Mechanisms underlying the training effects associated with neuromuscular electrical stimulation.Under appropriate conditions, neuromuscular neuromuscular /neu·ro·mus·cu·lar/ (-mus´ku-ler) pertaining to nerves and muscles, or to the relationship between them. neu·ro·mus·cu·lar adj. 1. electrical stimulation (NMES NMES Neuromuscular Electrical Stimulation NMES National Medical Expenditure Survey ) can cause an increase in strength. [1,2] There is, however, some uncertainty concerning the mechanisms by which NMES produces these changes. [3,4] Are these changes strictly peripheral in nature or, like voluntary exercise, can they involve central processes? Although NMES represents an artificial means of activating muscle that bypasses the processes associated with volition vo·li·tion n. 1. The act or an instance of making a conscious choice or decision. 2. A conscious choice or decision. 3. The power or faculty of choosing; the will. , three lines of evidence suggest that it can induce strength-related neural adaptations [1]: (1) a time course of strength gains that precedes changes in muscle size, (2) a lower requisite training intensity compared with that necessary for voluntary training, and (3) increased strength of the nonexercised contralateral contralateral /con·tra·lat·er·al/ (-lat´er-al) pertaining to, situated on, or affecting the opposite side. con·tra·lat·er·al adj. limb that accompanies the strengthening of the test limb with NMES. These observations caused us to question the mechanisms by which NMES might elicit increases in strength. Neuromuscular electrical stimulation elicits muscle force by initiating action potentials in intramuscular intramuscular /in·tra·mus·cu·lar/ (-mus´ku-ler) within the muscular substance. in·tra·mus·cu·lar adj. Abbr. IM Within a muscle. nerve branches. [5] As with voluntary activation, one of the principal means of varying muscle force with NMES is by altering the number of active motor units. Under most conditions, tests of central nervous system function have indicated that motor units are recruited in a relatively fixed and unalterable order, which seems to depend on the size and biophysical properties of motor neurons Motor neurons Nerve cells that transmit signals from the brain or spinal cord to the muscles. Mentioned in: Electromyography motor neurons, n. and the distribution of synaptic synaptic /syn·ap·tic/ (si-nap´tik) 1. pertaining to or affecting a synapse. 2. pertaining to synapsis. syn·ap·tic adj. Of or relating to synapsis or a synapse. input onto the motor neurons. [6] The order of motor unit activation with NMES, however, depends on the combined effects of axon diameter [7,8] and the distance between the axon and the active electrode. [9,10] These differences in the activation of muscle between voluntary control and NMES can be mimicked by two protocols that recruit different fractions of the motor unit pool; these protocols are the Hoffman reflex (H-reflex) and the direct motor response (M-response). H-reflexes involve activation of large-diameter afferent afferent /af·fer·ent/ (af´er-ent) 1. conveying toward a center. 2. something that so conducts, such as a fiber or nerve. af·fer·ent adj. axons and recruit motor units in an order that goes from smallest to largest, as with volitional vo·li·tion n. 1. The act or an instance of making a conscious choice or decision. 2. A conscious choice or decision. 3. The power or faculty of choosing; the will. activation, and produce relatively slow twitch responses in muscle. In contrast, M-responses, for which a stimulus is delivered to the efferent nerve efferent nerve n. A nerve conveying impulses from the central nervous system to the periphery. Also called centrifugal nerve. , selectively involve faster contracting motor units and produce faster twitch responses in muscle. [11] Based on this distinction in the time course of the twitch response, it is possible to elicit H-reflexes and M-responses in conjunction with NMES in order to determine whether NMES affects the population of activated motor units. The purposes of the study were (1) to compare the time course of the twitch elicited by the H-reflex and the M-response and (2) to determine whether the population of motor units that is activated during an H-reflex is affected by the application of submotor NMES. The first aim was tested by comparing changes in the time to peak twitch force for H-reflexes that were elicited by over-the-nerve stimulation with twitches associated with M-responses that were evoked by over-the-muscle stimulation. The second aim was tested by examining the effect of submotor NMES on the twitch response elicited with an H-reflex. Because the H-reflex involves the activation of motor units in the order from smallest to largest, a change in the time course of the twitch response would suggest an effect of submotor NMES on the recruitment order of motor units. Based on the electrical stimulation literature, we hypothesized that the time to peak twitch force would be less for the M-responses compared with the H-reflexes. Furthermore, we hypothesized that the order of motor unit recruitment Motor unit recruitment is the progressive activation of a muscle by successive recruitment of contractile units (motor units) to accomplish increasing