Human motor compensations for thixotropy-dependent changes in resting wrist joint position after large joint movements.

AIM: Resting tension of relaxed skeletal muscle fibres held at a given length varies with the immediate previous history of length changes and contractions. The primary aim of this study was to explore the motor control consequences of this history-dependency in healthy subjects. METHODS: Angular position and passive torque were recorded from the intact wrist joint. Integrated surface electromyography (IEMG) was recorded from wrist extensor and flexor muscles. RESULTS: In relaxed subjects, wrist joint position was displaced towards dorsiflexion after a single high-amplitude dorsiflexion movement combined with a strong flexor/extensor co-contraction (dorsiflexion conditioning), whereas after volarflexion conditioning there was a shift towards volarflexion. These after-effects could be abruptly cancelled by short periods ( approximately 5 s) of rapid flapping hand movements or forceful isometric co-contractions, findings indicative of muscle thixotropy. The IEMG-evaluated motor after-effects were as follows. A slowly subsiding wrist flexor contraction was needed to restore and maintain the original resting wrist position after dorsiflexion conditioning whereas a slowly subsiding extensor contraction was needed for the same goal after volarflexion conditioning. Furthermore, ongoing wrist extensor IEMG activity required to actively hold the wrist in a moderate dorsiflexed position or to resist a constant volar torque at resting position was temporarily reduced after dorsiflexion conditioning and enhanced (not significantly) after volarflexion conditioning. CONCLUSION: The results provide evidence that during voluntary maintenance of a desired wrist joint position the motor commands to the position-holding muscles are unconsciously adjusted to compensate for thixotropy-dependent variations in the resting tension of the muscles.

Human motor control consequences of thixotropic changes in muscular short-range stiffness.

1. The primary aim of the present study was to explore whether in healthy subjects the muscle contractions required for unrestrained voluntary wrist dorsiflexions are adjusted in strength to thixotropy-dependent variations in the short-range stiffness encountered in measurements of passive torque resistance to imposed wrist dorsiflexions. 2. After a period of rest, only the first movement in a series of passive wrist dorsiflexions of moderate amplitude exhibited clear signs of short-range stiffness in the torque response. During analogous types of voluntary movements, the extensor EMG during the first movement after rest showed a steep initial rise of activity, which apparently served to compensate for the short-range stiffness. 3. The passive torque resistance to minute repetitive wrist dorsiflexions (within the range of short-range stiffness) was markedly reduced after various types of mechanical agitation. During analogous low-amplitude voluntary wrist dorsiflexions the extensor EMG signals were weaker after than before agitation. 4. Mechanical agitation also led to enhancement of passive dorsiflexion movements induced by weak constant torque pulses. In an analogous way, the movement-generating capacity of weak voluntary extensor activations (as determined by EMG recordings) was greatly enhanced by mechanical agitation. 5. The signals from a force transducer probe pressed against the wrist flexor tendons--during passive wrist dorsiflexions--revealed short-range stiffness responses which highly resembled those observed in the torque measurements, suggesting that the latter to a large extent emanated from the stretched, relaxed flexor muscles. During repetitive stereotyped voluntary wrist dorsiflexions, a close correspondence was observed between the degree of short-range stiffness as sensed by the wrist flexor tension transducer and the strength of the initial extensor activation required for movement generation. 6. The results provide evidence that the central nervous system in its control of voluntary movements takes account of and compensates for the history-dependent degree of inherent short-range stiffness of the muscles antagonistic to the prime movers.

Thixotropy of rib cage respiratory muscles in normal subjects.

