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Papers by Martin Lakie

The Journal of physiology, Jan 26, 2015

Quiet standing is achieved through a combination of active and passive mechanisms, consisting of ... more Quiet standing is achieved through a combination of active and passive mechanisms, consisting of neural control and intrinsic mechanical stiffness of the ankle joint, respectively. The mechanical stiffness is partly determined by the calf muscles. But the visco-elastic properties of muscle are highly labile, exhibiting strong dependence on movement history. Here we determine if this lability has consequences for the passive stabilization of human standing, by measuring the effect of sway history upon ankle stiffness. Ten subjects stood quietly on a rotating platform whose axis was collinear with the ankle joint. Ankle sway was increased by slowly tilting this platform in a random fashion, or decreased by fixing the body to a board. Ankle stiffness was measured by using the same platform to simultaneously apply small, brief perturbations (<0.6 deg; 140 ms), while the resulting torque response was recorded. The results show that increasing sway reduces ankle stiffness by up to 43%,...

ABSTRACT Human physiological hand tremor has a resonant component. Proof of this is that its freq... more ABSTRACT Human physiological hand tremor has a resonant component. Proof of this is that its frequency can be modified by adding mass. However, adding mass also increases the load which must be supported. The necessary force requires muscular contraction which will change motor output and is likely to increase limb stiffness. The increased stiffness will partly offset the effect of the increased mass and this can lead to the erroneous conclusion that factors other than resonance are involved in determining tremor frequency. Using a human centrifuge to increase head-to-foot gravitational field strength, we were able to control for the increased effort by increasing force without changing mass. This revealed that the peak frequency of human hand tremor is 99% predictable on the basis of a resonant mechanism. We ask what, if anything, the peak frequency of physiological tremor can reveal about the operation of the nervous system. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.

J Neurophysiol, 2010

Axelson HW, Hagbarth KE. Human motor control consequences of thixotropic changes in muscular shor... more Axelson HW, Hagbarth KE. Human motor control consequences of thixotropic changes in muscular short-range stiffness. J Physiol 535: 279 -288, 2001. Campbell KS, Lakie M. A cross-bridge mechanism can explain the thixotropic short-range elastic component of relaxed frog skeletal muscle. J Physiol 510: 941-962, 1998. Campbell KS, Moss RL. A thixotropic effect in contracting rabbit psoas muscle: prior movement reduces the initial tension response to stretch. J Physiol 525: 531-548, 2000. Campbell KS, Moss RL. History-dependent mechanical properties of permeabilized rat soleus muscle fibers. Biophys J 82: 929 -943, 2002. Conway BA, Halliday DM, Farmer SF, Shahani U, Maas P, Weir AI, Rosenberg JR. Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J Physiol 489: 917-924, 1995. Dietz V, Bischofberger E, Wita C, Freund HJ. Correlation between the dischanges of two simultaneously recorded motor units and physiological tremor. Electroencephalogr Clin Neurophysiol 40: 97-105, 1976. Elble RJ, Randall JE. Motor-unit activity responsible for 8-to 12-Hz component of human physiological finger tremor. J Neurophysiol 39: 370 -383, 1976. Elble RJ, Randall JE. Mechanistic components of normal hand tremor. Electroencephalogr Clin Neurophysiol 44: 72-82, 1978.

The Journal of physiology, Jan 24, 2015

Human physiological hand tremor has a resonant component. Proof of this is that its frequency can... more Human physiological hand tremor has a resonant component. Proof of this is that its frequency can be modified by adding mass. However, adding mass also increases the load which must be supported. The necessary force requires muscular contraction which will change motor output and is likely to increase limb stiffness. The increased stiffness will partly offset the effect of the increased mass and this can lead to the erroneous conclusion that factors other than resonance are involved in determining tremor frequency. Using a human centrifuge to increase head-to-foot gravitational field strength, we were able to control for the increased effort by increasing force without changing mass. This revealed that the peak frequency of human hand tremor is 99% predictable on the basis of a resonant mechanism. We ask what, if anything, the peak frequency of physiological tremor can reveal about the operation of the nervous system. This article is protected by copyright. All rights reserved.

Journal of neuroscience methods

Automated image tracking provides new insights in many physiological studies, but present methods... more Automated image tracking provides new insights in many physiological studies, but present methods are ad hoc and can be difficult to use. They are generally based on following the movement of one or more specific regions of interested - point tracking. We tested newly available novel planar tracking technology commercially developed for the special effects industry, which does not use point tracking. We validated the tracker and made two dynamic physiological measurements. Our validation measurements describe the accuracy and repeatability of the technique, and our physiological measurements demonstrate the flexibility of the software. Our results suggest that planar tracking may be of particular use with techniques that produce low quality images such as ultrasonography.

Exercise and sport sciences reviews, 2014

Explanation of motor control is dominated by continuous neurophysiological pathways (e.g., transc... more Explanation of motor control is dominated by continuous neurophysiological pathways (e.g., transcortical, spinal) and the continuous control paradigm. Using new theoretical development, methodology, and evidence, we propose intermittent control, which incorporates a serial ballistic process within the main feedback loop, provides a more general and more accurate paradigm necessary to explain attributes highly advantageous for competitive survival and performance.

