David F. Collins

Sensori-sensory afferent conditioning with leg movement: gain control in spinal reflex and ascending paths.

Studies are reviewed, predominantly involving healthy humans, on gain changes in spinal reflexes and supraspinal ascending paths during passive and active leg movement. The passive movement research shows that the pathways of H reflexes of the leg and foot are down-regulated as a consequence of movement-elicited discharge from somatosensory receptors, likely muscle spindle primary endings, both ipsi- and contralaterally. Discharge from the conditioning receptors in extensor muscles of the knee and hip appears to lead to presynaptic inhibition evoked over a spinal path, and to long-lasting attenuation when movement stops. The ipsilateral modulation is similar in phase to that seen with active movement. The contralateral conditioning does not phase modulate with passive movement and modulates to the phase of active ipsilateral movement. There are also centrifugal effects onto these pathways during movement. The pathways of the cutaneous reflexes of the human leg also are gain-modulated during active movement. The review summarizes the effects across muscles, across nociceptive and non-nociceptive stimuli and over time elapsed after the stimulus. Some of the gain changes in such reflexes have been associated with central pattern generators. However, the centripetal effect of movement-induced proprioceptive drive awaits exploration in these pathways. Scalp-recorded evoked potentials from rapidly conducting pathways that ascend to the human somatosensory cortex from stimulation sites in the leg also are gain-attenuated in relation to passive movement-elicited discharge of the extensor muscle spindle primary endings. Centrifugal influences due to a requirement for accurate active movement can partially lift the attenuation on the ascending path, both during and before movement. We suggest that a significant role for muscle spindle discharge is to control the gain in Ia pathways from the legs, consequent or prior to their movement. This control can reduce the strength of synaptic input onto target neurons from these kinesthetic receptors, which are powerfully activated by the movement, perhaps to retain the opportunity for target neuron modulation from other control sources.

Movement illusions evoked by ensemble cutaneous input from the dorsum of the human hand.

1. In this study we tested the hypothesis that ensemble activity in human cutaneous sensory afferents evoked by the stretching of skin over and around the finger joints contributes to the conscious perception of movement of the fingers. 2. In nineteen normal adults, ensembles of cutaneous afferents were activated either by electrical stimulation, delivered through an array of electrodes on the dorsum of the hand and fingers, or by mechanical stretching of the skin over and around the joints. The stretching was applied through an array of threads stuck to the skin, in such a way as to avoid or minimize moving the underlying joints and to avoid applying pressure to underlying tendons and ligaments. Perceived movements were mimicked by voluntary movements of the fingers of the contralateral hand. 3. By way of comparison, kinaesthetic illusions were also evoked by activation of muscle receptors by vibration. 4. Illusions of movement were elicited with each type of stimulus. Electrical stimulation of skin afferents caused clear illusory movements in six out of seventeen subjects (35%), and borderline movement illusions in three out of the same seventeen subjects (total 9/17, 53%). Various other localized skin sensations were also reported. Skin stretch evoked movement illusions in eleven out of nineteen of subjects (58%). In all subjects who received both cutaneous stimuli, twelve out of seventeen (71%) reported some movement sensations with one or other of the stimulation techniques. Vibration tended to be the most reliable stimulus modality, eliciting illusory movements in fourteen out of sixteen subjects (88%). 5. Although the skin stretching technique did cause minute movements of nearby joints in several cases, these were monitored and shown in separate control experiments to be below perceptual threshold, and so the movement illusions could be safely attributed to the cutaneous afferent input evoked by skin stretch. 6. The results support the hypothesis that input from skin stretched during finger movement contributes to the conscious perception of the movement. Vibration‐evoked muscle afferent input tended to be more reliable than the skin input in producing kinaesthetic illusions, though comparisons of the relative efficacy of the three techniques must be made with caution.

Sustained contractions produced by plateau-like behaviour in human motoneurones

Electrical stimulation over human muscle can generate force directly by activation of motor axons and indirectly by ‘reflex’ recruitment of spinal motoneurones. These experiments were designed to define the properties of the centrally generated ‘reflex’ force, including the optimal stimulus conditions for producing it in tibialis anterior (TA) and triceps surae (TS), and its interaction with volition. Subjects (n= 21) were seated with their foot strapped to an isometric myograph. Surface EMG was recorded from TS and TA. High‐frequency electrical stimulation (100 Hz) of TS and TA with wide pulse widths (1 ms) was most effective to evoke the sustained centrally generated forces. The maximal force evoked by this mechanism during stimulation of TA for 40 s was ∼42 % of that produced by a maximal voluntary contraction. For both muscle groups, ramp increases and decreases in stimulus frequency (from ∼4 to 100 Hz and back to 4 Hz over 6 s) resulted in marked hysteresis in the force‐frequency plot. After a single ‘burst’ of 100 Hz stimulation during prolonged stimulation at 25 Hz, force remained elevated. Repeated bursts often generated progressively larger force increments. These behaviours were abolished by an anaesthetic nerve block proximal to the stimulation site, confirming the central origin for the ‘extra’ force. After a brief voluntary contraction was performed during 25 Hz stimulation, force remained elevated, and this showed some gradation with voluntary contraction amplitude. Sometimes voluntary contractions alone initiated the sustained central motor output. Involuntary contractions often persisted for many seconds after electrical stimulation ceased. These were not terminated by brief inhibitory inputs to the active motoneurones but could be stopped by the voluntary command to ‘relax completely’. Overall, these centrally generated contractions are consistent with activation of plateau potentials in motoneurones innervating the ankle dorsiflexors and plantarflexors. Large forces can be produced through this mechanism. The interaction with volitional drives suggests that plateau behaviour may contribute significantly to the normal output of human motoneurones.