gradations of contractile strength. A motor unit consists of one motor neuron and all of the muscle fibres it contracts. associated with an H-reflex would be altered during submotor NMES because of input to motor neurons from cutaneous cutaneous /cu·ta·ne·ous/ (ku-ta´ne-us) pertaining to the skin. cu·ta·ne·ous adj. Of, relating to, or affecting the skin. Cutaneous Pertaining to the skin. afferents that have been activated by the artificial signal [12,13] and that this effect would be apparent by a change in the time to peak force of the twitch response. Such a difference in the time course of the twitch would suggest that submotor NMES influences the recruitment order associated with volitional activation. These two observations (the time to peak force of the H-reflexes versus the M-responses and the effect of submotor NMES on the time to peak force of the H-reflexes) on the effects of over-the-muscle electrical stimulation on the time to peak force might explain some of the neural adaptations, such as those outlined in the first paragraph, that are associated with NMES. Method The study was based on measurements of force and, on some occasions, electromyographic (EMG EMG abbr. electromyogram Electromyography (EMG) A diagnostic test that records the electrical activity of muscles. ) potentials that were associated with electrically evoked twitch responses. Two types of evoked twitches were used, the H-reflex and the direct M-response. The H-reflex was evoked by passing a graded current across a peripheral nerve that resulted in a twitch response (force) and an associated EMG potential in the test muscle. The H-reflex occurs as a result of excitation of the group 1a afferents and the subsequent activation of motor units in the natural sequence of smallest to largest. [14] The M-response was evoked by passing a graded current between large electrodes placed over each test muscle. The M-response, which involved higher stimulus intensities than the H-reflex, was elicited by direct activation of the motor axons. The H-reflex and the M-response can be distinguished on the basis of the latency from the stimulus to the evoked response e·voked response n. An alteration in the electrical activity of a particular part of the nervous system as a result of receiving a sensory stimulus. . Both the H-reflex and the M-response evoke EMG waveforms and a twitch response in the test muscle. In this study, the focus was on the amplitude and the time-dependent characteristics of the twitch response. Because the time course of the twitch response, such as the time to peak twitch force, represents the summated effect of the many motor units that are activated by the electrical stimulus, variation in the time to peak force indicates changes in the population of motor units contributing to the response. For a group of fast-contracting motor units, such as those activated during an M-response, the time to peak force should be less than that for a group of slow-contracting motor units, such as those activated during an H-reflex. Subjects Twenty-two subjects (15 male, 7 female) volunteered to participate in the study and gave their informed consent on an institutionally approved form. All subjects did not participate in all phases of the project. The subjects ranged in age from 19 to 53 years and had no history of neuromuscular disease Neuromuscular disease is a very broad term that encompasses many diseases and ailments that either directly (via intrinsic muscle pathology) or indirectly (animal muscle in general. Neuromuscular diseases are those that affect the muscles and/or their nervous control. . The two muscle groups tested in this study were the quadriceps femoris Noun 1. quadriceps femoris - a muscle of the thigh that extends the leg musculus quadriceps femoris, quadriceps, quad extensor, extensor muscle - a skeletal muscle whose contraction extends or stretches a body part and the triceps surae. There was no attempt to determine differential activation of the muscles within each group. Stimulation and Recording Techniques The subjects were positioned on a bench, either in a supine position (for quadriceps femoris muscles) or in a prone position (for triceps surae muscles). In the supine position, the hip was placed in full extension, the knee was flexed by 20 to 30 degrees, and both the left and right shanks (lower legs) extended beyond the bench so that the test leg could be aligned with a force transducer transducer, device that accepts an input of energy in one form and produces an output of energy in some other form, with a known, fixed relationship between the input and output. (*1) via an inextensible in·ex·ten·si·ble adj. Not extensible: an inextensible antenna. Adj. 1. inextensible - not extensile nonextensile, nonprotractile strap to measure a knee-extensor force. In this position, the shin of the right leg rested against a strap so that when the quadriceps femoris muscles were stimulated, the leg exerted a force against the strap and the force was measured by the transducer. In the prone position, the hip and knee were placed in full extension and both feet hung over the end of the bench so that they could be connected to the force transducer in order to measure the plantar-flexor force. The ankle was fixed in a position close to neutral (between dorsiflexion dorsiflexion /dor·si·flex·ion/ (dor?si-flek´shun) flexion or bending toward the extensor aspect of a limb, as of the hand or foot. dor·si·flex·ion n. The turning of the foot or the toes upward. and plantar plantar /plan·tar/ (plan´tar) pertaining to the sole of the foot. plan·tar adj. Of, relating to, or occurring on the sole. flexion flexion /flex·ion/ (flek´shun) the act of bending or the condition of being bent. flex·ion n. 1. The act of bending a joint or limb in the body by the action of flexors. 