ABSTRACT In almost every person there is a clear oscillation at ~10 Hz in the limbs under postura... more ABSTRACT In almost every person there is a clear oscillation at ~10 Hz in the limbs under postural conditions. This postural physiological tremor has been investigated and explained in terms of either mechanical influences (e.g. mechanical resonance of the limb), or neural influences (e.g. rhythmicities of central neural firing) (McAuley and Marsden 2000). We recently showed that human physiological tremor has a strongly mechanical basis (Lakie et al, 2010) and largely results from broad band forcing (EMG) of a resonant system. Here we investigate the effect of altering the forcing by making the muscles ischaemic. With ethical permission we recorded tremor of the outstretched splinted middle finger in 12 subjects (11 male) using a 3 axis accelerometer. One slow movement condition and three postural conditions were studied. Ischaemia was produced by an arm cuff inflated to 150 mm Hg for up to 8 minutes. Surface EMG was recorded from the forearm extensor muscles. Records lasted 60 s each and were repeated 4 times over 2 days. Cross spectral gain between rectified EMG and vertical acceleration was subsequently calculated. Acceleration size was greatly reduced by ischaemia. EMG was if anything slightly increased. Accordingly gain was greatly reduced (Fig 1). Ischaemia is known to substantially reduce tremor size (Christakos et al, 2006). This reduction has been attributed to the effect of ischaemia on muscle spindles (Lippold, 1970) or to its effect on muscle contractile properties (Lakie et al, 2004). The reduction in gain that we see in the present experiments strongly supports the latter explanation.

Journal of Neurophysiology, 2014

Two frequency peaks of variable preponderance have been reported for human physiological finger t... more Two frequency peaks of variable preponderance have been reported for human physiological finger tremor. The high-frequency peak (20-25 Hz, seen only in postural tremor) is generally attributed to mechanical resonance, whereas the lower frequency peak (8-12 Hz, seen in both postural and kinetic tremor) is usually attributed to synchronous central or reflexive neural drive. In this study, we determine whether mechanical resonance could generate both peaks. In relaxed subjects, an artificial finger tremor was evoked by random mechanical perturbations of the middle finger or random electrical muscular stimulation of the finger extensor muscle. The high and the low frequencies observed in physiological tremor could both be created by either type of artificial input at appropriate input intensity. Resonance, inferred from cross-spectral gain and phase, occurred at both frequencies. To determine any neural contribution, we compared truly passive subjects with those who exhibited some electromyographic (EMG) activity in the finger extensor; artificially created tremor spectra were almost identical between groups. We also applied electrical stimuli to two clinically deafferented subjects lacking stretch reflexes. They exhibited the same artificial tremor spectrum as control subjects. These results suggest that both typical physiological finger tremor frequencies can be reproduced by random artificial input; neither requires synchronized neural input. We therefore suggest that mechanical resonance could generate both dominant frequency peaks characteristic of physiological finger tremor. The inverse relationship between the input intensity and the resulting tremor frequency can be explained by a movement-dependent reduction in muscle stiffness, a conjecture we support using a simple computational model.

Experimental Physiology, 1994

Ethanol reduces the size of essential tremor. We here show that, contrary to a recent report, eth... more Ethanol reduces the size of essential tremor. We here show that, contrary to a recent report, ethanol also causes a large decrease in the size of physiological tremor. As in the case of essential tremor, the frequency is not changed. The reduction in tremor probably explains the well-known link between certain types of skilled activity and alcohol consumption.

The Journal of Physiology, 2012

Limb resonance imparts a characteristic spectrum to hand tremor. Movement will alter the resonanc... more Limb resonance imparts a characteristic spectrum to hand tremor. Movement will alter the resonance. We have examined the consequences of this change. Rectified forearm extensor muscle EMG and physiological hand tremor were recorded. In postural conditions the EMG spectrum is relatively flat whereas the acceleration spectrum is sharply peaked. Consequently, the gain between EMG and acceleration is maximal at the frequency where the tremor is largest (∼8 Hz). The shape of the gain curve implies mechanical resonance. Substantial alterations in posture do not significantly change the characteristics of the tremor or the shape or size of the gain curve. By contrast, slow or moderately paced voluntary wrist flexion–extension movements dramatically increase the hand tremor size and lower its peak frequency. These changes in size and frequency of the tremor cannot be attributed to changes in the EMG. Instead they reflect a very large change in the size and shape of the gain curve relating EMG to acceleration. The gain becomes larger and the peak moves to a lower frequency (∼6 Hz). We suggest that a movement-related (thixotropic) alteration in resonant properties of the wrist provides a simple explanation for these changes. The mechanism is illustrated by a model. Our new findings confirm that resonance plays a major role in wrist tremor. We also demonstrate that muscles operate very differently under postural and dynamic conditions. The different coupling between EMG and movement in posture and when moving must pose a considerable challenge for neural predictive control of skeletal muscles.

