Metabolic and attentional energy costs of interlimb coordination.

The authors investigated metabolic and attentional energy costs as participants (N = 6) practiced in-phase, antiphase, and 90 degrees -phase cycling (order counterbalanced) on independent bicycle ergometers, with resistance (40 W/ergometer) and frequency (40 rpm) held constant. Coordination stabilized and became more accurate for all 3 cycling modes, as shown by measures of relative phase, but that collective variable could not account for other relevant attributes of the multifaceted motor behavior observed across the 3 coordination modes. In-phase and antiphase cycling were similar in stability and accuracy, but antiphase had the lowest metabolic and attentional energy costs. Because both homologous muscle action and perceptually symmetrical oscillations coincided in the in-phase mode, the absence of predominance of the inphase pattern showed that neither of those musculoskeletal and perceptual factors exclusively determined the strongest attractor of the coordination dynamics. Both metabolic and attentional costs declined with practice, consistent with the hypothesis that adaptive motor behavior is guided by sensory information concerning the energy demands of the task. Attentional cost was influenced not only by the information-processing demands of kinematic stability but also by the metabolic energy demands. Metabolic energy cost appeared to be the crucial determinant of the preferred solution for this coordination task.

The metabolic and cognitive energy costs of stabilising a high-energy interlimb coordination task.

Kinematic (relative phase error), metabolic (oxygen consumption, heart rate) and attentional (baseline and cycling reaction times) variables were measured while participants practised a high energy-demanding, intrinsically unstable 90 degrees relative phase coordination pattern on independent bicycle ergometers. The variables were found to be strongly inter-correlated, suggesting a link between emerging performance stability with practice and minimal metabolic and attentional cost. The effects of practice of 90 degrees relative phase coordination on the performance of in-phase (0 degrees-phase) and antiphase (180 degrees-phase) coordination were investigated by measuring the relative phase attractor layouts and recording the metabolic and attentional cost of the three coordination patterns before and after practice. The attentional variables did not differ significantly between coordination patterns and did not change with practice. Before practice, the coordination performance was most accurate and stable for in-phase cycling, with antiphase next and 90 degrees-phase the poorest. However, metabolic cost was lower for antiphase than either in-phase or 90 degrees-phase cycling, and the pre-practice attractor layout deviated from that predicted on the basis of dynamic stability as an attractor state, revealing an attraction to antiphase cycling. After practice of 90 degrees-phase cycling, in-phase cycling remained the most accurate and stable, with 90 degrees-phase next and antiphase the poorest, but antiphase retained the lowest metabolic energy cost. The attractor layout had changed, with new attractors formed at the practised 90 degrees-phase pattern and its symmetrical partner of 270 degrees-phase. Considering both the pre- and post-practice results, attractors were formed at either a low metabolic energy cost but less stable (antiphase) pattern or at a more stable but higher metabolic energy cost (90 degrees-phase) pattern, but in neither case at the most stable and accurate (in-phase) pattern. The results suggest that energetic factors affect coordination dynamics and that coordination modes lower in metabolic energy expenditure may compete with dynamically stable modes.

The spasticity paradox: movement disorder or disorder of resting limbs?

BACKGROUND: Spasticity is defined/assessed in resting limbs, where increased stretch reflex activity and mechanical joint resistance are evident. Treatment with antispastic agents assumes that these features contribute to the movement disorder, although it is unclear whether they persist during voluntary contraction. OBJECTIVES: To compare reflex amplitude and joint resistance in spastic and normal limbs over an equivalent range of background contraction. METHODS: Thirteen normal and eight hemiparetic subjects with mild/moderate spasticity and without significant contracture were studied. Reflex and passive joint resistance were compared at rest and during six small increments of biceps voluntary contraction, up to 15% of normal maximum. A novel approach was used to match contraction levels between groups. RESULTS: Reflex amplitude and joint mechanical resistance were linearly related to contraction in both groups. The slopes of these relations were not above normal in the spastic subjects on linear regression. Thus, reflex amplitude and joint resistance were not different between groups over a comparable range of contraction levels. Spastic subjects exhibited a smaller range of reflex modulation than normals because of decreased maximal contraction levels (weakness) and significant increases of resting contraction levels. CONCLUSIONS: Spasticity was most evident at rest because subjects could not reduce background contraction to normal. When background contractions were matched to normal levels, no evidence of exaggerated reflex activity or mechanical resistance was found. Instead, reduced capacity to modulate reflex activity dynamically over the normal range may contribute to the movement disorder. This finding does not support the routine use of antispastic agents to treat the movement disorder.