2. ), the position in which the slack in the musculotendinous unit was removed. To measure the plantar-flexor force, the sole of the foot rested against a strap and, when the triceps surae musculature musculature /mus·cu·la·ture/ (mus´kul-ah-cher) the muscular apparatus of the body or of a part. mus·cu·la·ture n. The arrangement of the muscles in a part or in the body as a whole. was stimulated, the foot pushed against the strap and the force was measured with the transducer. Although subject position varied slightly between experiments, the position of each subject was kept constant within each experiment. The submaximal H-reflex and the M-response were elicited by rectangular, monophasic stimulus pulses that were delivered through stimulus-isolation and constant-current units.(*2) For the quadriceps femoris musculature, the current pulses (width=0.5 ms) for the H-reflex were passed across the femoral nerve femoral nerve n. A nerve that arises from the second, third, and fourth lumbar nerves and supplies the muscles and skin of the anterior region of the thigh. , with the cathode (1.5 cm [2]) placed in the femoral triangle femoral triangle n. A triangular space at the upper part of the thigh, bounded by the sartorius and adductor longus muscles and the inguinal ligament. Also called Scarpa's triangle. and the anaode (22 cm [2]) located in the gluteal fold gluteal fold n. A prominent fold on the back of the upper thigh that marks the upper limit of the thigh from the lower limit of the buttock. opposite the cathode. For the triceps surae musculature, the current pulses (width=1.0 ms) for the H-reflex were passed across the posterior tibial nerve, with the cathode located in the popliteal fossa and the anode anode (ăn`ōd), electrode through which current enters an electric device. In electrolysis, it is the positive electrode in the electrolytic cell. anode Terminal or electrode from which electrons leave a system. placed over the superior aspect of the patella patella (pətĕl`ə): see kneecap. . Because it is usually more difficult when passing current across a nerve to elicit an M-response without an H-reflex, M-responses were elicited by activating the intramuscular nerve branches with large carbon electrodes (100 cm [2] and 36 cm [2]) placed over the test muscles (pulse width pulse width Pulse duration Cardiac pacing The duration of a pacing pulse in msecs =1-10 ms). The variation in current pulse width between conditions and subjects was necessary to improve our resolution for grading the stimulus intensity. H-reflexes and M-responses were elicited at several stimulus intensities at which the minimal intensity necessary to elicit a response was defined as the stimulus threshold and stimulus intensity was incremented in fixed steps (one-quarter turns); however, we did not determine the increase in current with each step increment in stimulus intensity. The twitch responses evoked by the nerve stimulation were characterized by the measurement of EMG latency, time to peak force, and peak force. The surface EMG measurements were obtained either from the vastus lateralis vas·tus lat·e·ra·lis n. A muscle with origin from the posterior ridge of the femur as far as the greater trochanter, with insertion into the tibia, with nerve supply from the femoral nerve, and whose action extends the leg. and vastus medialis vastus me·di·a·lis n. A muscle with origin from the shaft of the femur, with insertion into the tibial tuberosity, with nerve supply from the femoral nerve, and whose action extends the leg. muscles or from the soleus so·le·us n. A muscle with origin from the head and shaft of the fibula, the medial margin of the tibia, and the tendinous arch passing between the tibia and fibula, with insertion into the tuberosity of the calcaneus, with nerve supply from the tibial and lateral gastrocnemius muscles using standardized bipolar electrode arrangements (silver-silver chloride, 8-mm diameter; interelectrode distance=3 cm; band-width=10 Hz-5 kHz).