The Journal of Physiology, 1998

The precise control of posture and movement imposes severe constraints on the human neuromuscular... more The precise control of posture and movement imposes severe constraints on the human neuromuscular system. In particular, to maintain stability, the motor control system must continually react to proprioceptive feedback as the body is perturbed by unpredictable external forces. In this type of control mechanism there is an inevitable time delay (due to e.g. nerve conduction and electromechanical coupling) between the sensing of the perturbation and the completion of the corrective movement. The delays in the feedback loop are destabilizing and may result in tremulous movement . A small resistance to movement inherent in the muscle fibres themselves would provide 1. The passive tension and sarcomere length of relaxed frog skeletal muscle fibres were measured in response to imposed length stretches. The tension response to a constantvelocity stretch exhibited a clear discontinuity. Tension rose more rapidly during the initial • 0·4 % LÑ of the stretch than during the latter stages (where LÑ is the resting length of the fibre). This initial tension response is attributed to the short-range elastic component (SREC). 2. The use of paired triangular stretches revealed that the maximum tension produced during the SREC response of the second stretch was significantly reduced by the first stretch. This history-dependent behaviour of the SREC reflects thixotropic stiffness changes that have been previously described in relaxed muscle. 3. The biphasic nature of the SREC tension response to movement was most apparent during the first imposed length change after a period at a fixed length, irrespective of the direction of movement. 4. If a relaxed muscle was subjected to an imposed triangular length change so that the muscle was initially stretched and subsequently shortened back to its original fibre length, the resting tension at the end of the stretch was reduced relative to its initial pre-stretch value. Following the end of the stretch, tension slowly increased towards its initial value but the tension recovery was not accompanied by a contemporaneous increase in sarcomere length. This finding suggests that the resting tension of a relaxed muscle fibre is not entirely due to passive elasticity. The results are compatible with the suggestion that a portion of the resting tension -the filamentary resting tension (FRT) -is produced by a low level of active force generation. 5. If a second identical stretch was imposed on the muscle at a time when the resting tension was reduced by the previous stretch, the maximal tension produced during the second stretch was the same as that produced during the first, despite the second stretch commencing from a lower initial resting tension. 6. In experiments using paired triangular length changes, an inter-stretch interval of zero did not produce a substantially greater thixotropic reduction in the second stretch elastic limit force than an inter-stretch interval in the range 0·5-1 s. 7. A theoretical model was developed in which the SREC and FRT arise as manifestations of a small number of slowly cycling cross-bridges linking the actin and myosin filaments of a relaxed skeletal muscle. The predictions of the model are compatible with many of the experimental observations. If the SREC and FRT are indeed due to cross-bridge activity, the model suggests that the cross-bridge attachment rate must increase during interfilamentary movement. A mechanism (based on misregistration between the actin binding sites and the myosin cross-bridges) by which this might arise is presented. 7399 Single intact iliofibularis muscle fibre. Stretch length • 0·011 LÑ. Stretch velocity • 0·011 LÑ s¢. The fibre had been held at a constant length for 1 min before the first stretch was initiated. Temperature 5·0°C.

The Journal of Physiology, 2002

During quiet standing the human &amp;amp;amp;amp;amp;amp;amp;amp;quot;inverted pendulum&a... more During quiet standing the human &amp;amp;amp;amp;amp;amp;amp;amp;quot;inverted pendulum&amp;amp;amp;amp;amp;amp;amp;amp;quot; sways irregularly. In previous work where subjects balanced a real inverted pendulum, we investigated what contribution the intrinsic mechanical ankle stiffness makes to achieve stability. Using the results of a plausible model, we suggested that intrinsic ankle stiffness is inadequate for providing stability. Here, using a piezo-electric translator we applied small, unobtrusive mechanical perturbations to the foot while the subject was standing freely. These short duration perturbations had a similar size and velocity to movements which occur naturally during quiet standing, and they produced no evidence of any stretch reflex response in soleus, or gastrocnemius. Direct measurement confirms our earlier conclusion; intrinsic ankle stiffness is not quite sufficient to stabilise the body or pendulum. On average the directly determined intrinsic stiffness is 91 +/- 23 % (mean +/- S.D.) of that necessary to provide minimal stabilisation. The stiffness was substantially constant, increasing only slightly with ankle torque. This stiffness cannot be neurally regulated in quiet standing. Thus we attribute this stiffness to the foot, Achilles&amp;amp;amp;amp;amp;amp;amp;amp;#39; tendon and aponeurosis rather than the activated calf muscle fibres. Our measurements suggest that the triceps surae muscles maintain balance via a spring-like element which is itself too compliant to guarantee stability. The implication is that the brain cannot set ankle stiffness and then ignore the control task because additional modulation of torque is required to maintain balance. We suggest that the triceps surae muscles maintain balance by predictively controlling the proximal offset of the spring-like element in a ballistic-like manner.

The Journal of Physiology, 2001

Using the ankle musculature, subjects balanced a large inverted pendulum. The equilibrium of the ... more Using the ankle musculature, subjects balanced a large inverted pendulum. The equilibrium of the pendulum is unstable and quasi-regular sway was observed like that in quiet standing. Two main questions were addressed. Can subjects systematically change sway size in response to instruction and availability of visual feedback? If so, do subjects decrease sway size by increasing ankle impedance or by some alternative mechanism? The position of the pendulum, the torque generated at each ankle and the soleus and tibialis anterior EMG were recorded. Results showed that subjects could significantly reduce the mean sway size of the pendulum by giving full attention to that goal. With visual feedback sway size could be minimised significantly more than without visual feedback. In changing sway size, the frequency of the sways was not changed. Results also revealed that ankle impedance and muscle co-contraction were not significantly changed when the sway size was decreased. As the ankle impedance and sway frequency do not change when the sway size is decreased, this implies no change in ankle stiffness or viscosity. Increasing ankle impedance, stiffness or viscosity are not the only methods by which sway size could be reduced. A reduction in torque noise or torque inaccuracy via a predictive process which provides active damping could reduce sway size without changing ankle impedance and is plausible given the data. Such a strategy involving motion recognition and generation of an accurate motor response may require higher levels of control than changing ankle impedance by altering reflex or feedforward gain.

