Beyond sense-specific processing: decoding texture in the brain from touch and sonified movement.

Texture, a fundamental object attribute, is perceived through multisensory information including touch and auditory cues. Coherent perceptions may rely on shared texture representations across different senses in the brain. To test this hypothesis, we delivered haptic textures coupled with a sound synthesizer to generate real-time textural sounds. Participants completed roughness estimation tasks with haptic, auditory, or bimodal cues in an MRI scanner. Somatosensory, auditory, and visual cortices were all activated during haptic and auditory exploration, challenging the traditional view that primary sensory cortices are sense-specific. Furthermore, audio-tactile integration was found in secondary somatosensory (S2) and primary auditory cortices. Multivariate analyses revealed shared spatial activity patterns in primary motor and somatosensory cortices, for discriminating texture across both modalities. This study indicates that primary areas and S2 have a versatile representation of multisensory textures, which has significant implications for how the brain processes multisensory cues to interact more efficiently with our environment.

A new patterned air-flow device to reveal the network for tactile motion coding using fMRI.

BACKGROUND: Studying brain processes underlying tactile perception induced by natural-like stimulation is challenging yet crucial to closely match real-world situations. NEW METHOD: We developed a computer-controlled pneumatic device that allows the delivery of complex airflow patterns on subject's body, through a MR-compatible system fixed on an independent clippable mounting device. The intensity of stimulation as well as the timing of each of the four air channels are completely programmable and independent, allowing the precise control and modularity of the airflow delivery. RESULTS: An analysis of signal-to-noise ratio (SNR) measurements did not show any impact of the PAF device on anatomical or functional scan acquisitions. A psychophysical experiment was also performed on 24 volunteers to evaluate the perception of different airflow patterns delivered over the lower part of their face. It revealed that all participants were able to finely discriminate the direction of these leftward to rightward flow motions. The fMRI experiment, which consisted in presenting to 20 participants four different airflow patterns, shed light on the brain network associated with tactile motion perception. A multivariate analysis further showed a specific coding of the different patterns inside this tactile brain network including the primary and secondary somatosensory cortex COMPARISON WITH EXISTING METHOD(S): The Patterned Air-Flow (PAF) is an easy-to-set-up, portable, adaptable device, which can be spatially and temporally modulated to provide complex tactile stimuli. CONCLUSIONS: This device will be useful to further explore complex dynamic touch exerted over various body parts and can also be combined with visual or auditory stimulation to study multisensory mechanisms.

Hand movement illusions show changes in sensory reliance and preservation of multisensory integration with age for kinaesthesia.

To perceive self-hand movements, the central nervous system (CNS) relies on multiple sensory inputs mainly derived from vision, touch, and muscle proprioception. However, how and to what extent the CNS relies on these sensory systems to build kinesthetic percepts as the systems decline with age remain poorly understood. Illusory sensations of right hand rotation were induced by separately stimulating these three sensory modalities at two intensity levels. A mechanical vibrator applied to the pollicis longus muscle, a textured disk for touching, and a visual pattern rotating under the participant's hand were used to activate muscle proprioception, touch, and vision, respectively. The perceptual responses of 19 healthy elderly adults (60-88 yrs) were compared to those of 12 younger adults (19-40 yrs). In the younger group, the three types of stimulation elicited similar kinesthetic illusions at each intensity level applied. The same visual and tactile stimuli elicited more salient and faster illusions in older adults than in younger adults. In contrast, the vibration-induced illusions were significantly fewer, less salient and delayed in the older adults. For the three modalities considered, increasing the intensity of stimulation resulted in smaller increases in illusion velocity in older adults than in younger adults. Lastly, a similar improvement in the perceptual responses was observed in older and younger adults when several stimulations were combined and older participants reported more salient illusions than younger participants only in the visuo-tactile condition. This study suggests that reliance on sensory inputs for kinesthetic purposes is profoundly reshaped with aging. The elderly may rely more on visual and tactile afferents for perceiving self-hand movements than younger adults likely due to relatively greater muscle proprioception degradation. In addition, multisensory integration seems preserved but not enhanced to compensate for the global decline of all sensory systems with age.