(*3) The recording electrodes were positioned as follows: (1) vastus medialis muscle--one fifth of the distance from the medial margin of the knee to the anterior superior iliac spine The anterior superior iliac spine (ASIS) is an important landmark of surface anatomy. It refers to the anterior extremity of the iliac crest of the pelvis, which provides attachment for the inguinal ligament and the sartorius muscle. , (2) vastus lateralis muscle--one third of the distance from the superior pole of the patella to the greater torchanter, (3) soleus muscle--approximately 4 cm above the point at which the two heads of the gastrocnemius muscle join the Achilles tendon Achilles tendon n. The large tendon connecting the heel bone to the calf muscle of the leg. Also called calcanean tendon, heel tendon. , and (4) lateral gastrocnemius gastrocnemius /gas·troc·ne·mi·us/ (gas?tro-ne´me-?s) (gas?trok-ne´me-us) see under muscle. gas·troc·ne·mi·us n. pl. muscle--one third of the distance from the head of the fibula fibula (fĭb`yələ): see leg. to the calcaneus calcaneus /cal·ca·ne·us/ (kal-ka´ne-us) pl. calca´nei [L.] heel bone; the irregular quadrangular bone at the back of the tarsus. calca´nealcalca´nean cal·ca·ne·us or cal·ca·ne·um n. . The EMG waveform could not be measured when the M-response was elicited by electrodes placed over the muscle or when NMES was used to stimulate the cutaneous afferents. In subsequent work (MH Trimble, unpublished observations) with over-the-muscle stimulation, a short-latency (2-4-ms) EMG wave was seen at stimulus intensities from threshold to supramaximum with no longer-latency waves observed. This finding indicates that the response was due to excitation of efferent efferent /ef·fer·ent/ (ef´er-ent) 1. conveying away from a center. 2. something that so conducts, as an efferent nerve. ef·fer·ent adj. branches and was not a reflex-mediated response. The EMG and force signals were displayed on oscilloscopes(*4) and recorded on FM tape.(*5) In addition to these standard tests of the H-reflex and the M-response, H-reflexes were elicited before, during, and after a 3-minute conditioning period with submotor NMES. The NMES consisted of a sinusoidal sinusoidal /si·nus·oi·dal/ (si?nu-soi´dal) 1. located in a sinusoid or affecting the circulation in the region of a sinusoid. 2. shaped like or pertaining to a sine wave. high-frequency (3.3-kHz) current that was modulated to give bursts of stimuli at a rate of 50 per second.(*6) The stimulus was delivered through two large electrodes (either 100 cm [2] or 36 cm [2]) that were located over the belly of the test muscle. The stimulus intensity was arbitrary and subthreshold sub·thresh·old adj. Psychology Not strong enough to be perceived or to produce a response. Used of a stimulus. for a motor response (submotor), yet sufficient to elicit a tingling tin·gle v. tin·gled, tin·gling, tin·gles v.intr. 1. To have a prickling, stinging sensation, as from cold, a sharp slap, or excitement: tingled all over with joy. sensation that was presumably pre·sum·a·ble adj. That can be presumed or taken for granted; reasonable as a supposition: presumable causes of the disaster. associated with cutaneous afferent feedback to the motor neuron pool In muscle physiology, a motor neuron pool is a collection of motor neurons that innervate a single muscle. . Protocol Once a subject was positioned on the bench with the leg connected to the force transducer and the EMG electrodes attached, one of the muscle groups of the subject was tested with one of three protocols: (1) H-reflex recruitment curve, (2) M-response recruitment curve, and (3) NMES. For the H-reflex recruitment curve protocol, the stimulus strength was varied over several increments to elicit H-reflexes that varied in amplitude, but that elicited, at most, a minimal M-response. The M-response was kept small (low stimulus intensity) in order to limit the activation to slower-contracting motor units. Five responses were elicited at each stimulus strength. These data were intended to show how the H-reflex-elicited twitch responses (ie, time to peak force and peak force) varied as a function of stimulus strength. For the M-response recruitment curve protocol, the same protocol was used to elicit M-responses of varying magnitude and to indicate the association between the M-response-elicited twitch responses and stimulus strength. For the NMES protocol, 20 H-reflexes were elicited before, during, and after the 3 minutes of submotor NMES. For all three protocols, the H-reflexes and M-responses were elicited at a rate of one every 7 seconds. Data Analysis The dependent variables in this design were time to peak force and peak force of the twitch responses associated with the H-reflexes and the M-responses (Fig. 1). The reliability of the twitches for each type of response in the two test muscles was assessed by determining Pearson Product-Moment Correlation Coefficients (r) between stimulus intensity and twitch response parameters across trials; correlation coefficients close to 1.00 for each subject would suggest a reliable association between stimulus intensity and twitch response. The subjects' EMG activity was assessed qualitatively in order to determine the relative contributions of the H-reflex and the M-response to the twitch force during the recruitment protocols and to determine whether the stimulus remained relatively constant before and after the NMES protocol. A one-factor analysis of variance (ANOVA anova see analysis of variance. ANOVA Analysis of variance, see there ) for repeated measures was performed on each dependent variable in each of the three protocols. For the H-reflex and M-response recruitment protocols, stimulus intensity was the independent variable. This analysis was designed to determine whether time to peak force and peak force changed as stimulus intensity was varied. When the ANOVA detected a significant effect, a trend analysis was conducted to determine the extent to which the association