The Journal of Physiology, 2005

The Journal of Physiology, 2006

Ten subjects balanced their own body or a mechanically equivalent unstable inverted pendulum by h... more Ten subjects balanced their own body or a mechanically equivalent unstable inverted pendulum by hand, through a compliant spring linkage. Their balancing process was always characterized by repeated small reciprocating hand movements. These bias adjustments were an observable sign of intermittent alterations in neural output. On average, the adjustments occurred at intervals of approximately 400 ms. To generate appropriate stabilizing bias adjustments, sensory information about body or load movement is needed. Subjects used visual, vestibular or proprioceptive sensation alone and in combination to perform the tasks. We first ask, is the time between adjustments (bias duration) sensory specific? Vision is associated with slow responses. Other senses involved with balance are known to be faster. Our second question is; does bias duration depend on sensory abundance? An appropriate bias adjustment cannot occur until unplanned motion is unambiguously perceived (a sensory threshold). The addition of more sensory data should therefore expedite action, decreasing the mean bias adjustment duration. Statistical analysis showed that (1) the mean bias adjustment duration was remarkably independent of the sensory modality and (2) the addition of one or two sensory modalities made a small, but significant, decrease in the mean bias adjustment duration. Thus, a threshold effect can alter only a very minor part of the bias duration. The bias adjustment duration in manual balancing must reflect something more than visual sensation and perceptual thresholds; our suggestion is that it is a common central motor planning process. We predict that similar processes may be identified in the control of standing.

The Journal of Physiology, 2005

It has been widely assumed for nearly a century, that postural muscles operate in a spring-like m... more It has been widely assumed for nearly a century, that postural muscles operate in a spring-like manner and that muscle length signals joint angle (the mechano-reflex mechanism). Here we employ automated analysis of ultrasound images to resolve calf muscle (soleus and gastrocnemius) length changes as small as 10 µm in standing subjects. Previously, we have used balancing of a real inverted pendulum to make predictions about human standing. Here we test and confirm these predictions on 10 subjects standing quietly. We show that on average the calf muscles are actively adjusted 2.6 times per second and 2.8 times per unidirectional sway of the body centre of mass (CoM). These alternating, small (30-300 µm) movements provide impulsive, ballistic regulation of CoM movement. The timing and pattern of these adjustments are consistent with multisensory integration of all information regarding motion of the CoM, pattern recognition, prediction and planning using internal models and are not consistent with control solely by local reflexes. Because the system is unstable, errors in stabilization provide a perturbation which grows into a sway which has to be reacted to and corrected. Sagittal sway results from this impulsive control of calf muscle activity rather than internal sources (e.g. the heart, breathing). This process is quite unlike the mechano-reflex paradigm. We suggest that standing is a skilled, trial and error activity that improves with experience and is automated (possibly by the cerebellum). These results complement and extend our recent demonstration that paradoxical muscle movements are the norm in human standing.

The Journal of Physiology, 2005

In humans, during standing the calf muscles soleus and gastrocnemius actively prevent forward top... more In humans, during standing the calf muscles soleus and gastrocnemius actively prevent forward toppling about the ankles. It has been generally assumed that these postural muscles behave like springs with dynamic stiffness reflecting their mechanical properties, reflex gain including higher derivatives, and central control. Here, for the first time, we have used an ultrasound scanner and automated image analysis to record the tiny muscular movements occurring in normal standing. This new, non-invasive technique resolves changes in muscle length as small as 10 mum without disturbing the standing process. This technical achievement has allowed us to test the long-established mechano-reflex, muscle spring hypothesis that muscle length changes in a spring-like way during sway of the body. Our results contradict that hypothesis. Muscle length changes in a non-spring-like manner: on average, shortening during forward sway and lengthening during backwards sway (paradoxical movements). This counter-intuitive result is a consequence of the fact that calf muscles generate tension through a series elastic component (SEC, Achilles tendon and foot) which limits maximal ankle stiffness to 92 +/- 20% of that required to balance the body. Paradoxical movements cannot be generated by stretch reflexes with constant intrafusal drive but might be produced by reflex coupling of extrafusal (alpha) and intrafusal (beta, gamma) drive or by positive force feedback. Standing requires the predictive ability to produce the observed muscle movements preceded (110 +/- 50 ms) by corresponding changes in integrated EMG signal. We suggest higher level anticipatory control is more plausible.

The Journal of Physiology, 2002

The Journal of Physiology, 2011

Human motor control is often explained in terms of engineering &amp;amp;amp;amp;amp;amp;amp;a... more Human motor control is often explained in terms of engineering &amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39;servo&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39; theory. Recently, continuous, optimal control using internal models has emerged as a leading paradigm for voluntary movement. However, these engineering paradigms are designed for high band-width, inflexible, consistent systems whereas human control is low bandwidth and flexible using noisy sensors and actuators. By contrast, engineering intermittent control was designed for bandwidth-limited applications. Our general interest is whether intermittent rather than continuous control is generic to human motor control. Currently, it would be assumed that continuous control is the superior and physiologically natural choice for controlling unstable loads, for example as required for maintaining human balance. Using visuo-manual tracking of an unstable load, we show that control using gentle, intermittent taps is entirely natural and effective. The gentle tapping method resulted in slightly superior position control and velocity minimisation, a reduced feedback time delay, greater robustness to changing actuator gain and equal or greater linearity with respect to the external disturbance. Control was possible with a median contact rate of 0.8±0.3 s(-1). However, when optimising position or velocity regulation, a modal contact rate of 2 s(-1) was observed. This modal rate was consistent with insignificant disturbance-joystick coherence beyond 1-2 Hz in both tapping and continuous contact methods. For this load, these results demonstrate a motor control process of serial ballistic trajectories limited to an optimum rate of 2 s(-1). Consistent with theoretical reasoning, our results suggest that intermittent open loop action is a natural consequence of human physiology.

