Anne Kavounoudias

The plantar sole is a 'dynamometric map' for human balance control

THIS study investigated the role of the plantar cutaneous information in controlling human balance. We hypothesized that the cutaneous afferent messages from the main supporting zones of the feet have sufficient spatial relevance to inform the CNS about the body position with respect to the vertical reference and consequently to induce adapted regulative postural responses. Skin mechanoreceptors of anterior and/or posterior areas of one or both soles of 10 standing subjects were activated by superficial mechanical vibration with high frequency and low amplitude. Variations of the subjects center of pressure (CoP) were recorded. Spatially oriented whole-body tilts were observed for every subject. Their direction depended on the foot areas stimulated and was always opposite to the vibration-simulated pressure increase. These responses are found to subserve a postural regulative function and we suggest that co-processing of the various cutaneous messages followed a vector addition mode.

Cutaneous afferents from human plantar sole contribute to body posture awareness.

We investigated whether the tactile information from the main supporting areas of the foot are used by the brain for perceptual purposes, namely body posture awareness and body representation in space. We applied various patterns of tactile stimulation to one or both soles of unmoving and blindfolded subjects by a 60 micro-vibrator tactile matrix set in a force platform. The perceptual effects of the stimulation were assessed through a 3D joystick handled by the subjects. All subjects reported illusory perceptions of whole-body leaning. Both orientation and amplitude of these perceptions depended on the stimulation pattern. Additional kinesthetic illusions sometimes occurred along the longitudinal axis of the body. We conclude that foot sole input contributes to the coding and the spatial representation of body posture.

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 ones own hand movements.

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.

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.

Passive or simulated displacement of one arm (but not its mirror reflection) modulates the involuntary motor behavior of the other arm

Recent studies of both healthy and patient populations have cast doubt on the mirror paradigms beneficial effect on motor behavior. Indeed, the voluntary arm displacement that accompanies reflection in the mirror may be the determining factor in terms of the motor behavior of the contralateral arm. The objective of the present study was to assess the respective effects of mirror reflection and arm displacement (whether real or simulated) on involuntary motor behavior of the contralateral arm following sustained, isometric contraction (Kohnstamm phenomenon). Our results revealed that (i) passive displacement of one arm (displacement of the left arm via a motorized manipulandum moving at 4°/s) influenced the velocity of the Kohnstamm phenomenon (forearm flexion occurring shortly after the cessation of muscle contraction) in the contralateral arm and (ii) mirror vision had no effect. Indeed, the velocity of the Kohnstamm phenomenon tended to be adjusted to match the velocity of the passive displacement of the other arm. In a second experiment, arm displacement was simulated by vibrating the triceps at 25, 50 or 75 Hz. Results showed that the velocity of the Kohnstamm phenomenon in one arm increased with the vibration frequency applied to the other arm. Our results revealed the occurrence of bimanual coupling because involuntary displacement of one arm was regulated by muscle-related information generated by the actual or simulated displacement of the other arm. In line with the literature data on voluntary motor behavior, our study failed to evidence an additional impact of mirror vision on involuntary motor behavior.

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.

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 elses 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 ones 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.

Optimal visuo-tactile integration for velocity discrimination of self-hand movements

Illusory hand movements can be elicited by a textured disk or a visual pattern rotating under ones hand, while proprioceptive inputs convey immobility information (Blanchard C, Roll R, Roll JP, Kavounoudias A. PLoS One 8: e62475, 2013). Here, we investigated whether visuotactile integration can optimize velocity discrimination of illusory hand movements in line with Bayesian predictions. We induced illusory movements in 15 volunteers by visual and/or tactile stimulation delivered at six angular velocities. Participants had to compare hand illusion velocities with a 5°/s hand reference movement in an alternative forced choice paradigm. Results showed that the discrimination threshold decreased in the visuotactile condition compared with unimodal (visual or tactile) conditions, reflecting better bimodal discrimination. The perceptual strength (gain) of the illusions also increased: the stimulation required to give rise to a 5°/s illusory movement was slower in the visuotactile condition compared with each of the two unimodal conditions. The maximum likelihood estimation model satisfactorily predicted the improved discrimination threshold but not the increase in gain. When we added a zero-centered prior, reflecting immobility information, the Bayesian model did actually predict the gain increase but systematically overestimated it. Interestingly, the predicted gains better fit the visuotactile performances when a proprioceptive noise was generated by covibrating antagonist wrist muscles. These findings show that kinesthetic information of visual and tactile origins is optimally integrated to improve velocity discrimination of self-hand movements. However, a Bayesian model alone could not fully describe the illusory phenomenon pointing to the crucial importance of the omnipresent muscle proprioceptive cues with respect to other sensory cues for kinesthesia.

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.