In this study, we searched for signs of thixotropic behavior in human rib cage respiratory muscles. If rib cage respiratory muscles possess thixotropic properties similar to those seen in other skeletal muscles in animals and humans, we expect resting rib cage circumference would be temporarily changed after deep rib cage inflations or deflations and that these aftereffects would be particularly pronounced in trials that combine conditioning deep inflations or deflations with forceful isometric contractions of the respiratory muscles. We used induction plethysmography to obtain a continuous relative measure of rib cage circumference changes during quiet breathing in 12 healthy subjects. Rib cage position at the end of the expiratory phase (EEP) was used as an index of resting rib cage circumference. Comparisons were made between EEP values of five spontaneous breaths immediately before and after six types of conditioning maneuvers: deep inspiration (DI); deep expiration (DE); DI combined with forceful effort to inspire (FII) or expire (FEI); and DE combined with forceful effort to inspire (FIE) or expire (FEE), both with temporary airway occlusion. The aftereffects of the conditioning maneuvers on EEP values were consistent with the supposition that human respiratory muscles possess thixotropic properties. EEP values were significantly enhanced after all conditioning maneuvers involving DI, and the aftereffects were particularly pronounced in the FII and FEI trials. In contrast, EEP values were reduced after DE maneuvers. The aftereffects were statistically significant for the FEE and FIE, but not DE, trials. It is suggested that respiratory muscle thixotropy may contribute to the pulmonary hyperinflation seen in patients with chronic obstructive pulmonary disease.

Postural after-contractions in man attributed to muscle spindle thixotropy.

1. It is an old observation that non-volitional arm abduction movements accompanied by a sensation of arm lightness often occur as an after-effect following forceful voluntary arm abductor contractions against a restraint. In the present study we have tested the hypothesis that such non-volitional, so-called 'postural after-contractions' are tonic reflex responses to an enhanced resting discharge in primary muscle spindle afferents which in turn is a consequence of thixotropy-dependent enhanced stiffness of intrafusal muscle fibres. 2. Results obtained in ten volunteers show that the arm abductor after-contraction phenomenon in man is most readily evoked by a type of conditioning procedure which in various respects mimics the procedure proven in animal experiments to be particularly effective in producing thixotropy-dependent excitation of primary spindle endings. 3. It is also shown that changes in arm abductor intramuscular temperature affect the strength of the after-contractions in a direction predicted by the thixotropy hypothesis. 4. Attention is drawn to several similarities between the after-contraction phenomenon with accompanying sensory illusions and the tonic reflex responses and illusions that can be induced when primary spindle endings are excited by muscle vibration. 5. The results support our hypothesis that postural after-contractions are induced by activity in primary muscle spindle afferents as a consequence of thixotropic properties of intrafusal muscle fibres. Central excitability changes following the conditioning voluntary effort may contribute to the phenomenon.

Effects of preceding movements and contractions on the tonic vibration reflex of human finger extensor muscles.

The vibration sensitivity of feline muscle spindle endings is known to vary as a result of preceding muscle conditioning manoeuvres. If similar after-effects occur in man they should be expected to influence the strength of the tonic vibration reflex (TVR). To study this issue, vibration was applied over the finger extensor tendons of 11 volunteers who actively held their fingers in a semi-extended position. The TVR, measured as electromyographic responses and angular deflections at the metacarpophalangeal joints, was found to be stronger when the extensors prior to the test had been contracted in a shortened position than when they had been contracted in a stretched position. This difference was reduced when the vibration stimulus was preceded by a strong extensor contraction in the test position. The antigravity extensor EMG activity required to keep the fingers in the test position was weaker when the conditioning contraction was performed at a short muscle length than when it was performed at a long muscle length. The variations in magnitude of the TVR can be attributed to 'thixotropic' properties of intrafusal muscle fibres, resulting in a slack following conditioning at a long muscle length. The different EMG levels required for position holding can be explained by similar properties of extrafusal muscle fibres. In conclusion, the results demonstrate the importance of taking the 'history of movement' into account in the design of all TVR studies.

Reduced servo-control of fatigued human finger extensor and flexor muscles.

1. In healthy human subjects holding the index finger semi-extended at the metacarpophalangeal joint against a moderate load, electromyographic (EMG) activity was recorded from the finger extensor and flexor muscles during different stages of muscle fatigue. The aim was to study the effect of muscle fatigue on the level of background EMG activity and on the reflex responses to torque pulses causing sudden extensor unloadings. Paired comparisons were made between the averaged EMG and finger deflection responses under two conditions: (1) at a stage of fatigue (following a sustained co-contraction) when great effort was required to maintain the finger position, and (2) under non-fatigue conditions while the subject tried to produce similar background EMG levels to those in the corresponding fatigue trials. 2. Both the unloading reflex in the extensor and the concurrent stretch reflex in the flexor were significantly less pronounced and had a longer latency in the fatigue trials. Consequently, the finger deflections had a larger amplitude and were arrested later in the fatigue trials. 3. It is concluded that--with avoidance of 'automatic gain compensation', i.e. reflex modifications attributable to differences in background EMG levels--the servo-like action of the unloading and stretch reflexes is reduced in fatigued finger extensor and flexor muscles.