The Journal of physiology, Jan 26, 2015

Quiet standing is achieved through a combination of active and passive mechanisms, consisting of ... more Quiet standing is achieved through a combination of active and passive mechanisms, consisting of neural control and intrinsic mechanical stiffness of the ankle joint, respectively. The mechanical stiffness is partly determined by the calf muscles. But the visco-elastic properties of muscle are highly labile, exhibiting strong dependence on movement history. Here we determine if this lability has consequences for the passive stabilization of human standing, by measuring the effect of sway history upon ankle stiffness. Ten subjects stood quietly on a rotating platform whose axis was collinear with the ankle joint. Ankle sway was increased by slowly tilting this platform in a random fashion, or decreased by fixing the body to a board. Ankle stiffness was measured by using the same platform to simultaneously apply small, brief perturbations (<0.6 deg; 140 ms), while the resulting torque response was recorded. The results show that increasing sway reduces ankle stiffness by up to 43%,...

ABSTRACT Human physiological hand tremor has a resonant component. Proof of this is that its freq... more ABSTRACT Human physiological hand tremor has a resonant component. Proof of this is that its frequency can be modified by adding mass. However, adding mass also increases the load which must be supported. The necessary force requires muscular contraction which will change motor output and is likely to increase limb stiffness. The increased stiffness will partly offset the effect of the increased mass and this can lead to the erroneous conclusion that factors other than resonance are involved in determining tremor frequency. Using a human centrifuge to increase head-to-foot gravitational field strength, we were able to control for the increased effort by increasing force without changing mass. This revealed that the peak frequency of human hand tremor is 99% predictable on the basis of a resonant mechanism. We ask what, if anything, the peak frequency of physiological tremor can reveal about the operation of the nervous system. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.

J Neurophysiol, 2010

Axelson HW, Hagbarth KE. Human motor control consequences of thixotropic changes in muscular shor... more Axelson HW, Hagbarth KE. Human motor control consequences of thixotropic changes in muscular short-range stiffness. J Physiol 535: 279 -288, 2001. Campbell KS, Lakie M. A cross-bridge mechanism can explain the thixotropic short-range elastic component of relaxed frog skeletal muscle. J Physiol 510: 941-962, 1998. Campbell KS, Moss RL. A thixotropic effect in contracting rabbit psoas muscle: prior movement reduces the initial tension response to stretch. J Physiol 525: 531-548, 2000. Campbell KS, Moss RL. History-dependent mechanical properties of permeabilized rat soleus muscle fibers. Biophys J 82: 929 -943, 2002. Conway BA, Halliday DM, Farmer SF, Shahani U, Maas P, Weir AI, Rosenberg JR. Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J Physiol 489: 917-924, 1995. Dietz V, Bischofberger E, Wita C, Freund HJ. Correlation between the dischanges of two simultaneously recorded motor units and physiological tremor. Electroencephalogr Clin Neurophysiol 40: 97-105, 1976. Elble RJ, Randall JE. Motor-unit activity responsible for 8-to 12-Hz component of human physiological finger tremor. J Neurophysiol 39: 370 -383, 1976. Elble RJ, Randall JE. Mechanistic components of normal hand tremor. Electroencephalogr Clin Neurophysiol 44: 72-82, 1978.

The Journal of physiology, Jan 24, 2015

Human physiological hand tremor has a resonant component. Proof of this is that its frequency can... more Human physiological hand tremor has a resonant component. Proof of this is that its frequency can be modified by adding mass. However, adding mass also increases the load which must be supported. The necessary force requires muscular contraction which will change motor output and is likely to increase limb stiffness. The increased stiffness will partly offset the effect of the increased mass and this can lead to the erroneous conclusion that factors other than resonance are involved in determining tremor frequency. Using a human centrifuge to increase head-to-foot gravitational field strength, we were able to control for the increased effort by increasing force without changing mass. This revealed that the peak frequency of human hand tremor is 99% predictable on the basis of a resonant mechanism. We ask what, if anything, the peak frequency of physiological tremor can reveal about the operation of the nervous system. This article is protected by copyright. All rights reserved.

Journal of neuroscience methods

Automated image tracking provides new insights in many physiological studies, but present methods... more Automated image tracking provides new insights in many physiological studies, but present methods are ad hoc and can be difficult to use. They are generally based on following the movement of one or more specific regions of interested - point tracking. We tested newly available novel planar tracking technology commercially developed for the special effects industry, which does not use point tracking. We validated the tracker and made two dynamic physiological measurements. Our validation measurements describe the accuracy and repeatability of the technique, and our physiological measurements demonstrate the flexibility of the software. Our results suggest that planar tracking may be of particular use with techniques that produce low quality images such as ultrasonography.

Exercise and sport sciences reviews, 2014

Explanation of motor control is dominated by continuous neurophysiological pathways (e.g., transc... more Explanation of motor control is dominated by continuous neurophysiological pathways (e.g., transcortical, spinal) and the continuous control paradigm. Using new theoretical development, methodology, and evidence, we propose intermittent control, which incorporates a serial ballistic process within the main feedback loop, provides a more general and more accurate paradigm necessary to explain attributes highly advantageous for competitive survival and performance.