Practice effects on coordination and control, metabolic energy expenditure, and muscle activation.

One defining characteristic of skilled motor performance is the ability to complete the task with minimum energy expenditure. This experiment was designed to examine practice effects on coordination and control, metabolic energy expenditure, and muscle activation. Participants rowed an ergometer at 100 W for ten 16-min sessions. Oxygen consumption and perceived exertion (central and peripheral) declined significantly with practice and movement economy improved (reliably) by 9%. There was an associated but non-significant reduction in heart rate. Stroke rate decreased significantly. Peak forces applied to the ergometer handle were significantly less variable following practice and increased stability of the post-practice movement pattern was also revealed in more tightly clustered plots of hip velocity against horizontal displacement. Over practice trials muscle activation decreased, as revealed in integrated EMG data from the vastus lateralis and biceps brachii, and coherence analysis revealed the muscle activation patterns became more tightly coordinated. The results showed that practice reduced the metabolic energy cost of performance and practice-related refinements to coordination and control were also associated with significant reductions in muscle activation.

Abnormal muscle activation characteristics associated with loss of dexterity after stroke.

The aim of this study was to characterise the abnormalities of muscle activation which underlie low dexterity after stroke. A broad definition of dexterity was adopted, where loss of dexterity refers to an inability to coordinate muscle activity in the performance of a motor task (i.e. dexterity was not confined to manual dexterity). EMG of biceps brachii and triceps brachii were monitored from 16 people after stroke and 10 neurologically normal controls as they performed a tracking task requiring coordinated elbow flexion and extension. Weakness could not interfere with performance since the task was designed to require minimal strength. Stroke subjects were assigned to a low (n=10) or high (n=6) dexterity group based on their performance. Spatiotemporal aspects of biceps and triceps EMG were analysed. Low dexterity performance after stroke was characterised by excessive biceps muscle activation (P=0.002) and decreased coupling of muscle activation to target motion (P=0.002). In this study, we could rule out weakness, slowness of muscle activation, excessive co-contraction and spasticity as causes of these abnormalities. Therefore, the loss of dexterity after stroke can be seen as a specific negative impairment which can exist independently of other motor impairments and reflects a loss of skill in generating spatial and temporal muscle activation patterns which conform with environmental demands.

Tonic stretch reflexes in older able-bodied people.

It is a general assumption that, in able-bodied persons, tonic stretch reflex (TSR) activity is not elicited during stretching of relaxed muscles and that the presence of TSR activity following brain damage is, therefore, indicative of spasticity. However, a variety of studies have reported age-related changes in reflex activity, raising the question of whether this assumption is justified in older subjects. The aim of this study was to determine if TSRs were activated in the relaxed elbow flexors of able-bodied people in an age-group at risk of stroke. Electromyographic (EMG) activity was recorded in 30 able-bodied subjects aged 46 to 78 years when their relaxed elbow flexors were subjected to ramp and sinusoidal stretches of different amplitudes and velocities. It was found that these subjects did not exhibit TSR activity under these conditions. Therefore, the practice of measuring TSR activity as a means of quantifying spasticity in stroke patients appears justified.

Does spasticity contribute to walking dysfunction after stroke?