Central Contributions to Contractions Evoked by Tetanic Neuromuscular Electrical Stimulation

Tetanic electrical stimulation applied over human muscle or peripheral nerve generates contractions by depolarizing motor axons beneath the stimulating electrodes. However, the simultaneous depolarization of sensory axons can also contribute to the contractions by the synaptic recruitment of spinal motoneurons. Maximizing this central contribution may be beneficial for reducing muscle atrophy or restoring movement for persons with movement disorders.

Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley.

Neuromuscular electrical stimulation (NMES) generates contractions by depolarising axons beneath the stimulating electrodes. The depolarisation of motor axons produces contractions by signals travelling from the stimulation location to the muscle (peripheral pathway), with no involvement of the central nervous system (CNS). The concomitant depolarisation of sensory axons sends a large volley into the CNS and this can contribute to contractions by signals travelling through the spinal cord (central pathway) which may have advantages when NMES is used to restore movement or reduce muscle atrophy. In addition, the electrically evoked sensory volley increases activity in CNS circuits that control movement and this can also enhance neuromuscular function after CNS damage. The first part of this review provides an overview of how peripheral and central pathways contribute to contractions evoked by NMES and describes how differences in NMES parameters affect the balance between transmission along these two pathways. The second part of this review describes how NMES location (i.e. over the nerve trunk or muscle belly) affects transmission along peripheral and central pathways and describes some implications for motor unit recruitment during NMES. The third part of this review summarises some of the effects that the electrically evoked sensory volley has on CNS circuits, and highlights the need to identify optimal stimulation parameters for eliciting plasticity in the CNS. A goal of this work is to identify the best way to utilize the electrically evoked sensory volley generated during NMES to exploit mechanisms inherent to the neuromuscular system and enhance neuromuscular function for rehabilitation.

Proprioception: peripheral inputs and perceptual interactions.

Much emphasis has been placed on the specific role of specific inputs from muscle, joint and cutaneous afferents in the detection of movement. However, particularly for the hand, multiple inputs from the moving part are likely to be important. This chapter reviews some recent studies which examine the co-operative interaction between the various proprioceptive channels. Proprioceptive control of movement must also take account of the length of the various limb segments, a variable which is independent of muscle lengths and joint angles. Evidence is presented that body image can be affected by the tonic discharge of non-muscle receptors.

Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: triceps surae

Neuromuscular electrical stimulation (NMES) can be delivered over a nerve trunk or muscle belly and both can generate contractions through peripheral and central pathways. Generating contractions through peripheral pathways is associated with a nonphysiological motor unit recruitment order, which may limit the efficacy of NMES rehabilitation. Presently, we compared recruitment through peripheral and central pathways for contractions of the knee extensors evoked by NMES applied over the femoral nerve vs. the quadriceps muscle. NMES was delivered to evoke 10 and 20% of maximum voluntary isometric contraction torque 2-3 s into the NMES (time(1)) in two patterns: 1) constant frequency (15 Hz for 8 s); and 2) step frequency (15-100-15 Hz and 25-100-25 Hz for 3-2-3 s, respectively). Torque and electromyographic activity recorded from vastus lateralis and medialis were quantified at the beginning (time(1)) and end (time(2); 6-7 s into the NMES) of each pattern. M-waves (peripheral pathway), H-reflexes, and asynchronous activity (central pathways) during NMES were quantified. Torque did not differ regardless of NMES location, pattern, or time. For both muscles, M-waves were ∼7-10 times smaller and H-reflexes ∼8-9 times larger during NMES over the nerve compared with over the muscle. However, unlike muscles studied previously, neither torque nor activity through central pathways were augmented following 100 Hz NMES, nor was any asynchronous activity evoked during NMES at either location. The coefficient of variation was also quantified at time(2) to determine the consistency of each dependent measure between three consecutive contractions. Torque, M-waves, and H-reflexes were most variable during NMES over the nerve. In summary, NMES over the nerve produced contractions with the greatest recruitment through central pathways; however, considering some of the limitations of NMES over the femoral nerve, it may be considered a good complement to, as opposed to a replacement for, NMES over the quadriceps muscle for maintaining muscle quality and reducing contraction fatigue during NMES rehabilitation.