Conductivity ratios of the scalp-skull-brain head model in estimating equivalent dipole sources in human brain.

The dipole tracing (DT) method estimates the position and vector dipole moment of an equivalent current dipole by minimizing the mean squared error of the dipole potentials at the surface electrode positions. In the scalp-skull-brain/DT (SSB/DT) method, which we have developed, the head model consists of three compartments of uniform conductors corresponding to the scalp, skull and brain. The accuracy of the calculations are mainly dependent on the ratios of the conductivities of the three compartments. The best result was obtained with the conductivity ratios of 1:1/80:1 for the scalp, skull and brain compartments, respectively.

After-effects on stiffness and stretch reflexes of human finger flexor muscles attributed to muscle thixotropy.

1. While the subject maintained a weak contraction in his finger flexor muscles, holding the metacarpophalangeal joints in 45 deg flexion, test torque pulses were applied which caused rapid finger extension movements and electromyographic (EMG) stretch reflex responses. Before each test pulse the fingers were passively flexed or extended ('post-short' and 'post-long' trials) for about 10 s. The EMG and joint deflection responses in the two types of trial were compared after averaging. 2. In the 'post-long' trials, the EMG reflex response showed a comparative increase in latency, with a reduction of the short-latency (M1) component and an enhancement of the medium-latency (M2) component. 3. The angular deflections were larger, and the turning points of the deflections, which indicated the start of the mechanical reflex responses, occurred later in the 'post-long' trials. These differences were not seen when the torque pulse was immediately preceded by a strong, brief isometric finger flexor contraction in the test position. 4. Immediately following the return to the test position the background finger flexor EMG activity was larger in the 'post-long' trials, a difference which gradually subsided over 15-20 s. A strong, brief contraction in the test position also eliminated this inter-trial difference. 5. The results are interpreted as manifestations of thixotropic after-effects in intra- and extrafusal muscle fibres. It is proposed that the M1 component of the stretch reflex is largely a response to the 'initial burst' of impulses in primary spindle afferents.(ABSTRACT TRUNCATED AT 250 WORDS)

The fusimotor system. Its role in fatigue.

Several lines of evidence point to an important role of the fusimotor system in the "muscle-wisdom" phenomenon during peripheral fatigue of some human voluntary contractions: 1) muscle afferents provide a net amplification of skeletomotor output, with the only known afferent species capable of this being the muscle spindle; 2) muscle spindle firing rates decline during constant-force voluntary contractions, so fusimotor support to skeletomotor output decreases; 3) this waning support can be offset by application of high-frequency vibration to the fatiguing muscle, which excites spindle endings; and 4) the progressive decline in motor unit firing rates during maximal voluntary contractions is abolished by blocking muscle afferent inputs, and it is argued that, at least in the initial stages of a contraction, this must be due to a progressive withdrawal of spindle support.

Location of electric current sources in the human brain estimated by the dipole tracing method of the scalp-skull-brain (SSB) head model.

Using a realistic, 3-shell head model including the scalp (S), skull (S) and brain (B) with conductivity ratios of 1:1/80:1, respectively, the electrical activity in the human brain recorded by conventional electroencephalography was approximated by 1 or 2 equivalent current dipoles. The dipole locations and vector moments were estimated by minimizing the squared difference between the potentials actually recorded from the scalp and those theoretically calculated from the equivalent dipoles. The validity of this dipole tracing method (the DT of the SSB head model) was tested in patients with focal epileptic seizures undergoing presurgical evaluation with intracranial subdural strip electrodes. Weak currents were passed through 1 or 2 pairs of subdural electrodes to create artificial dipoles. The dipole estimations correctly distinguished between single and double generator sources, but there were certain dislocations of the calculated dipoles. The average error of dislocation was found to be 8.5 mm for the 1-dipole model. That for the 2-dipole model was 6 mm for one of the components and 18 mm for the other. It was concluded that the DT method of the SSB head model can be a valuable clinical tool in 3-dimensional localization of focal epileptic discharges in the human brain.