OBJECTIVES: Clinically, it is assumed that spasticity of the calf muscles interferes with walking after stroke. The aim was to examine this assumption by evaluating the contribution of spasticity in the gastrocnemius muscle to walking dysfunction in an ambulant stroke population several months after stroke. METHODS: Fourteen stroke patients who were able to walk independently and 15 neurologically normal control subjects were recruited. Both resting and action stretch reflexes of the gastrocnemius muscle were investigated under conditions that simulated walking. Resting tonic stretch reflexes were measured to assess spasticity whereas action tonic stretch reflexes were measured to assess the possible contribution of spasticity to gait dysfunction. RESULTS: Two thirds of the stroke patients exhibited resting tonic stretch reflexes which indicate spasticity, whereas none of the control subjects did. However, the stroke patients exhibited action tonic stretch reflexes that were of similar magnitude to the control subjects, suggesting that their reflex activity during walking was not different from that of control subjects. Furthermore, there was no evidence that the action stretch reflex in the stroke patients contributed a higher resistance to stretch than the control subjects. CONCLUSIONS: Whereas most of the stroke patients exhibited spasticity when measured both clinically and physiologically, they did not exhibit an increase in resistance to dorsiflexion due to exaggerated action tonic stretch reflexes. It is concluded that it is unlikely that spasticity causes problems in walking after stroke in ambulant patients. Therefore, it seems inappropriate to routinely reduce or inhibit the reflex response to improve functional movement in stroke rehabilitation. Factors other than spasticity should be considered when analysing walking after stroke, so that appropriate treatment is provided to patients.

Reflex hyperexcitability and muscle contracture in relation to spastic hypertonia.

Mechanisms of spasticity and possible therapeutic interventions continue to dominate research into motor disorders following cerebral lesions. However, the accumulated evidence suggests that this focus on spasticity may be out of step with its effects. In contrast, hypertonia remains an important problem. Further investigation into its link with muscle contracture is required and it needs to be clearly distinguished from reflex hyperexcitability in patients with spasticity.

Spasticity and muscle contracture following stroke.

It has become increasingly recognized that the major functional deficits following brain damage are largely due to "negative' features such as weakness and loss of dexterity rather than spasticity. A variety of studies suggest that spasticity is a distinct problem and separate from the loss of dexterity, but that it may be implicated in the formation of muscle contracture and even in the recovery of strength. In order to address these issues, we examined the relationship between spasticity, contracture, strength and dexterity in the affected upper limb following stroke. Spasticity was measured both as increased tonic stretch reflexes and increased resistance to passive stretch (hypertonia). Twenty-four patients were recruited non-selectively from three rehabilitation units within 13 months of their stroke. Few patients exhibited increased tonic reflexes but half were found to have muscle contracture, the earliest at 2 months following stroke. Hypertonia was associated with contracture but not with reflex hyperexcitability. Increased tonic stretch reflexes were observed only in a subgroup of those with contracture and where present could usually be elicited only at the end of muscle range. This findings suggests that instead of spasticity causing contracture, contracture may actually potentiate spasticity in some patients. However, the majority of patients with contracture did not have increased tonic stretch reflexes. In addition, we found no relationship between spasticity and either weakness or loss of dexterity. Therefore, while hypertonia remains an important problem following cerebral lesions, it would appear that the amount of attention directed to reflex hyperexcitability associated with spasticity is out of proportion with its effects. Consequently, hypertonia needs to be clearly distinguished from reflex hyperexcitability in patients with spasticity.

Control of isometric muscle activity in cerebral palsy.

Voluntary control of muscle contraction was examined in five adults with cerebral palsy, who were required to track a moving target by continuously varying the level of isometric contraction of elbow flexor muscles (measured by EMG). First performance varied from minimal control to almost normal control, depending on the severity of disability. Practice over 12 weeks reduced inappropriate muscle activity in the most disabled patients, but there was no increase in appropriate muscle activity for any patient beyond that observed after the first few minutes of tracking. Thus their ability to translate a visual response into the appropriate motor activity was impaired, and there was no evidence of potential to overcome this. This supports the authors' earlier proposal that impairment of sensory-motor learning is the primary cause of functional disability in cerebral palsy. The EMG tracking task may provide a technique for assessing the ability of individuals with cerebral palsy to control muscle contraction.