Age-Related Impairment of Hand Movement Perception Based on Muscle Proprioception and Touch.

Impairment in fine hand motor dexterity is well established in older people, yet little is known, about the impaired perception of hand movement in the elderly. Only an age-related increase in movement detection threshold has been reported. Perception of hand movements relies on multiple sensory information, including touch and muscle proprioception. The present study aims to investigate to what extent aging impacts the ability to perceive hand movements accurately and whether this impairment is from a muscle touch and/or tactile origin. To disentangle proprioception and touch, we used specifically designed stimuli: a mechanical vibration applied to the wrist muscle tendon and a tactile-textured disk rotating under the participant's hand, respectively. These two stimuli elicited illusions of hand rotations in two groups of young (20-30 years) and older (65-75 years) participants. Psychophysical testing showed that velocity discrimination thresholds of tactile and proprioceptive illusions were about twice lower in the young, than the older group. Also, relatively small isometric contractions were involuntarily elicited in wrist muscles during the illusions in both groups, but this motor response was positively correlated with the discrimination performance of the young, but not the older, participants. The present results show that muscle proprioception and touch are both functionally affected in kinesthesia after 65 years old, with a more pronounced alteration for muscle proprioception. This alteration in discriminative ability is likely due to impairment in the accurate encoding of the kinematic properties of hand movements. The possible central vs peripheral origin of these perceptive-motor changes with aging is discussed.

Optimal visuotactile integration for velocity discrimination of self-hand movements.

Illusory hand movements can be elicited by a textured disk or a visual pattern rotating under one's 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.

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 paradigm's 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.

Illusory movements prevent cortical disruption caused by immobilization.

Enforced limb disuse strongly disrupts the cortical networks that are involved in sensorimotor activities. This disruption causes a cortical reorganization that may be functionally maladaptive. In this study, we used functional magnetic resonance imaging (fMRI) to investigate whether it is possible to prevent this reorganization by compensating for the lack of actual kinesthetic perception with illusory movements induced by "neuromimetic" proprio-tactile feedback that is artificially delivered during immobilization. Sixteen healthy volunteers were equipped for five days with full-hand ortheses that prevented them from performing finger and hand movements but allowed for kinesthetic and tactile sensations. Eight participants received a twice-daily proprio-tactile treatment consisting of the perception of kinesthetic sensations resembling those felt during actual movements generated by miniature vibrators set in the ortheses at the finger and wrist levels. Eight untreated participants received no stimulation. The effects of hand immobilization and treatment were assessed by fMRI during a calibrated voluntary hand movement task and hand tactile stimulation before cast placement and immediately after cast removal. We found that the sensorimotor network was preserved in subjects who underwent this treatment during hand immobilization, while the sensorimotor network of untreated subjects was significantly altered. These findings suggest that sensory feedback and associated movement perception may counteract disuse-induced cortical plastic changes through recruitment of a large part of the cortical network used for actual performed movement. The possibility of guiding cortical plasticity with proprioceptive augmented feedback is potentially relevant for rehabilitation efforts.

Proprio-tactile integration for kinesthetic perception: an fMRI study.

This study aims to identify the cerebral networks involved in the integrative processing of somesthetic inputs for kinesthetic purposes. In particular, we investigated how muscle proprioceptive and tactile messages can result in a unified percept of one's own body movements. We stimulated either separately or conjointly these two sensory channels in order to evoke kinesthetic illusions of a clockwise rotation of 10 subjects' right hand in an fMRI environment. Results first show that, whether induced by a tactile or a proprioceptive stimulation, the kinesthetic illusion was accompanied by the activation of a very similar cerebral network including cortical and subcortical sensorimotor areas, which are also classically found in passive or imagined movement tasks. In addition, the strongest kinesthetic illusions occurred under the congruent proprio-tactile co-stimulation condition. They were specifically associated to brain area activations distinct from those evidenced under the unimodal stimulations: the inferior parietal lobule, the superior temporal sulcus, the insula-claustrum region, and the cerebellum. These findings support the hypothesis that heteromodal areas may subserve multisensory integrative mechanisms at cortical and subcortical levels. They also suggest the integrative processing might consist of detection of the spatial coherence between the two kinesthetic messages involving the inferior parietal lobule activity and of a detection of their temporal coincidence via a subcortical relay, the insula structure, usually linked to the relative synchrony of different stimuli. Finally, the involvement of the superior temporal sulcus in the feeling of biological movement and that of the cerebellum in the movement timing control are also discussed.