between time to peak force or peak force and stimulus intensity was linear. For the ANOVA, stimulus intensity was normalized with respect to the threshold intensity and then grouped by step increments (one-quarter turn on the constant current stimulating unit) of stimulus intensity. Thus, in Figures 2 and 3, the values on the abscissa abscissa: see Cartesian coordinates. (mathematics) abscissa - The horizontal or x coordinate on an (x, y) graph; the input of a function against which the output is plotted. The vertical or y coordinate is the "ordinate". See Cartesian coordinates. represent five current steps on the stimulator. In the submotor NMES protocol, the two force parameters (ie, time to peak force and peak force) were examined before, during, and after the application of NMES. Tables 1 and 2 contain the means and standard errors of the time to peak force and the peak force for the subjects. The alpha level of acceptance was set at .05 for all protocols. Results The data consist of baseline values for twitch responses associated with H-reflexes and M-responses and the effect of submotor NMES on the H-reflex-elicited twitch responses. The trial-to-trial reliability coefficients (r values) across subjects for the peak twitch force and the time to peak force associated with the H-reflexes and the M-responses ranged from .90 to .99. H-Reflex Recruitment Curve The H-reflex--elicited twitches in the two muscle groups were similar in peak force and time to peak force. In the quadriceps femoris musculature, peak force for all subjects ranged from 19 to 195 N (X[+ or -]SE=88.9[+ or -]36.8) and time to peak force varied from 65 to 100 milliseconds (74.2[+ or -]7.4), whereas for the triceps surae musculature, the ranges of peak force and time to peak force were 17 to 83 N (47.2[+ or -]21.9) and 56 to 102 milliseconds (80.6[+ or -]12.3), respectively. Peak force for the H-reflex occurred prior to the appearance of an M-response, which is known to cause the H-reflex force to diminish. The magnitude of the peak twitch force increased and the time to peak twitch force decreased as the H-reflex stimulus intensity increased. These changes were apparent in both the superimposed su·per·im·pose tr.v. su·per·im·posed, su·per·im·pos·ing, su·per·im·pos·es 1. To lay or place (something) on or over something else. 2. twitch responses (Fig. 1) and in the values averaged across subjects (Figs. 2, 3) for the two test muscles. The data were derived from 11 subjects for the quadriceps femoris musculature and from 4 subjects for the triceps surae musculature. The ANOVAs indicated that both the time to peak force and the peak force changed significantly with stimulus strength (P<.001). Trend analyses revealed that the changes in time to peak force and peak force were linearly related to stimulus intensity; 91% to 99% of the variance was accounted for by the linear function. Time to peak force and peak twitch force of the H-reflexes were negatively correlated (r=-.85 to -.99), indicating that time to peak force decreased as peak force increased. M-Response Recruitment Curve As with the H-reflexes, the magnitude of the peak twitch force increased with the M-response stimulus intensity (Fig. 3). In contrast to the H-reflexes, however, the time to peak twitch force increased with stimulus strength (Figs. 1, 2). The ANOVAs, based on 11 subjects for the quadriceps femoris musculature and 14 subjects for the triceps surae musculature, indicated that time to peak force and peak force varied significantly (P<.05) across stimulus intensity. As with the H-reflexes, trend analyses revealed a dominant linear association (94%-96% of the variance) between the force measurements and stimulus intensity. The Pearson product-moment [TABULAR DATA OMITTED] [TABULAR DATA OMITTED] correlation between peak force and time to peak force ranged from .89 to .99 for the M-responses of the quadriceps femoris musculature and from .51 to .99 for the triceps surae musculature, indicating that increases in time to peak force accompanied increases in peak force. Submotor Neuromuscular Electrical Stimulation The overlapping EMG records shown in Figure 4, which include 20 responses before and 20 responses after submotor NMES, indicated that it was possible to elicit stable submaximal (50%-75%) H-reflexes in both the quadriceps femoris and triceps surae muscle groups. Prior to application of the submotor NMES, the twitch responses for the quadriceps femoris musculature (n=7) and the triceps surae musculature (n=2) had time to peak forces (mean[+ or -]SE of the group data) of 77.2[+ or -]2.0 and 91.6[+ or -]3.7 milli-seconds, respectively, and peak forces of 111.9[+ or -]18.8 and 53.3[+ or -]29.5 N, respectively (Tabs. 1, 2). Most of the variability could probably be accounted for by between-subject differences such as muscle-fiber length and characteristics, elastic properties of non-contractile tissue, and the degree of subject fixation to the apparatus. The 3-minute conditioning period of sub-motor NMES over the bellies of the test muscles did not alter the peak twitch force, but is did significantly shorten the time to peak twitch force during NMES (P<.05). Time to peak force decreased by an average of 8 milliseconds in the quadriceps femoris musculature and by an