Reducing spasticity to control muscle contracture of children with cerebral palsy.

A biofeedback training technique to control spasticity, previously successful with adults with cerebral palsy, was adapted for three children with spastic diplegia at risk for contractures. Visual feedback of muscle stretch reflex sensitivity is provided by video games, which are played by reducing reflex sensitivity. After a 10-week training period two of the three children had significantly reduced spasticity in the gastrocnemius muscle. The technique can be used with children as young as four years, is inexpensive, and can be carried out by parents with supervision by a physiotherapist.

Voluntary muscle control in normal and athetoid dysarthric speakers.

Time domain and frequency domain analyses were performed on smoothed and averaged electromyographic (IEMG) activity recorded intramuscularly from 6 muscles of the lips, tongue and jaw during speech in normal and athetoid cerebral palsy subjects. The speech IEMG waveforms in both groups were composed of slowly changing tonic activity merging with more rapidly changing phasic bursts. Significant increases both in the durations and average levels of IEMG activity in the athetoid subjects resulted in a 5- to 30-fold increase in the speech muscle energy expended by these subjects. The peak-to-peak amplitudes of the IEMG activity were significantly increased in the athetoid subjects, commensurate with their increased average levels, thus demonstrating that they could vary their muscle contraction levels over a wide range. The velocities (rates of change) of muscle IEMG activity did not differ significantly between the two groups. The velocity of the IEMG activity increased linearly with its amplitude in both subject groups, but the durations of the IEMG bursts nevertheless were highly variable. The slope of the velocity-amplitude relation in the athetoid subjects was less than half that in the normal subjects, suggesting that the frequency bandwidth of muscle activity was reduced in the athetoid subjects, despite a normal range of IEMG velocities. The frequency analysis confirmed this suggestion. The upper limit of the average frequency spectrum of voluntary muscle activity for speech was 7 Hz in the normal subjects, whereas this limit was 4 Hz in the athetoid subjects. In the normal subjects each muscle had a different frequency spectrum, whereas the spectra for the 6 muscles were remarkably uniform in the athetoid subjects, implying an abnormality in the functional organization of their muscles. The findings of this study showed clearly that the temporospatial patterns of voluntary muscle activity in the athetoid subjects were grossly abnormal. Since this voluntary activity was reproducible across multiple repetitions of the same speech sample, the dysarthria in these speakers may be attributed to abnormal control of voluntary activity, not to involuntary movement. The results support the view that the primary disability in cerebral palsy is a disruption of the physiological mechanisms which subserve the acquisition of motor skills.

Motor control deficits of orofacial muscles in cerebral palsy.

Voluntary control of the masseter and orbicularis oris superioris muscles was examined in able bodied and cerebral palsied subjects using visual tracking tasks. A smoothed measure of muscle activity (the full-wave rectified and low-pass filtered electromyogram) was presented as a marker on a computer display screen and the subjects could control the vertical position of the marker by voluntarily altering the level of isometric contraction of one of the muscles. A target marker was also displayed on the screen and the subjects were required to follow or "track" the irregular movements of this target with the response marker. Their success in aligning the response marker with the target was analysed for these orofacial muscles. The masseter is influenced by muscle spindle based reflexes, while the orbicularis oris superioris lacks such reflex control. The cerebral palsied subjects displayed similarly poor control over both muscles, implying that their voluntary motor deficits are not related to abnormal muscle spindle based reflexes. It is suggested that the impairment may be related to perceptual-motor integration.

Internal models and intermittency: a theoretical account of human tracking behavior.