ABSTRACT In almost every person there is a clear oscillation at ~10 Hz in the limbs under postura... more ABSTRACT In almost every person there is a clear oscillation at ~10 Hz in the limbs under postural conditions. This postural physiological tremor has been investigated and explained in terms of either mechanical influences (e.g. mechanical resonance of the limb), or neural influences (e.g. rhythmicities of central neural firing) (McAuley and Marsden 2000). We recently showed that human physiological tremor has a strongly mechanical basis (Lakie et al, 2010) and largely results from broad band forcing (EMG) of a resonant system. Here we investigate the effect of altering the forcing by making the muscles ischaemic. With ethical permission we recorded tremor of the outstretched splinted middle finger in 12 subjects (11 male) using a 3 axis accelerometer. One slow movement condition and three postural conditions were studied. Ischaemia was produced by an arm cuff inflated to 150 mm Hg for up to 8 minutes. Surface EMG was recorded from the forearm extensor muscles. Records lasted 60 s each and were repeated 4 times over 2 days. Cross spectral gain between rectified EMG and vertical acceleration was subsequently calculated. Acceleration size was greatly reduced by ischaemia. EMG was if anything slightly increased. Accordingly gain was greatly reduced (Fig 1). Ischaemia is known to substantially reduce tremor size (Christakos et al, 2006). This reduction has been attributed to the effect of ischaemia on muscle spindles (Lippold, 1970) or to its effect on muscle contractile properties (Lakie et al, 2004). The reduction in gain that we see in the present experiments strongly supports the latter explanation.

Journal of Neurophysiology, 2014

Two frequency peaks of variable preponderance have been reported for human physiological finger t... more Two frequency peaks of variable preponderance have been reported for human physiological finger tremor. The high-frequency peak (20-25 Hz, seen only in postural tremor) is generally attributed to mechanical resonance, whereas the lower frequency peak (8-12 Hz, seen in both postural and kinetic tremor) is usually attributed to synchronous central or reflexive neural drive. In this study, we determine whether mechanical resonance could generate both peaks. In relaxed subjects, an artificial finger tremor was evoked by random mechanical perturbations of the middle finger or random electrical muscular stimulation of the finger extensor muscle. The high and the low frequencies observed in physiological tremor could both be created by either type of artificial input at appropriate input intensity. Resonance, inferred from cross-spectral gain and phase, occurred at both frequencies. To determine any neural contribution, we compared truly passive subjects with those who exhibited some electromyographic (EMG) activity in the finger extensor; artificially created tremor spectra were almost identical between groups. We also applied electrical stimuli to two clinically deafferented subjects lacking stretch reflexes. They exhibited the same artificial tremor spectrum as control subjects. These results suggest that both typical physiological finger tremor frequencies can be reproduced by random artificial input; neither requires synchronized neural input. We therefore suggest that mechanical resonance could generate both dominant frequency peaks characteristic of physiological finger tremor. The inverse relationship between the input intensity and the resulting tremor frequency can be explained by a movement-dependent reduction in muscle stiffness, a conjecture we support using a simple computational model.

Experimental Physiology, 1994

Ethanol reduces the size of essential tremor. We here show that, contrary to a recent report, eth... more Ethanol reduces the size of essential tremor. We here show that, contrary to a recent report, ethanol also causes a large decrease in the size of physiological tremor. As in the case of essential tremor, the frequency is not changed. The reduction in tremor probably explains the well-known link between certain types of skilled activity and alcohol consumption.

The Journal of Physiology, 2012

Limb resonance imparts a characteristic spectrum to hand tremor. Movement will alter the resonanc... more Limb resonance imparts a characteristic spectrum to hand tremor. Movement will alter the resonance. We have examined the consequences of this change. Rectified forearm extensor muscle EMG and physiological hand tremor were recorded. In postural conditions the EMG spectrum is relatively flat whereas the acceleration spectrum is sharply peaked. Consequently, the gain between EMG and acceleration is maximal at the frequency where the tremor is largest (∼8 Hz). The shape of the gain curve implies mechanical resonance. Substantial alterations in posture do not significantly change the characteristics of the tremor or the shape or size of the gain curve. By contrast, slow or moderately paced voluntary wrist flexion–extension movements dramatically increase the hand tremor size and lower its peak frequency. These changes in size and frequency of the tremor cannot be attributed to changes in the EMG. Instead they reflect a very large change in the size and shape of the gain curve relating EMG to acceleration. The gain becomes larger and the peak moves to a lower frequency (∼6 Hz). We suggest that a movement-related (thixotropic) alteration in resonant properties of the wrist provides a simple explanation for these changes. The mechanism is illustrated by a model. Our new findings confirm that resonance plays a major role in wrist tremor. We also demonstrate that muscles operate very differently under postural and dynamic conditions. The different coupling between EMG and movement in posture and when moving must pose a considerable challenge for neural predictive control of skeletal muscles.

