, and a ball in the other hand). Results showed that mirror vision of the moving tool was not sufficient for mirror illusions to occur, the same tool in the two hands being an essential condition. Finally, in Experiment 3, we showed that neither prior practice nor active tool use was necessary for the tool mirror illusion to occur. Altogether, these results demonstrate that the visual cues originating from the held-tool are integrated for sensing arm movement.

What's left of the mirror illusion when the mirror can no longer be seen? Bilateral integration of proprioceptive afferents!

Recent data suggest that manipulating the muscle afferents of one arm affects both ipsilateral and contralateral perceptual estimates. Here, we used the mirror paradigm to study the bimanual integration of kinesthetic muscle afferents. The reflection of a moving hand in a mirror positioned in the sagittal plane creates an illusion of symmetrical bimanual movement. Although vision clearly has a role in kinesthesia, its role in the mirror illusion might have been overestimated. Conversely, the role of bimanual integration of muscle afferents might have been underestimated. We hypothesized that muscle-proprioceptive afferents of the passively displaced arm (the image of which was reflected in the mirror) are involved in this illusion. We evoked in 19 healthy adult participants the mirror illusion by displacing passively their left arm, the image of which was reflected in the mirror. Once participants experienced the illusion that their hidden right arm was moving, we then either occluded their view of the mirror (using occlusive glasses) and/or prevent the passive left arm displacement. Participants' illusion characteristics (duration and kinematic) under these conditions were compared with classical mirror illusion (without visual occlusion). We found that as long as the arm was still moving, the kinesthetic illusion decayed slowly after visual occlusion. These findings suggest that the mirror illusion results from the combination of visuo-proprioceptive signals from the two arms and is not purely visual in origin. Our findings also support the more general concept whereby proprioceptive afferents are integrated bilaterally for the purpose of kinesthesia during bimanual tasks.

Specific brain activation patterns associated with two neuromuscular electrical stimulation protocols.

The influence of neuromuscular electrical stimulation (NMES) parameters on brain activation has been scarcely investigated. We aimed at comparing two frequently used NMES protocols - designed to vary in the extent of sensory input. Whole-brain functional magnetic resonance imaging was performed in sixteen healthy subjects during wide-pulse high-frequency (WPHF, 100 Hz-1 ms) and conventional (CONV, 25 Hz-0.05 ms) NMES applied over the triceps surae. Each protocol included 20 isometric contractions performed at 10% of maximal force. Voluntary plantar flexions (VOL) were performed as control trial. Mean force was not different among the three protocols, however, total current charge was higher for WPHF than for CONV. All protocols elicited significant activations of the sensorimotor network, cerebellum and thalamus. WPHF resulted in lower deactivation in the secondary somatosensory cortex and precuneus. Bilateral thalami and caudate nuclei were hyperactivated for CONV. The modulation of the NMES parameters resulted in differently activated/deactivated regions related to total current charge of the stimulation but not to mean force. By targeting different cerebral brain regions, the two NMES protocols might allow for individually-designed rehabilitation training in patients who can no longer execute voluntary movements.

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

The 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.

Brain Regions Associated to a Kinesthetic Illusion Evoked by Watching a Video of One's Own Moving Hand.

It is well known that kinesthetic illusions can be induced by stimulation of several sensory systems (proprioception, touch, vision…). In this study we investigated the cerebral network underlying a kinesthetic illusion induced by visual stimulation by using functional magnetic resonance imaging (fMRI) in humans. Participants were instructed to keep their hand still while watching the video of their own moving hand (Self Hand) or that of someone else's moving hand (Other Hand). In the Self Hand condition they experienced an illusory sensation that their hand was moving whereas the Other Hand condition did not induce any kinesthetic illusion. The contrast between the Self Hand and Other Hand conditions showed significant activation in the left dorsal and ventral premotor cortices, in the left Superior and Inferior Parietal lobules, at the right Occipito-Temporal junction as well as in bilateral Insula and Putamen. Most strikingly, there was no activation in the primary motor and somatosensory cortices, whilst previous studies have reported significant activation in these regions for vibration-induced kinesthetic illusions. To our knowledge, this is the first study that indicates that humans can experience kinesthetic perception without activation in the primary motor and somatosensory areas. We conclude that under some conditions watching a video of one's own moving hand could lead to activation of a network that is usually involved in processing copies of efference, thus leading to the illusory perception that the real hand is indeed moving.