average of 11 milliseconds in the triceps surae musculature during submotor NMES. These values represented an 11% (average) decrease in contraction time during the submotor NMES and can be contrasted to the 2% variability in time to peak force when comparing the before and after NMES conditions. Although the peak force varied 4%, on average, during the three conditions, the magnitude and direction of this variance was not associated with super-imposition of the NMES, as indicated by the ANOVA. This decrease in time to peak force was interpreted as the activation of a faster-contracting population of motor units during submotor NMES. Furthermore, because the values before and after submotor NMES were not significantly different, the decrease in the time to peak twitch force represented a transient effect. Discussion The objective of this study was to determine whether the recruitment order of motor units elicited by over-the-muscle electrical stimulation was different from that achieved with voluntary activation in human subjects. One unique feature of the study was that, rather than assess recruitment order on the basis of a pair-wise comparison of motor units, we examined the effect on populations of motor units. Along with previous literature, the results indicate two ways in which electrical stimulation can later the recruitment order of motor units in human subjects. First, as has been shown in animal models [7,8] but not convincingly in humans, [15] graded electrical stimulation elicits M-responses of progressively increasing time to peak force and peak force. This association suggests that as the stimulus intensity was increased in our study, motor units with a slower contraction time were progressively recruited, which resulted in a lengthening in the time to peak force of the M-response. In contrast, an increase in the stimulus strength for the H-reflexes resulted in a decrease in the time to peak force. These findings are consistent with the recruitment of progressively faster-contracting motor units, as occurs under the condition of voluntary activation. Thus, direct activation of the motor axons by electrical stimulation, as occurs with NMES, produces a recruitment order of motor units that is different from the order used during voluntary exercise. [16] Second, activation of cutaneous afferents has been shown to alter the recruitment threshold of motor units particpating in voluntary and reflex muscle contractions in both humans [11] and animals. [12] The results of our study extend these observations by indicating that NMES at an intensity below the motor threshold can alter the population of motor units that is activated during the H-reflex. Because the H-reflex is a labile labile /la·bile/ (la´bil) 1. gliding; moving from point to point over the surface; unstable; fluctuating. 2. chemically unstable. la·bile adj. 1. response that is readily influenced by movement of the stimulating electrode, remote muscle activity (ie, Jendrassik effects), and variations in spinal cord spinal cord, the part of the nervous system occupying the hollow interior (vertebral canal) of the series of vertebrae that form the spinal column, technically known as the vertebral column. excitability excitability readiness to respond to a stimulus; irritability. , the appearance of overlapping EMG responses is regarded as evidence that the H-reflex stimulus remained constant before and after the NMES. Furthermore, even minor variations in the responses would have been accentuated by the bipolar measurement of EMG activity that was used in this study. The consistent EMG response before and after the submotor NMES suggests that the current passed acriss the Peripheral nerve of each test muscle remained relatively constant during the NMES. The activation of a different population of motor units during the submotor NMES was apparent by the change in the time to peak force for the twitches elicited by the H-reflex before, during, and after the submotor NMES. The decrease in the time to peak force during submotor NMES was interpreted as the activation of a faster-contracting population of motor units. Thus, cutaneous afferent input, which occurs with NMES, can alter the population of motor units that is activated by voluntary and reflex means. The literature suggests that electrical stimulation of nerve or muscle can alter either the recruitment order of motor units or the population of motor units that is activated by a stimulus. It seems that these changes are the consequence of differences in efferent axon excitability and differential feedback effects from cutaneous afferents. With regard to efferent axon excitability, the largest efferent axons are the most excitable excitable /ex·ci·ta·ble/ (ek-sit´ah-b'l) irritable (1). ex·cit·a·ble adj. 1. Capable of reacting to a stimulus. Used of a tissue, cell, or cell membrane. 