Double blind cross over trial with deprenyl in amyotrophic lateral sclerosis.

In this paper we present results from a double blind cross over trial with deprenyl, a selective and irreversible monoamine oxidase-B (MAO-B) inhibitor, in 10 patients suffering from amyotrophic lateral sclerosis. The patients were randomised in such a way that half of the patients started with the active drug and half with the placebo treatment. Each patient was given 10 mg deprenyl (eldepryl, 10 mg tablets) per day for 12 weeks and then placebo for the same length of time. There was a drug free period of 12 weeks between the courses. The neurological status of the patients were evaluated every six weeks by using Norris, spinal and bulbar scores and it was observed that all cases deteriorated in their clinical status during the 36 weeks of the controlled study. MAO-B activity in blood platelets was completely inhibited during treatment with deprenyl. In the preliminary analysis performed so far, no obvious retardation in the progress of the disease could be observed with deprenyl treatment.

Microneurography and applications to issues of motor control: Fifth Annual Stuart Reiner Memorial Lecture.

Among the hypotheses regarding fusimotor functions based on earlier animal experiments some are inconsistent, others are in conformity with microneurographic observations in man. The human data provide evidence against the following two theories: (1) the length follow-up servo theory; and (2) the theory that fusimotor neurons can be selectively activated to produce spindle sensitization and stretch reflex reinforcements. The human data support the theory of alpha-gamma coactivation. In particular, in the early phase of isometric voluntary contractions fusimotor-driven afferent spindle activity assists in autogenetic activation of alpha motoneurons and in reciprocal relaxation of antagonists. As muscle fatigue develops, the autogenetic reflex drive via the fusimotor route declines. The fusimotor bias during contraction provides for maintenance of spindle sensitivity to minute perturbations and for load-compensating reflex adjustments to such perturbations. Reflex overcorrections may lead to uncontrollable oscillations of the type seen in enhanced physiological tremor.

Decline in spindle support to alpha-motoneurones during sustained voluntary contractions.

1. To address whether the muscle spindle support to alpha-motoneurones is maintained during prolonged isometric voluntary contractions, the discharge of eighteen muscle spindle afferents, originating in the dorsiflexors of the ankle or toes, was recorded from the common peroneal nerve in eight subjects. Isometric contractions were generally sustained for 1 min, usually below 30% of the maximal voluntary dorsiflexion force. 2. Once the afferent had been identified, subjects were instructed to dorsiflex the foot slowly to recruit the spindle ending, to continue the ramp contraction until a predetermined target force was reached, and then to hold that force until requested to relax. 3. Five muscle spindle afferents maintained a constant discharge frequency during the hold phase of the isometric contraction. Following relaxation of the contraction two spindle afferents from tibialis anterior, exhibited a post-contraction discharge despite the absence of detectable electromyographic activity (EMG). 4. The discharge frequency of most of the spindle afferents (72%) declined progressively during the isometric contraction. The mean firing rates had declined to two-thirds of those at the onset of the contraction by 30 s, and to half after 1 min. The decline in spindle firing rate commenced during the ramp phase of the contraction and was statistically significant by 10 s, when force was held constant. The extent of the decline was greater for those units with the higher initial firing rates and for those units studied after many preceding contractions. 5. In the same contractions a progressive increase in EMG was required to maintain force and consequently the change in EMG was inversely related to the change in spindle discharge. While many mechanisms may contribute to the decline in spindle discharge during a sustained isometric contraction, it is argued that the result will be a progressive disfacilitation of alpha-motoneurones, which may contribute to the decline in motor unit firing rates during a sustained contraction.

Multiunit neural responses to strong finger pulp vibration. I. Relationship to age.

The effect of age on mechanoreceptive function in the distal part of the fingers was studied in 12 healthy subjects aged 18-64 years. A recording microelectrode was inserted into a sensory fascicle of the median nerve at the wrist. Multiunit mechanoreceptor activity was recorded from the fascicular field, which is typically restricted to the ulnar or radial half of one finger, corresponding to the innervation zone of one digital nerve. Strong standardized vibration (40 Hz) was applied to the finger pulp, with the amplitude of the vibration pulses high enough to induce maximal neural impulse volleys. With the same microelectrode recording position, maximal neural impulse volleys were also induced by electrical pulses applied to the ventral digital nerve supplying the finger pulp. In each subject, the areas of the mechanically and the electrically induced responses were measured (after integration and averaging) and the ratio of mechanically to electrically induced responses (MR/ER) was determined. The MR/ER ratio decreased with increasing age of the subject. This finding was considered to indicate that it is the peripheral parts of the sensory units, involved in the mechanoelectrical transfer functions, that exhibit the most pronounced degenerative changes during the ageing process. This is in line with previous histological findings of pronounced age-related degeneration of Meissner corpuscles and other mechanoreceptive end organs in the finger pulps.