The Journal of Physiology, 1998

The precise control of posture and movement imposes severe constraints on the human neuromuscular... more The precise control of posture and movement imposes severe constraints on the human neuromuscular system. In particular, to maintain stability, the motor control system must continually react to proprioceptive feedback as the body is perturbed by unpredictable external forces. In this type of control mechanism there is an inevitable time delay (due to e.g. nerve conduction and electromechanical coupling) between the sensing of the perturbation and the completion of the corrective movement. The delays in the feedback loop are destabilizing and may result in tremulous movement . A small resistance to movement inherent in the muscle fibres themselves would provide 1. The passive tension and sarcomere length of relaxed frog skeletal muscle fibres were measured in response to imposed length stretches. The tension response to a constantvelocity stretch exhibited a clear discontinuity. Tension rose more rapidly during the initial • 0·4 % LÑ of the stretch than during the latter stages (where LÑ is the resting length of the fibre). This initial tension response is attributed to the short-range elastic component (SREC). 2. The use of paired triangular stretches revealed that the maximum tension produced during the SREC response of the second stretch was significantly reduced by the first stretch. This history-dependent behaviour of the SREC reflects thixotropic stiffness changes that have been previously described in relaxed muscle. 3. The biphasic nature of the SREC tension response to movement was most apparent during the first imposed length change after a period at a fixed length, irrespective of the direction of movement. 4. If a relaxed muscle was subjected to an imposed triangular length change so that the muscle was initially stretched and subsequently shortened back to its original fibre length, the resting tension at the end of the stretch was reduced relative to its initial pre-stretch value. Following the end of the stretch, tension slowly increased towards its initial value but the tension recovery was not accompanied by a contemporaneous increase in sarcomere length. This finding suggests that the resting tension of a relaxed muscle fibre is not entirely due to passive elasticity. The results are compatible with the suggestion that a portion of the resting tension -the filamentary resting tension (FRT) -is produced by a low level of active force generation. 5. If a second identical stretch was imposed on the muscle at a time when the resting tension was reduced by the previous stretch, the maximal tension produced during the second stretch was the same as that produced during the first, despite the second stretch commencing from a lower initial resting tension. 6. In experiments using paired triangular length changes, an inter-stretch interval of zero did not produce a substantially greater thixotropic reduction in the second stretch elastic limit force than an inter-stretch interval in the range 0·5-1 s. 7. A theoretical model was developed in which the SREC and FRT arise as manifestations of a small number of slowly cycling cross-bridges linking the actin and myosin filaments of a relaxed skeletal muscle. The predictions of the model are compatible with many of the experimental observations. If the SREC and FRT are indeed due to cross-bridge activity, the model suggests that the cross-bridge attachment rate must increase during interfilamentary movement. A mechanism (based on misregistration between the actin binding sites and the myosin cross-bridges) by which this might arise is presented. 7399 Single intact iliofibularis muscle fibre. Stretch length • 0·011 LÑ. Stretch velocity • 0·011 LÑ s¢. The fibre had been held at a constant length for 1 min before the first stretch was initiated. Temperature 5·0°C.

The Journal of Physiology, 2002

During quiet standing the human &amp;amp;amp;amp;amp;amp;amp;amp;quot;inverted pendulum&a... more During quiet standing the human &amp;amp;amp;amp;amp;amp;amp;amp;quot;inverted pendulum&amp;amp;amp;amp;amp;amp;amp;amp;quot; sways irregularly. In previous work where subjects balanced a real inverted pendulum, we investigated what contribution the intrinsic mechanical ankle stiffness makes to achieve stability. Using the results of a plausible model, we suggested that intrinsic ankle stiffness is inadequate for providing stability. Here, using a piezo-electric translator we applied small, unobtrusive mechanical perturbations to the foot while the subject was standing freely. These short duration perturbations had a similar size and velocity to movements which occur naturally during quiet standing, and they produced no evidence of any stretch reflex response in soleus, or gastrocnemius. Direct measurement confirms our earlier conclusion; intrinsic ankle stiffness is not quite sufficient to stabilise the body or pendulum. On average the directly determined intrinsic stiffness is 91 +/- 23 % (mean +/- S.D.) of that necessary to provide minimal stabilisation. The stiffness was substantially constant, increasing only slightly with ankle torque. This stiffness cannot be neurally regulated in quiet standing. Thus we attribute this stiffness to the foot, Achilles&amp;amp;amp;amp;amp;amp;amp;amp;#39; tendon and aponeurosis rather than the activated calf muscle fibres. Our measurements suggest that the triceps surae muscles maintain balance via a spring-like element which is itself too compliant to guarantee stability. The implication is that the brain cannot set ankle stiffness and then ignore the control task because additional modulation of torque is required to maintain balance. We suggest that the triceps surae muscles maintain balance by predictively controlling the proximal offset of the spring-like element in a ballistic-like manner.

The Journal of Physiology, 2001

Using the ankle musculature, subjects balanced a large inverted pendulum. The equilibrium of the ... more Using the ankle musculature, subjects balanced a large inverted pendulum. The equilibrium of the pendulum is unstable and quasi-regular sway was observed like that in quiet standing. Two main questions were addressed. Can subjects systematically change sway size in response to instruction and availability of visual feedback? If so, do subjects decrease sway size by increasing ankle impedance or by some alternative mechanism? The position of the pendulum, the torque generated at each ankle and the soleus and tibialis anterior EMG were recorded. Results showed that subjects could significantly reduce the mean sway size of the pendulum by giving full attention to that goal. With visual feedback sway size could be minimised significantly more than without visual feedback. In changing sway size, the frequency of the sways was not changed. Results also revealed that ankle impedance and muscle co-contraction were not significantly changed when the sway size was decreased. As the ankle impedance and sway frequency do not change when the sway size is decreased, this implies no change in ankle stiffness or viscosity. Increasing ankle impedance, stiffness or viscosity are not the only methods by which sway size could be reduced. A reduction in torque noise or torque inaccuracy via a predictive process which provides active damping could reduce sway size without changing ankle impedance and is plausible given the data. Such a strategy involving motion recognition and generation of an accurate motor response may require higher levels of control than changing ankle impedance by altering reflex or feedforward gain.