2. to electrical stimulation, whereas among the motor neuron pool, the motor neurons with the smallest somas are generally considered to be the most excitable to synaptic excitatory ex·ci·ta·tive or ex·ci·ta·to·ry adj. Causing or tending to cause excitation. Adj. 1. excitatory - (of drugs e.g. input. Most inputs to a motor neuron pool tend to activate motor neurons in the order of smallest to largest. [6,7] However, it appears possible to preferentially activate groups of faster-contracting motor units, either with feedback from cutaneous afferents [11,12] or from other sources. [17] The results of our study indicate that over-the-muscle electrical stimulation elicits an M-response that has a relatively fast (compared with the H-reflex) contraction time and that submotor NMES can alter the population of motor units that is activated during an H-reflex. These two observations probably represent the mechanisms by which NMES-induced therapeutic effects may differ from those associated with volitional activation. Clinical Implications One of the most surprising observations in the NMES literature is the report that it is possible to induce increases in strength with minimal training intensities, [18,19] much less than the intensities needed for voluntary training. [20] This difference in the requisite training intensity is probably due to different motor units that may have been activated under the two training conditions. Perhaps NMES induces strength increases in higher threshold motor units that can normally be trained only at high intensities in voluntary conditions. Consistent with this rationale, some reports [21,22] in the literature have indicated that the strengthening of hypotrophic muscle is more easily achieved with NMES than with voluntary exercise. Complete activation of hypotrophic muscle may not be possible voluntarily, especially following a decrease in motor neuron motor neuron n. A neuron that conveys impulses from the central nervous system to a muscle, gland, or other effector tissue. Motor neuron excitability. Neuromuscular electrical stimulation, however, may bypass these deficiencies and cause an increase in motor neuron excitability, both by direct activation of larger motor units [16] and by the facilitatory effect of cutaneous afferent feedback on large motor neurons. Conclusion The percutaneous application of electrical stimulation to the limbs of human subjects, as compared with volitional activation, can alter the recruitment order of motor units and the motor unit population that is activated by a given stimulus. These alterations seem to depend on two distinct mechanisms, one involving direct activation of large efferent axons and the other depending on the feedback effects of cutaneous afferents. The results obtained in this study indicate that over-the-muscle electrical stimulation activates faster-contracting motor units and that submotor NMES provides cutaneous feedback that alters the population of motor units activated during an H-reflex. By these means, it appears possible to preferentially activate faster-contracting motor units, perhaps those that are normally only active at high exercise intensities under voluntary conditions. This selectivity can be a useful adjunct to various rehabilitation interventions. One example would include situations in which strong muscle contractions would be detrimental to an injured extremity. Neuromuscular electrical stimulation, either in conjunction with or in alternation alternation /al·ter·na·tion/ (awl?ter-na´shun) the regular succession of two opposing or different events in turn. alternation of generations metagenesis. with voluntary exercise, may provide a more effective means of training high threshold motor units. M Trimble, MS, PT, is a graduate student, Department of Kinesiology, Indiana University, Bloomington, IN 47405. R Enoka, PhD, is Associate Professor, Department of Exercise and Sport Sciences, University of Arizona (body, education) University of Arizona - The University was founded in 1885 as a Land Grant institution with a three-fold mission of teaching, research and public service. , Tucson, AZ 85721 (USA). Address correspondence to Dr Enoka. This study was completed in partial fulfillment of the requirements for Mr Trimble's Master of Science degree in Exercise Science at the University of Arizona and was supported by the Motor Control Training Program (USPHS USPHS United States Public Health Service. USPHS abbr. United States Public Health Service NS 07309). This article was presented at the 12th Annual Meeting of the American Society of Biomechanics, September 28-30, 1988, Champaign, IL. This study was approved by the University of Arizona Institutional Review Board. This article submitted November 21, 1989, and was accepted November 14, 1990. (*) Barnhill Three Inc, 7319 Stetson Dr, Scottsdale, AZ 85251. (**) Grass Instrument Co, 101 Old Colony Ave, PO Box 516, Quincy, MA 02169. (***) Coulbourn Instruments, PO Box 2251, Lehigh Valley, PA 18001. (****) Tektronix Inc, Howard Vollum Industrial Park, PO Box 500, Beaverton, OR 97077. (*****) Honeywell 7600, Service Associates, 10471 Roselle Roselle (rōzĕl`), borough (1990 pop. 20,314), Union co., NE N.J.; set off from Linden 1890 and inc. 1894. Chiefly residential, the borough has some industry. St, San Diego, CA 92121. (******) Electrostim USA Ltd, Div of Promatek Medical Inc, 1851 Black Rd, Joliet, IL 60435. References [1] Enoka RM. Muscle strength and its development: new perspectives. Sports Med. 1988;6:146-168. [2] Delitto A, Brown M, Strube MJ, et al. Electrical stimulation of quadriceps femoris in an elite weight lifter weight·lift·er or weight lift·er n. One who lifts heavy weights for exercise or in an athletic competition. weight lifter n → levantador(a) m/f de pesas : a single subject experiment. Int J Sports Med. 1989;10:187-191. [3] Delitto A, Snyder-Mackler L. Two theories of muscle strength augmentation using percutaneous electrical stimulation. Phys Ther. 1990;70:158-164. [4] Knaflitz M, Merletti R, DeLuca CJ. Inference of motor unit recruitment order in voluntary and electrically elicited contractions. J Appl Physiol. 