Vibration-induced post-effects: a means to improve postural asymmetry in lower leg amputees?

Muscle vibration has been shown to induce long-lasting and oriented alteration of standing posture in healthy individuals. The postural alterations can last several minutes following the end of vibration and are called post-effects. The goal of this study was to determine whether persons with lower leg amputation that show persistent postural asymmetry after usual rehabilitation experience these postural post-effects and if this could improve their weight bearing on the prosthesis. Centre of pressure (CP) position during stance was recorded prior to and up to 13 min after a 30s unilateral vibration applied during sitting to lateral neck (trapezius) or hip (gluteus medius) muscles in 14 individuals with unilateral lower leg amputation and 18 controls. The amputees' postural asymmetry was confirmed prior to the vibration intervention. A CP displacement, without an increase in CP velocity, was observed in both groups of participants over the 13 min post-vibration. For both the neck or hip vibration sites, the CP shifts were directed in the medio-lateral plane and were oriented either towards the vibrated side or the opposite side across subjects. This led to a decrease of postural asymmetry in half of the group of amputees. Within subject, the orientation of the post-effect was constant and changed to the opposite direction with vibration of the opposite body side. It is suggested that the post-effects are produced by a change of the postural reference consequent to the sustained proprioceptive message induced during the muscle vibration period. The orientation of the post-effects is discussed in relation to the notion of reference frame preference. All in all, because post-effect orientation is constant within subject and adaptive, future studies should investigate if individuals with lower leg amputation could benefit from postural post-effects induced by muscle vibration to improve function.

Cerebral correlates of the "Kohnstamm phenomenon": an fMRI study.

This paper addresses the issue of the central correlates of the "Kohnstamm phenomenon", i.e. the long-lasting involuntary muscle contraction which develops after a prolonged isometric voluntary contraction. Although this phenomenon was described as early as 1915, the mechanisms underlying these post-effects are not yet understood. It was therefore proposed to investigate whether specific brain areas may be involved in the motor post-effects induced by either wrist muscle contraction or vibration using the fMRI method. For this purpose, experiments were carried out on the right wrist of 11 healthy subjects. Muscle activity (EMG) and regional cerebral blood flow were recorded during isometric voluntary muscle contraction and muscle vibration, as well as during the subsequent involuntary contractions (the post-effects) which occurred under both conditions. Brain activations were found to occur during the post-contraction and post-vibration periods, which were very similar under both conditions. Brain activation involved motor-related areas usually responsible for voluntary motor command (primary sensory and motor cortices, premotor cortex, anterior and posterior cingulate gyrus) and sensorimotor integration structures such as the posterior parietal cortex. Comparisons between the patterns of brain activation associated with the involuntary post-effects and those accompanying voluntary contraction showed that cerebellar vermis was activated during the post-effect periods whereas the supplementary motor area was activated only during the induction periods. Although post-effects originate from asymmetric proprioceptive inputs, they might also involve a central network where the motor and somatosensory areas and the cerebellum play a key role. In functional terms, they might result from the adaptive recalibration of the postural reference frame altered by the sustained proprioceptive inputs elicited by muscle contraction and vibration.

Long-lasting body leanings following neck muscle isometric contractions.

Our objective was to investigate the neural mechanisms and the functional relevance of motor effects that develop involuntarily following the release of a sustained isometric muscle contraction. The few data available in the literature deal only with post-contractions occurring in a body segment. Although these data emphasise the role of proprioceptive input, the question as to whether this phenomenon is of central or peripheral origin remains unclear. Given the leading role of neck muscle proprioceptive input in body orientation and posture regulation, we designed two experiments to test for postural posteffects after voluntary and involuntary neck muscle contraction. The spatiotemporal characteristics of the posteffects were analysed by means of stabilometric recordings following 30-s isometric contraction of splenius, trapezius and levator muscle groups, and 30-s electrically-induced contraction of the levator muscle group. Results show that a postural response occurred after voluntary contraction of each muscle group tested, which was oriented in the plane of action of the muscle, and lasted 14 min at least. In contrast, no clearly oriented body leanings were found after electrical stimulation of the levator muscle, except for a slight increase in natural postural instability. Data are interpreted as a change in the postural reference resulting from an increase in proprioceptive inflow accompanying mainly the voluntary muscle contraction.