The role of tactile afference in shaping motor behaviour and implications for prosthetic innovation.

The present review focusses on how tactile somatosensory afference is encoded and processed, and how this information is interpreted and acted upon in terms of motor control. We relate the fundamental workings of the sensorimotor system to the rehabilitation of amputees using modern prosthetic interventions. Our sense of touch is central to our everyday lives, from allowing us to manipulate objects accurately to giving us a sense of self-embodiment. There are a variety of specialised cutaneous mechanoreceptive afferents, which differ in terms of type and density according to the skin site. In humans, there is a dense innervation of our hands, which is reflected in their vast over-representation in somatosensory and motor cortical areas. We review the accumulated evidence from animal and human studies about the precise interplay between the somatosensory and motor systems, which is highly integrated in many brain areas and often not separable. The glabrous hand skin provides exquisite, discriminative detail about touch, which is useful for refining movements. When these signals are disrupted, such as through injury or amputation, the consequences are considerable. The development of sensory feedback in prosthetics offers a promising avenue for the full integration of a missing body part. Real-time touch feedback from motor intentions aids in grip control and the ability to distinguish different surfaces, even introducing the possibility of pleasure in artificial touch. Thus, our knowledge from fundamental research into sensorimotor interactions should be used to develop more realistic and integrative prostheses.

Kinaesthetic mirror illusion and spatial congruence.

Position sense and kinaesthesia are mainly derived from the integration of somaesthetic and visual afferents to form a single, coherent percept. However, visual information related to the body can play a dominant role in these perceptual processes in some circumstances, and notably in the mirror paradigm. The objective of the present study was to determine whether or not the kinaesthetic illusions experienced in the mirror paradigm obey one of the key rules of multisensory integration: spatial congruence. In the experiment, the participant's left arm (the image of which was reflected in a mirror) was either passively flexed/extended with a motorized manipulandum (to induce a kinaesthetic illusion in the right arm) or remained static. The right (unseen) arm remained static but was positioned parallel to the left arm's starting position or placed in extension (from 15° to 90°, in steps of 15°), relative to the left arm's flexed starting position. The results revealed that the frequency of the illusion decreased only slightly as the incongruence prior to movement onset between the reflected left arm and the hidden right arm grew and remained quite high even in the most incongruent settings. However, the greater the incongruence between the visually and somaesthetically specified positions of the right forearm (from 15° to 90°), the later the onset and the lower the perceived speed of the kinaesthetic illusion. Although vision dominates perception in a context of visuoproprioceptive conflict (as in the mirror paradigm), our results show that the relative weightings allocated to proprioceptive and visual signals vary according to the degree of spatial incongruence prior to movement onset.

Differential contributions of vision, touch and muscle proprioception to the coding of hand movements.

To further elucidate the mechanisms underlying multisensory integration, this study examines the controversial issue of whether congruent inputs from three different sensory sources can enhance the perception of hand movement. Illusory sensations of clockwise rotations of the right hand were induced by either separately or simultaneously stimulating visual, tactile and muscle proprioceptive channels at various intensity levels. For this purpose, mechanical vibrations were applied to the pollicis longus muscle group in the subjects' wrists, and a textured disk was rotated under the palmar skin of the subjects' right hands while a background visual scene was projected onto the rotating disk. The elicited kinaesthetic illusions were copied by the subjects in real time and the EMG activity in the adductor and abductor wrist muscles was recorded. The results show that the velocity of the perceived movements and the amplitude of the corresponding motor responses were modulated by the nature and intensity of the stimulation. Combining two sensory modalities resulted in faster movement illusions, except for the case of visuo-tactile co-stimulation. When a third sensory input was added to the bimodal combinations, the perceptual responses increased only when a muscle proprioceptive stimulation was added to a visuo-tactile combination. Otherwise, trisensory stimulation did not override bimodal conditions that already included a muscle proprioceptive stimulation. We confirmed that vision or touch alone can encode the kinematic parameters of hand movement, as is known for muscle proprioception. When these three sensory modalities are available, they contribute unequally to kinaesthesia. In addition to muscle proprioception, the complementary kinaesthetic content of visual or tactile inputs may optimize the velocity estimation of an on-going movement, whereas the redundant kinaesthetic content of the visual and tactile inputs may rather enhance the latency of the perception.

Combined contribution of tactile and proprioceptive feedback to hand movement perception.