This paper concerns the use of tracking studies to test a theoretical account of the information processing performed by the human CNS during control of movement. The theory provides a bridge between studies of reaction time and continuous tracking. It is proposed that the human CNS includes neuronal circuitry to compute inverse internal models of the multiple input, multiple output, dynamic, non-linear relationships between outgoing motor commands and their resulting perceptual consequences. The inverse internal models are employed during movement execution to transform preplanned trajectories of desired perceptual consequences into appropriate outgoing motor commands to achieve them. A finite interval of time is required by the CNS to preplan the desired perceptual consequences of a movement and it does not commence planning a new movement until planning of the old one has been completed. This behavior introduces intermittency into the planning of movements. In this paper we show that the gain and phase frequency response characteristics of the human operator in a visual pursuit tracking task can be derived theoretically from these assumptions. By incorporating the effects of internal model inaccuracy and of speed-accuracy trade-off in performance, it is shown that various aspects of experimentally measured tracking behavior can be accounted for.

Stochastic prediction in pursuit tracking: an experimental test of adaptive model theory.

In this paper we test the proposition that in pursuit tracking, subjects compute stochastic (statistical) models of the temporal variations in position of the target and use these models to forecast target position for at least a response time interval into the future. A computer simulation of a human operator employing stochastic model prediction of target position is used to generate a synthetic pursuit tracking response signal. Actual pursuit tracking response signals are measured from 10 normal subjects using the same stimulus signal. Cross correlation and spectral analysis are employed to compute gain and phase frequency response characteristics for both synthetic and actual tracking data. The similarity of the gain and phase curves for synthetic and actual data provides compelling evidence in support of the proposition.

Reproducibility and variability of speech muscle activity in athetoid dysarthria of cerebral palsy.

Athetoid dysarthria is thought to result from involuntary movements which are variable and irregular in nature. In this study, electromyographic (EMG) activity recorded from six speech muscles was quantified during repetitions of a test sentence by normal and athetoid adult subjects. In the athetoid subjects the articulation of the test sentence was disrupted intermittently by involuntary activity which usually occurred in the time intervals between the syllables in the test sentence, rather than during articulation of the syllables themselves. The EMG activity associated with each syllable in the test sentence was partitioned into reproducible and variable components. The ratio of the reproducible component to the variable component--the signal-to-noise ratio--did not differ significantly between the two subject groups. In the athetoid subjects, however, the reproducible component of the EMG activity was grossly abnormal. We concluded that this abnormal voluntary activity, rather than variable involuntary activity, was the primary cause of athetoid dysarthria.

Control of upper airway structures during nonspeech tasks in normal and cerebral-palsied subjects: EMG findings.

Electromyographic (EMG) recordings taken from 13 orofacial and mandibular muscles during a sequence of nonspeech movements were compared in six normal and six cerebral-palsied adult subjects. Abnormalities in the amplitude of muscle activity and timing of muscle control in the cerebral-palsied subjects were borne out in statistically significant differences between the two subject groups on five measures of muscle activity. The findings do not support hypotheses that weakness affects individual upper airway muscles in cerebral-palsied persons or that a pathological imbalance between positive and negative oral reactions is present in these subjects. A possible mechanism for hypertonicity in facial muscles in cerebral palsy is suggested, based on inappropriate activation patterns across muscles. The results are consistent with a previous proposal that a defect in the specification of motor commands and/or their communication to muscles is a fundamental abnormality in cerebral-palsied individuals which affects both speech and nonspeech motor control.

Pathophysiology of dysarthria in cerebral palsy.

Electromyograms were recorded with hooked-wire electrodes from sixteen lip, tongue and jaw muscles in six normal and seven cerebral palsied adult subjects during a variety of speech and non-speech tasks. The recorded patterns of muscle activity fail to support a number of theories concerning the pathophysiology of dysarthria in cerebral palsy. There was no indication of weakness in individual articulator muscles. There was no evidence of uncontrolled sustained background activity or of abnormal tonic stretch reflex responses in lip or tongue muscles. Primitive or pathological reflexes could not be elicited by orofacial stimulation. No imbalance between positive and negative oral responses was observed. The view that random involuntary movement disrupts essentially normal voluntary control in athetosis was not supported. Each cerebral palsied subject displayed an idiosyncratic pattern of abnormal muscle activity which was reproduced across repetitions of the same phrase, indicating a consistent defect in motor programming.