Foot sole and ankle muscle inputs contribute jointly to human erect posture regulation.

In order to assess the relative contribution and the interactions of the plantar cutaneous and muscle proprioceptive feedback in controlling human erect posture, single or combined vibratory stimuli were applied to the forefoot areas and to the tendons of the tibialis anterior muscles of nine standing subjects using various vibration frequency patterns (ranging from 20 to 80 Hz). The variations in the centre of foot pressure, ankle angle and the EMG activities of the soleus and tibialis anterior muscles of each subject were recorded and analysed. Separate stimulation of the plantar forefoot zones or the tibialis anterior muscles always resulted in whole-body tilts oppositely directed backwards and forwards, respectively, the amplitude of which was proportional to the vibration frequency. EMG activity of ankle muscles also varied according to the direction of the postural responses. However, the same vibration frequency did not elicit equivalent postural responses: in the low frequency range, tactile stimulation induced stronger postural effects than proprioceptive stimulation, and the converse was the case for the higher frequency range. Under sensory conflict conditions, i.e. foot sole-flexor ankle muscle co-stimulation, the direction of the body tilts also varied according to the difference and the absolute levels of the vibration frequencies. In all cases, the resulting postural shifts always corresponded to the theoretical sum of the isolated effects observed upon vibrating each of these two sensory channels. We proposed that tactile and proprioceptive information from the foot soles and flexor ankle muscles might be co-processed following a vector addition mode to subserve the maintenance of erect stance in a complementary way.

Specific whole-body shifts induced by frequency-modulated vibrations of human plantar soles.

This study sought to analyze the postural responses induced by separately or simultaneously vibrating with different frequencies the forefoot and rear foot zones of both soles in standing subjects. Stimulating each zone separately resulted in spatially oriented body tilts; their amplitude and velocity varied linearly according to the frequency, and their direction was always opposite to the plantar site vibrated. When the two zones were each co-stimulated at different frequencies, the parameters of the postural responses depended on the frequency difference. When this frequency difference was zero, no clearly oriented body tilts occurred. We concluded that the change in the relative pressures evoked by differently co-vibrating these zones gave rise to regulative postural adjustments able to cancel the simulated body deviation.

From balance regulation to body orientation: two goals for muscle proprioceptive information processing?

This study was based on the assumption that the central processing of proprioceptive inputs that arise from numerous muscles contributes to both awareness and control of body posture. The muscle-spindle inputs form a "proprioceptive chain" which functionally links the eye muscles to the foot muscles. Here, we focused on the specific contribution of two links in the control of human erect posture by investigating how proprioceptive messages arising from ankle and neck muscles may be integrated by the central nervous system. Single or combined mechanical vibrations were applied to different muscle tendons at either one (ankle or neck) or both (ankle plus neck) body levels. The amplitude and the specific direction of the resulting oriented body tilts were analyzed by recording the center of foot pressure (CoP) through a force platform with four strain gauges. The results can be summarized as follows: (1) the vibration-induced whole-body tilts were oriented according to the muscles stimulated; furthermore, the tilts were in opposite directions when neck or ankle muscles on the same side of the body were stimulated; (2) except for the ankle antagonist muscles, co-vibrating adjacent or antagonist muscles at the same body level (ankle or neck) resulted in body sways, whose orientation was a combination of those obtained by stimulating these muscles separately; and (3) likewise, co-vibrating ankle and neck muscles induced whole-body postural responses, whose direction and amplitude were a combination of those obtained by separate vibration. We conclude that the multiple proprioceptive inputs originating from either one or both body levels may be co-processed in terms of vector-addition laws. Moreover, we propose that proprioceptive information from ankle and neck muscles may be used for two tasks: balance control and body orientation, with central integration of both tasks.

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 subject's 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.