Jean-Pierre Roll

Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography.

SummaryThe characteristics of vibration-induced illusory joint movements were studied in healthy human subjects. Unseen by the subject, constant frequency vibration trains applied to the distal tendon of the Triceps or Biceps induced an almost constant velocity illusory movement of the elbow whose direction corresponded to that of a joint rotation stretching the vibrated muscle. Vibration trains of the same duration and frequency applied alternatively to the Biceps and Triceps evoked alternating flexion-extension illusory movements.During successive application of vibration trains at frequencies from 10 to 120 Hz, the perceived velocity of the illusory movements increased progressively from 10 to 70–80 Hz, then decreased from 80 to 120 Hz. The maximal perceived velocity was three times higher during alternating vibration of the Biceps and Triceps than during single muscle stimulation.Unit activity from 15 muscle spindle primary endings and five secondary endings located in Tibialis anterior and Extensor digitorum longus muscles were recorded using microneurography in order to study their responses to tendon vibration and passive and active movements of the ankle.Primary endings were all activated by low amplitude tendon vibration (0.2–0.5 mm) previously used to induce illusory movements of the elbow. The discharge of some was phase-locked with the vibration cycle up to 120 Hz, while others responded one-to-one to the vibration cycle up to 30–50 Hz, then fired in a sub-harmonic manner at higher frequencies. Secondary endings were much less sensitive to low amplitude tendon vibration.Primary and secondary ending responses to ramp and sinusoïdal movements of the ankle joint were compared. During the movement, the primary ending discharge frequency was almost constant, while the secondary ending activity progressively increased. During ankle movements the primary ending discharge appeared mainly related to velocity, while some secondary activities seemed related to both movement velocity and joint angle position.Muscle spindle sensory ending responses to active and passive ankle movements stretching the receptor-bearing muscle (plantar flexion) were qualitatively and quantitatively similar. During passive reverse movements (dorsiflexion) most of the sensory endings stopped firing when their muscle shortened. Active muscle shortening (isotonic contraction) modulated differently the muscle spindle sensory ending discharge, which could stop completely, decrease or some times increase during active ankle dorsiflexion. During isometric contraction most of the muscle spindle sensory endings were activated.The characteristics of the vibration-induced illusory movements and the muscle spindle responses to tendon vibration and to active and passive joint movements strengthened the possibility of the contribution of primary endings to kinaesthesia, as suggested by several previous works. Moreover, the present results led us to attribute to proprioception in the muscle stretched during joint movement a predominant, but not exclusive, role in this kind of perception.

Cutaneous afferents provide a neuronal population vector that encodes the orientation of human ankle movements

The aim of this study was to analyse the directional coding of two‐dimensional limb movements by cutaneous afferents from skin areas covering a multidirectional joint, the ankle. The activity of 89 cutaneous afferents was recorded in the common peroneal nerve, and the mean discharge frequency of each unit was measured during the outward phase of ramp and hold movements imposed in 16 different directions. Forty‐two afferents responded to the movements in the following decreasing order (SA2, n= 24/27; FA2, n= 13/17; FA1, n= 3/24; SA1, n= 2/21). All the units activated responded to a specific range of directions, defining their ‘preferred sector’, within which their response peaked in a given direction, their ‘preferred direction’. Based on the distribution of the preferred directions, two populations of afferents, and hence two skin areas were defined: the anterior and the external lateral parts of the leg. As the directional tuning of each population was cosine shaped, the neuronal population vector model was applied and found to efficiently describe the movement direction encoded by cutaneous afferents, as it has been previously reported for muscle afferents. The responses of cutaneous afferents were then considered with respect to those of the afferents from the underlying muscles, which were previously investigated, and an almost perfect matching of directional sensitivity was observed. It is suggested that the common movement‐encoding characteristics exhibited by cutaneous and muscle afferents, as early as the peripheral level, may facilitate the central co‐processing of their feedbacks subserving kinaesthesia.