Sensory integration in the perception of movements at the human metacarpophalangeal joint

1 These experiments were designed to investigate illusions of movements of the fingers produced by combined feedback from muscle spindle receptors and receptors located in different regions of the skin of the hand. 2 Vibration (100 Hz) applied in cyclic bursts (4 s ‘on’, 4 s ‘off’) over the tendons of the finger extensors of the right wrist produced illusions of flexion‐extension of the fingers. Cutaneous receptors were activated by local skin stretch and electrical stimulation. Illusory movements at the metacarpophalangeal (MCP) joints were measured from voluntary matching movements made with the left hand. 3 Localised stretch of the dorsal skin over specific MCP joints altered vibration‐induced illusions in 8/10 subjects. For the group, this combined stimulation produced movement illusions at MCP joints under, adjacent to, and two joints away from the stretched region of skin that were 176 ± 33, 122 ± 9 and 67 ± 11 % of the size of those from vibration alone, respectively. Innocuous electrical stimulation over the same skin regions, but not at the digit tips, also ‘focused’ the sensation of movement to the stimulated digit. 4 Stretch of the dorsal skin and compression of the ventral skin around one MCP joint altered the vibration‐induced illusions in all subjects. The illusions became more focused, being 295 ± 57, 116 ± 18 and 65 ± 7 % of the corresponding vibration‐induced illusions at MCP joints that were under, adjacent to, and two joints away from the stimulated regions of skin, respectively. 5 These results show that feedback from cutaneous and muscle spindle receptors is continuously integrated for the perception of finger movements. The contribution from the skin was not simply a general facilitation of sensations produced by muscle receptors but, when the appropriate regions of skin were stimulated, movement illusions were focused to the joint under the stimulated skin. One role for cutaneous feedback from the hand may be to help identify which finger joint is moving.

Muscular sense is attenuated when humans move

1 Muscle receptors play an important role in our conscious perception of movement, but there are no published accounts of our ability to detect their signals during different motor tasks. The present experiments introduce a method to test muscular sense when humans move. 2 Muscle receptors were excited by an electrically induced twitch of the right extensor carpi ulnaris muscle. The muscle was stimulated via percutaneously inserted intramuscular electrodes or using surface stimulation through anaesthetized skin. Muscular sense was represented by the ability to detect the twitch and was compared between various tasks and stationary control trials. 3 Three hertz voluntary wrist movements significantly attenuated muscular sense to 37 % of control. This velocity‐dependent attenuation was present over a range of twitch amplitudes suggesting it does not simply reflect a masking of low intensity stimuli. Perceptual ratings of twitch amplitude during fast imposed passive movements were reduced by 40 %, though this did not quite reach statistical significance. However, perceptual ratings of twitches evoked up to 2 s after the termination of the passive movements were significantly different from control. 4 Reaching with the stimulated, but not the contralateral, arm also significantly reduced muscular sense (to 40 %). 5 Attenuation to 58 % of control during cyclic stretching of the skin on the dorsum of the hand showed that signals from peripheral receptors may play a role. Attenuation prior to a single wrist flexion movement indicated that central sources can also contribute. 6 The results are consistent with current findings of a general attenuation of sensory feedback during movement and raise questions regarding the role of muscular sense in movement control.

Ankle position and voluntary contraction alter maximal M waves in soleus and tibialis anterior

Compound muscle action potentials (CMAPs) recorded using surface electrodes are often used to assess the excitability of neural pathways to skeletal muscle. However, the amplitude of CMAPs can be influenced by changes at the recording site, independent of mechanisms within the central nervous system. We quantified how joint angle and background contraction influenced CMAP amplitude. In seven subjects CMAPs evoked by supramaximal transcutaneous electrical stimulation of motor axons (Mmax) were recorded using surface electrodes from soleus and tibialis anterior (TA) at static positions over the full range of ankle movement at 5° intervals. Across subjects the peak‐to‐peak amplitude of Mmax was 155% and 159% larger at the shortest than longest muscle lengths for soleus and TA, respectively. In five subjects the effect of ankle position and voluntary contraction on M‐wave/H‐reflex recruitment curves was assessed in the soleus. Both ankle position and level of contraction significantly influenced Mmax, Hmax, and the Hmax to Mmax ratio, but there were no interactions between the two parameters. These peripheral changes that influence Mmax will also impact other CMAPs such as submaximal M‐waves, H‐reflexes, and responses to transcranial magnetic stimulation. As such, during experimental studies CMAPs evoked at a given joint angle and contraction level should be normalized to Mmax recorded at similar joint angle and contraction strength. Muscle Nerve, 2007