1990;68:1657-1667. [5] Hultman E, Sjoholm H, Jaderholm-Ek I, Krynicki J. Evaluation of methods for electrical stimulation of human skeletal muscle in situ In place. When something is "in situ," it is in its original location. . Pflugers Arch. 1983;398:139-141. [6] Binder MD, Mendel LM. The Segmental Motor System. London, England: Oxford University Press; 1990. [7] Clamann HP, Gillies JD, Skinner RD, Henneman E. Quantitative measures of output of a motoneuron motoneuron /mo·to·neu·ron/ (mot?o-nldbomacr´on) motor neuron; a neuron having a motor function; an efferent neuron conveying motor impulses. pool during monosynaptic monosynaptic /mono·syn·ap·tic/ (-si-nap´tik) pertaining to or passing through a single synapse. mon·o·syn·ap·tic adj. Having a single neural synapse. reflexes. J Neurophysiol. 1974;37:1328-1337. [8] Eccles JC, Eccles RM, Lundberg A. The action potentials of the alpha motoneurones supplying fast and slow muscles. J Physiol (Lond). 1958;142:275-291. [9] gorman PH, Mortimer JT. The effect of stimulus parameteres on the recruitment characteristics of direct nerve stimulation. IEEE (Institute of Electrical and Electronics Engineers, New York, www.ieee.org) A membership organization that includes engineers, scientists and students in electronics and allied fields. Trans Biomed Eng. 1983;30:407-414. [10] McComas AJ, Fawcett PRW "Parents are watching." See digispeak. , Campbell MJ, Sica REP. Electrophysiological estimation of the number of motor units within a human muscle. J Neurol Neurosurg Psychaitry. 1971;34:121-131. [11] Buchthal F, Schmalbruch H. Contraction times of reflexly activated motor units and excitability cycle of the H-reflex. Prog Brain Res. 1976;44:367-376. [12] Garnett R, Stephens JA. Changes in the recruitment threshold of motor units produced by cutaneous stimulation in man. J Physiol (Lond). 1981;311:463-473. [13] Kanda K, Burke RE, Walmsley B. Differential control of fast and slow twitch motor units in the decerebrate decerebrate /de·cer·e·brate/ (-ser´e-brat) to eliminate cerebral function by transecting the brain stem or by ligating the common carotid arteries and basilar artery at the center of the pons; an animal so prepared, or a brain-damaged cat. Exp Brain Res. 1977;29:57-74. [14] Magladery JW, McDougal DB. Electrophysiological studies of nerve and reflex activity in normal man, 1: identification of certain reflexes in the electromyogram e·lec·tro·my·o·gram n. Abbr. EMG A graphic record of the electrical activity of a muscle as recorded by an electromyograph. Electromyogram (EMG) and the conduction velocity of peripheral nerve fibres. Bull Johns Hopkins Hosp. 1950;86:265-290. [15] Brown WF, Kadrie HA, Milner-Brown HS. Rank order of recruitment of motor units with graded stimulatiion of median or ulnar nerves in normal subjects and in patients with entrapment neuropathies. In: Desmedt JE, ed. Motor Unit Types, Recruitment and Plasticity in Health and Disease. Basel, Switzerland: S Karger AG, Medical and Scientific Publishers; 1981:319-330. [16] Sinacore DR, Delitto A, King DS, Rose SJ. Type II fiber activation with electrical stimulation: a preliminary report. Phys Ther. 1990;70:416-422. [17] Burke RE, Jankowska E, ten Bruggencate G. A comparison of peripheral and rubrospinal synaptic input to slow and fast twitch motor units of triceps surae. J Physiol (Lond). 1970;207:709-732. [18] Laughman RK, Youdas JW, Garrett TR, Chao EYS EYS Energy Search, Inc. (former stock symbol) EYS Electrical Y Seal . Strength changes in the normal quadriceps femoris muscle as a result of electrical stimulation. Phys Ther. 1983;63:494-499. [19] Stefanovska A, Vodovnik L. Change in muscle force following electrical stimulation. Scand J Rehabil Med. 1985;17:141-146. [20] McDonagh MJN MJN Mead Johnson Nutritionals , Davies CTM CTM Continuum (gaming) CTM Community Trade Mark (Europe) CTM Cisco Transport Manager CTM Confederacion de Trabajadores de Mexico (Spanish: Confederation of Mexican Workers) . Adaptive response of mammalian skeletal muscle to exercise with high loads. Eur J Appl Physiol. 1984;52:139-155. [21] Godfrey CM, Jayawardena A, Welsh P. Comparison of electro-stimulation and isometric exercise isometric exercise n. Exercise performed by the exertion of effort against a resistance that strengthens and tones the muscle without changing the length of the muscle fibers. in strengthening the quadriceps muscle. Physiotherapy Canada. 1979;31:265-267. [22] Williams RA, Morrissey MC, Brewster CE. The effect of electrical stimulation on quadriceps strength and thigh circumference in meniscectomy men·is·cec·to·my n. Excision of a meniscus, usually from the knee joint. meniscectomy (men´isek´t patients. Journal of Orthopaedic and Sports Physical Therapy. 1986;8:143-146. |
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