Post-contraction changes in human muscle spindle resting discharge and stretch sensitivity

SummaryThe activities of human muscle spindle primary endings were recorded in the lateral peroneal nerve using the microneurographic method. The aim of the study was to test whether voluntary isometric contraction causes any after-effects, first in the resting discharge of muscle spindle primary endings and secondly in their responses to a slow ramp stretch. To investigate the latter point, the initial angular position of the ankle was passively adjusted until the unit fell silent, in order to introduce a delay in the responses to muscle stretch. The results were as follows: (1) most of the units did not exhibit the “post-contraction sensory discharge” reported to occur in numerous animal experiments; this means that the muscle spindle resting discharge was essentially the same before and after isometric voluntary contraction. (2) Isometric voluntary contraction led to changes in muscle spindle stretch sensitivity which resulted in a reduction in the stretch threshold and a decrease in the muscle spindle dynamic sensitivity. These data suggest that the after-effects observed may have been triggered by static fusimotor neurones. The results are discussed with reference to the theory according to which the processing by the CNS of muscular proprioceptive messages deals mainly with signals arising from muscles stretched during movement, and it is concluded that the coactivation of α and y motoneurones during the contraction facilitates the coding of the parameters of forthcoming stretching movements, by the muscle spindles.

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.

Ankle joint movements are encoded by both cutaneous and muscle afferents in humans

We analyzed the cutaneous encoding of two-dimensional movements by investigating the coding of movement velocity for differently oriented straight-line movements and the coding of complex trajectories describing cursive letters. The cutaneous feedback was then compared with that of the underlying muscle afferents previously recorded during the same “writing-like” movements. The unitary activity of 43 type II cutaneous afferents was recorded in the common peroneal nerve in healthy subjects during imposed ankle movements. These movements consisted first of ramp-and-hold movements imposed at two different and close velocities in seven directions and secondly of “writing-like” movements. In both cases, the responses were analyzed using the neuronal population vector model. The results show that movement velocity encoding depended on the direction of the ongoing movement. Discriminating between two velocities therefore involved processing the activity of afferent populations located in the various skin areas surrounding the moving joint, as shown by the statistically significant difference observed in the amplitude of the sum vectors. Secondly, “writing-like” movements induced cutaneous neuronal patterns of activity, which were reproducible and specific to each trajectory. Lastly, the “cutaneous neuronal trajectories,” built by adding the sum vectors tip-to-tail, nearly matched both the movement trajectories and the “muscle neuronal trajectories,” built from previously recorded muscle afferents. It was concluded that type II cutaneous and the underlying muscle afferents show similar encoding properties of two-dimensional movement parameters. This similarity is discussed in relation to a central gating process that would for instance increase the gain of cutaneous inputs when muscle information is altered by the fusimotor drive.

A new vibrator to stimulate muscle proprioceptors in fMRI

Studying cognitive brain functions by functional magnetic resonance imaging (fMRI) requires appropriate stimulation devices that do not interfere with the magnetic fields. Since the emergence of fMRI in the 90s, a number of stimulation devices have been developed for the visual and auditory modalities. Only few devices, however, have been developed for the somesthesic modality. Here, we present a vibration device for studying somesthesia that is compatible with high magnetic field environments and that can be used in fMRI machines. This device consists of a poly vinyl chloride (PVC) vibrator containing a wind turbine and of a pneumatic apparatus that controls 1–6 vibrators simultaneously. Just like classical electromagnetic vibrators, our device stimulates muscle mechanoreceptors (muscle spindles) and generates reliable illusions of movement. We provide the fMRI compatibility data (phantom test), the calibration curve (vibration frequency as a function of air flow), as well as the results of a kinesthetic test (perceived speed of the illusory movement as a function of vibration frequency). This device was used successfully in several brain imaging studies using both fMRI and magnetoencephalography. Hum Brain Mapp, 2009.

Kinesthetic illusions attenuate experimental muscle pain, as do muscle and cutaneous stimulation.

In the present study, muscle pain was induced experimentally in healthy subjects by administrating hypertonic saline injections into the tibialis anterior (TA) muscle. We first aimed at comparing the analgesic effects of mechanical vibration applied to either cutaneous or muscle receptors of the TA or to both types simultaneously. Secondly, pain alleviation was compared in subjects in whom muscle tendon vibration evoked kinesthetic illusions of the ankle joint. Muscle tendon vibration, which primarily activated muscle receptors, reduced pain intensity by 30% (p<0.01). In addition, tangential skin vibration reduced pain intensity by 33% (p<0.01), primarily by activating cutaneous receptors. Concurrently stimulating both sensory channels induced stronger analgesic effects (-51%, p<0.01), as shown by the lower levels of electrodermal activity. The strongest analgesic effects of the vibration-induced muscle inputs occurred when illusory movements were perceived (-38%, p=0.01). The results suggest that both cutaneous and muscle sensory feedback reduce muscle pain, most likely via segmental and supraspinal processes. Further clinical trials are needed to investigate these new methods of muscle pain relief.