The Journal of Physiology, 2005

The Journal of Physiology, 2006

Ten subjects balanced their own body or a mechanically equivalent unstable inverted pendulum by h... more Ten subjects balanced their own body or a mechanically equivalent unstable inverted pendulum by hand, through a compliant spring linkage. Their balancing process was always characterized by repeated small reciprocating hand movements. These bias adjustments were an observable sign of intermittent alterations in neural output. On average, the adjustments occurred at intervals of approximately 400 ms. To generate appropriate stabilizing bias adjustments, sensory information about body or load movement is needed. Subjects used visual, vestibular or proprioceptive sensation alone and in combination to perform the tasks. We first ask, is the time between adjustments (bias duration) sensory specific? Vision is associated with slow responses. Other senses involved with balance are known to be faster. Our second question is; does bias duration depend on sensory abundance? An appropriate bias adjustment cannot occur until unplanned motion is unambiguously perceived (a sensory threshold). The addition of more sensory data should therefore expedite action, decreasing the mean bias adjustment duration. Statistical analysis showed that (1) the mean bias adjustment duration was remarkably independent of the sensory modality and (2) the addition of one or two sensory modalities made a small, but significant, decrease in the mean bias adjustment duration. Thus, a threshold effect can alter only a very minor part of the bias duration. The bias adjustment duration in manual balancing must reflect something more than visual sensation and perceptual thresholds; our suggestion is that it is a common central motor planning process. We predict that similar processes may be identified in the control of standing.

The Journal of Physiology, 2005

It has been widely assumed for nearly a century, that postural muscles operate in a spring-like m... more It has been widely assumed for nearly a century, that postural muscles operate in a spring-like manner and that muscle length signals joint angle (the mechano-reflex mechanism). Here we employ automated analysis of ultrasound images to resolve calf muscle (soleus and gastrocnemius) length changes as small as 10 µm in standing subjects. Previously, we have used balancing of a real inverted pendulum to make predictions about human standing. Here we test and confirm these predictions on 10 subjects standing quietly. We show that on average the calf muscles are actively adjusted 2.6 times per second and 2.8 times per unidirectional sway of the body centre of mass (CoM). These alternating, small (30-300 µm) movements provide impulsive, ballistic regulation of CoM movement. The timing and pattern of these adjustments are consistent with multisensory integration of all information regarding motion of the CoM, pattern recognition, prediction and planning using internal models and are not consistent with control solely by local reflexes. Because the system is unstable, errors in stabilization provide a perturbation which grows into a sway which has to be reacted to and corrected. Sagittal sway results from this impulsive control of calf muscle activity rather than internal sources (e.g. the heart, breathing). This process is quite unlike the mechano-reflex paradigm. We suggest that standing is a skilled, trial and error activity that improves with experience and is automated (possibly by the cerebellum). These results complement and extend our recent demonstration that paradoxical muscle movements are the norm in human standing.

The Journal of Physiology, 2005

In humans, during standing the calf muscles soleus and gastrocnemius actively prevent forward top... more In humans, during standing the calf muscles soleus and gastrocnemius actively prevent forward toppling about the ankles. It has been generally assumed that these postural muscles behave like springs with dynamic stiffness reflecting their mechanical properties, reflex gain including higher derivatives, and central control. Here, for the first time, we have used an ultrasound scanner and automated image analysis to record the tiny muscular movements occurring in normal standing. This new, non-invasive technique resolves changes in muscle length as small as 10 mum without disturbing the standing process. This technical achievement has allowed us to test the long-established mechano-reflex, muscle spring hypothesis that muscle length changes in a spring-like way during sway of the body. Our results contradict that hypothesis. Muscle length changes in a non-spring-like manner: on average, shortening during forward sway and lengthening during backwards sway (paradoxical movements). This counter-intuitive result is a consequence of the fact that calf muscles generate tension through a series elastic component (SEC, Achilles tendon and foot) which limits maximal ankle stiffness to 92 +/- 20% of that required to balance the body. Paradoxical movements cannot be generated by stretch reflexes with constant intrafusal drive but might be produced by reflex coupling of extrafusal (alpha) and intrafusal (beta, gamma) drive or by positive force feedback. Standing requires the predictive ability to produce the observed muscle movements preceded (110 +/- 50 ms) by corresponding changes in integrated EMG signal. We suggest higher level anticipatory control is more plausible.

The Journal of Physiology, 2002

The Journal of Physiology, 2011

Human motor control is often explained in terms of engineering &amp;amp;amp;amp;amp;amp;amp;a... more Human motor control is often explained in terms of engineering &amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39;servo&amp;amp;amp;amp;amp;amp;amp;amp;amp;amp;#39; theory. Recently, continuous, optimal control using internal models has emerged as a leading paradigm for voluntary movement. However, these engineering paradigms are designed for high band-width, inflexible, consistent systems whereas human control is low bandwidth and flexible using noisy sensors and actuators. By contrast, engineering intermittent control was designed for bandwidth-limited applications. Our general interest is whether intermittent rather than continuous control is generic to human motor control. Currently, it would be assumed that continuous control is the superior and physiologically natural choice for controlling unstable loads, for example as required for maintaining human balance. Using visuo-manual tracking of an unstable load, we show that control using gentle, intermittent taps is entirely natural and effective. The gentle tapping method resulted in slightly superior position control and velocity minimisation, a reduced feedback time delay, greater robustness to changing actuator gain and equal or greater linearity with respect to the external disturbance. Control was possible with a median contact rate of 0.8±0.3 s(-1). However, when optimising position or velocity regulation, a modal contact rate of 2 s(-1) was observed. This modal rate was consistent with insignificant disturbance-joystick coherence beyond 1-2 Hz in both tapping and continuous contact methods. For this load, these results demonstrate a motor control process of serial ballistic trajectories limited to an optimum rate of 2 s(-1). Consistent with theoretical reasoning, our results suggest that intermittent open loop action is a natural consequence of human physiology.