Generator mechanisms of epileptic potentials analyzed by dipole tracing method.

A new dipole tracing method, based on a realistic head model, was used to determine dipole locations and vector moments of interictal convexity sharp waves recorded (with conventional EEG technique) from the right fronto-temporal region in a patient with partial complex seizures. When the dipole locations in the head model were compared to MRI scans, the majority of the sharp wave dipoles were found to be located in the right hippocampal area. For individual sharp waves, the hippocampal dipoles moved along tracks corresponding to the vector moment directions, suggesting that the electrical sources of the convexity sharp waves were somato-dendritic currents which spread rapidly from one neuron group to the next in the hippocampal area. Previous long-term subdural recording had shown seizure onset in this area. After right-sided anterior temporal lobectomy including the hippocampus the patient has been seizure-free for three months.

Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man.

1. In the present study on human foot dorsiflexor muscles we have examined the effects of high-frequency (150 Hz) muscle vibration on weak or moderate voluntary contractions (maintained by constant effort) and on maximal voluntary contractions (MCVs) of (i) non-fatigued muscles, (ii) muscles fatigued by sustained MVCs and (iii) muscles deprived of gamma-fibre innervation by partial anaesthetic nerve block. The motor outcome of the voluntary dorsiflexion efforts was assessed by measuring the firing rates of single motor units in the anterior tibial (TA) muscle, the mean voltage EMG activity from the pretibial muscles and foot dorsiflexion force. 2. With the subject instructed to exert constant effort in maintaining a weak or moderate contraction, superimposed vibration caused an enhancement of EMG activity and contraction force. 3. Previous claims that muscle vibration has no facilitatory effect on motor output in MVCs were found to hold true for non-fatigued but not for fatigued muscles. Thus, the fatigue-induced decline in EMG activity and motor unit firing rates was counteracted by short periods (less than 10-20 s) of superimposed vibration. However, with longer vibration periods it seemed as if the initial facilitation converted into an opposite effect which accentuated the fatigue-induced decline in motor output and contraction force. 4. Like muscle fatigue, a partial anesthetic block of the deep peroneal nerve, supposedly interrupting transmission in gamma-motor fibres, caused a reduction of MVC motor unit firing rates which could be counteracted by muscle vibration. In prolonged MVCs performed during the block, motor unit firing rates did not show the normal progressive decline from an initially high level, but stayed at a relatively constant low level throughout the contraction period. 5. Even though alternative interpretations are possible, the results agree with the hypotheses (i) that in sustained MVCs, fatigue processes occur not only in extrafusal but also in intrafusal muscle fibres, (ii) that the intrafusal fatigue leads to a reduction of the voluntary drive conveyed to the alpha-motoneurones via the gamma-loop and (iii) that vibration-induced activity in group Ia afferents can act as a substitute for the diminished fusimotor drive.

Prolonged muscle vibration reducing motor output in maximal voluntary contractions in man.

1. We observed in a previous study on the human foot dorsiflexor muscles that the fatigue-induced decline in motor output during sustained maximal voluntary contractions (MVCs) was temporarily counteracted during the initial phase of superimposed high-frequency (150 Hz) muscle vibration, whereas prolonged muscle vibration seemed to accentuate the fatigue-induced decline in gross EMG activity and motor unit firing rates. A more extensive investigation of this late effect of muscle vibration on MVCs was performed in the present study. 2. Prolonged periods of superimposed muscle vibration caused a reduction of EMG activity, motor unit firing rates and contraction force in both intermittent and sustained MVCs. This vibration-induced effect had the following main characteristics: (i) it developed slowly during the course of about 1 min of sustained vibration and subsided within 10-20 s after the end of vibration; (ii) it was much more pronounced in some subjects than in others (not age-dependent) and it was accentuated by preceding muscle exercise; (iii) it affected primarily the subject's ability to generate and/or maintain high firing rates in high-threshold motor units. 3. Since the effect developed while vibration at the same time exerted a tonic excitatory influence on the alpha-motoneurone pool (as evidenced by the presence of a tonic vibration reflex) it is argued that the vibration-induced suppression of motor output in MVCs probably does not depend on alpha-motoneurone inhibition, but on a reduced accessibility of these neurones to the voluntary commands. It is suggested that contributing mechanisms might be vibration-induced presynaptic inhibition and/or 'transmitter depletion' in the group Ia excitatory pathways which constitute the afferent link of the gamma-loop.