UNLABELLED: Here we investigated how the tactile modality is used along with muscle proprioception in hand movement perception, whether these two sensory inputs are centrally integrated and whether they work complementarily or concurrently. The illusory right hand rotations induced in eleven volunteers by a textured disk scrolling under their hand in two directions at three velocities and/or by mechanical vibration applied to their wrist muscles at three frequencies were compared. The kinesthetic illusions were copied by the subjects on-line with their left hand. RESULTS: 1) in all the subjects, tactile stimulation alone induced an illusory hand rotation in the opposite direction to that of the disk, and the velocity of the illusion increased non-linearly with the disk velocity: the highest gain (the illusion velocity to disk velocity ratio) occurred at the slowest disk rotation; 2) adding a consistent proprioceptive stimulus increased the perceptual effects, whereas adding a conflicting proprioceptive stimulus of increasing frequency gradually decreased the tactile illusions and reversed their initial direction; 3) under both consistent and conflicting conditions, only strong proprioceptive stimulation significantly affected the gain of the resulting illusions, whereas the largest gain always occurred at low tactile stimulation levels when the illusory movements were in the same direction as the tactile-induced illusion. Tactile information may equal or even override muscle proprioceptive information in the perception of relatively small, slow hand movements. These two somatosensory inputs may be integrated complementarily, depending on their respective relevance to the task of accurately perceiving one's own hand movements.

Countering postural posteffects following prolonged exposure to whole-body vibration: a sensorimotor treatment.

Postural stability of bulldozer operators after a day of work is investigated. When operators are no longer exposed to whole-body vibration (WBV) generated by their vehicle, their sensorimotor coordination and body representation remain altered. A sensorimotor treatment based on a set of customized voluntary movements is tested to counter and prevent potential post-work accidents due to prolonged exposure to WBV. This treatment includes muscle stretching, joint rotations, and plantar pressures, all known to minimize the deleterious effects of prolonged exposure to mechanical vibrations. The postural stability of participants (drivers; N = 12) was assessed via the area of an ellipse computed from the X and Y displacements of the center-of-pressure (CoP) in the horizontal plane when they executed a simple balance task before driving, after driving, and after driving and having performed the sensorimotor treatment. An ancillary experiment is also reported in which a group of non-driver participants (N = 12) performed the same postural task three times during the same day but without exposure to WBV or the sensorimotor treatment. Prolonged exposure to WBV significantly increased postural instability in bulldozer drivers after they operated their vehicle compared to prior to their day of work. The sensorimotor treatment allowed postural stability to return to a level that was not significantly different from that before driving. The results reveal that (1) the postural system remains perturbed after prolonged exposure to WBV due to operating a bulldozer and (2) treatment immediately after driving provides a "sensorimotor recalibration" and a significant decrease in WBV-induced postural instability. If confirmed in different contexts, the postural re-stabilizing effect of the sensorimotor treatment would constitute a simple, rapid, inexpensive, and efficient means to prevent post-work accidents due to balance-related issues.

Postural changes after sustained neck muscle contraction in persons with a lower leg amputation.

Lower leg amputation generally induces asymmetrical weight-bearing, even after rehabilitation treatment is completed. This is detrimental to the amputees' long term quality of life. In particular, increasing strains on joint surfaces that receive additional weight load causes back and leg pain, premature wear and tear and arthritis. This pilot study was designed to determine whether subjects with lower leg amputation experience postural post-effects after muscle contraction, a phenomenon already observed in healthy subjects, and whether this could improve the weight-bearing on their prosthesis. Fifteen subjects with a unilateral lower leg amputation and 17 control subjects volunteered to participate in this study. Centre of pressure (CP) position was recorded during standing posture, under eyes closed and open conditions. Recordings were carried out before the subjects performed a 30-s voluntary isometric lateral neck muscle contraction, and again 1 and 4 min after the contraction. Postural post-effects characterized by CP shift, occurred in the medio-lateral plane in the majority of the amputated (7/15 eyes closed, 9/15 eyes open) and control (9/17 eyes closed, 11/17 eyes open) subjects after the contraction. Half of these subjects had a CP shift towards the side of the contraction and the other half towards the opposite side. In four amputated subjects tested 3 months apart, shift direction remained constant. These postural changes occurred without increase in CP velocity. Thus, a 30-s voluntary isometric contraction can change the standing posture of persons with lower leg amputation. The post-effects might result from the adaptation of the postural frame of reference to the proprioceptive messages associated with the isometric contraction.