Mechanoreceptive units in the human infra-orbital nerve.

Eighty-four low-threshold mechanoreceptive afferents innervating facial hairy skin or the red zone of the lip were recorded with micro-electrodes from the human infra-orbital nerve. Based on their responses to skin indentations, the units were classified as slowly or fast-adapting, with small or large receptive fields. The responses to hair movement, skin stretching and contraction of facial muscles were also studied. Both hairy skin and the red zone were innervated by slowly and by fast-adapting units. The innervation density was found to be highest at the corner of the mouth and on the upper lip. Slowly adapting units with small fields in hairy skin were most common and included units responding to sustained hair displacement. These units are suggested to have two types of end-organs, either pilo-Ruffini endings or Merkel cell-neurite complexes. The slowly adapting units with large fields were spontaneously active stretch receptors and may have corresponded to Ruffini corpuscles, although the possibility of other, intramuscular, receptors could not be ruled out. Only one afferent possibly innervated a Pacinian corpuscle. Most mechanoreceptors were also activated by skin stretching or contraction of facial muscles. Many of the slowly adapting units with small fields responded to the onset and release of stretch, whereas their discharge in response to sustained stretching adapted more or less completely. Spontaneously active units had the most sustained stretch response. It is concluded that several types of cutaneous mechanoreceptors can operate as sensitive proprioceptors of importance for facial kinaesthesia and motor control.

Motor-unit responses in human wrist flexor and extensor muscles to transcranial cortical stimuli.

1. Transcranial cortical stimuli (TCCS) were used to elicit motor responses in contralateral wrist flexor and extensor muscles of healthy adult subjects. The motor responses were assessed by surface EMG recordings, by needle recordings of single motor-unit discharges, and by measurements of wrist twitch force. Our main aim was to analyze the single-unit events underlying those changes in latency, amplitude, and duration of the compound EMG responses, which could be induced by voluntary preactivation of target muscles and by changes in stimulation strength. 2. Different stimulus strengths were tested with and without background contractions in the flexor or extensor muscles. For each test (consisting of a series of 20 stimuli) the compound EMG responses were averaged and displayed together with the averaged wrist force signals. Responses of individual flexor and extensor motor units were displayed in raster diagrams and peristimulus time histograms. For units exhibiting a background firing, the mean background interdischarge interval was calculated and compared with the subsequent poststimulus intervals. 3. In relaxed muscles, a shortening of onset latency of evoked compound EMG responses was observed when raising stimulation strength. A similar latency reduction was not seen in any of the single-unit recordings. This would be consistent with the size principle of motoneuron recruitment. 4. A shortening of onset latency of evoked EMG potentials was observed also as a result of a voluntary preactivation. Such latency shifts, which were seen also in single-unit recordings, might be attributed to variations in the time required for D and I wave temporal summation at the anterior horn cell. 5. When raising stimulation strength or when adding voluntary background contraction, the evoked compound EMG potential grew not only in amplitude but also in duration, as later peaks of activity were added to the initial ones. Under optimal conditions (strong stimulus + background contraction), the period of excitation (termed E1) had an onset latency of approximately 15 ms and a duration of approximately 35 ms and was similar for wrist flexor and extensor muscles. 6. We never saw the same flexor or extensor unit fire more than once during the E1 period. For units preactivated by a background contraction, the stimulus-triggered impulse exhibited latency shifts, which, to a large extent, depended on the timing of the stimulus in relation to a preceding background discharge and which could be influenced by a change in stimulation strength.(ABSTRACT TRUNCATED AT 400 WORDS)