Biomedical subjects

Martin Lakie

Publications and source records attributed to Martin Lakie.

9 recordsLinked to original sources

PubMed2006

The frequency of human, manual adjustments in balancing an inverted pendulum is constrained by intrinsic physiological factors.

While standing naturally and when manually or pedally balancing an equivalent inverted pendulum, the load sways slowly (characteristic unidirectional duration approximately 1 s) and the controller, calf muscles or hand, makes more frequent adjustments (characteristic unidirectional duration 400 ms). Here we test the hypothesis that these durations reflect load properties rather than some intrinsic property of the human neuromuscular system. Using a specialized set-up mechanically analogous to real standing, subjects manually balanced inverted pendulums with different moments of inertia through a compliant spring representing the Achilles tendon. The spring bias was controlled by a sensitive joystick via a servo motor and accurate visual feedback was provided on an oscilloscope. As moment of inertia decreased, inverted pendulum sway size increased and it became difficult to sustain successful balance. The mean duration of unidirectional balance adjustments did not change. Moreover, the mean duration of unidirectional inverted pendulum sway reduced only slightly, remaining around 1 s. The simplest explanation is that balance was maintained by a process of manual adjustments intrinsically limited to a mean frequency of two to three unidirectional adjustments per second corresponding to intermittent control observed in manual tracking experiments. Consequently the inverted pendulum sway duration, mechanically related to the bias duration, reflects an intrinsic constraint of the neuromuscular control system. Given the similar durations of sway and muscle adjustments observed in real standing, we postulate that the characteristic duration of unidirectional standing sway reflects intrinsic intermittent control rather than the inertial properties of the body.

Adult↗

PubMed2006

Manually controlled human balancing using visual, vestibular and proprioceptive senses involves a common, low frequency neural process.

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.

Adult↗

PubMed2005

Use of ultrasound to make noninvasive in vivo measurement of continuous changes in human muscle contractile length.

Continuous measurement of contractile length has been traditionally achieved using animal preparations in which the muscle and tendon are exposed. More modern methods, e.g., sonomicroscopy, are still invasive. There is a widely perceived need for a noninvasive, in vivo method of measuring continuous changes of human muscle contractile length. Ultrasonography has been used for several years to measure relatively static, discrete changes in tendon, aponeurosis, and muscle fascicle length. We have recently developed this technique to continuously track changes in muscle contractile length during quiet standing. Here, we present the tracking algorithm and use externally applied perturbations to establish the spatial and temporal resolution of the technique. Subjects maintained a low level of ankle torque while a pneumatic actuator applied rapid, square-pulse ankle rotations of defined magnitude and 0.2-s duration. Tracked changes in gastrocnemius and soleus contractile length follow the temporal profile of the perturbations and scale progressively (5-400 microm) with the size of the ankle rotation (0.03-0.7 degrees ). In a second experiment, we tracked a wire oscillating in water with known peak to peak amplitudes of 1.5 microm to 8 mm. The ultrasound tracking procedure had near 100% accuracy at all amplitudes for frequencies up to 3 Hz and showed attenuation at higher frequencies consistent with an effective sampling frequency of 12 Hz and sampling time of 80 ms. This noninvasive technique is sensitive, without averaging, to changes as small as 1 microm and is suitable for observing neuromotor activity in posture and locomotion.

Adult↗

PubMed2005

Active, non-spring-like muscle movements in human postural sway: how might paradoxical changes in muscle length be produced?

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.

Adult↗

PubMed2005

Human postural sway results from frequent, ballistic bias impulses by soleus and gastrocnemius.

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 mum 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 microm) 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.

Adult↗

PubMed2004

Paradoxical muscle movement in human standing.

In human standing, gravity causes forward toppling about the ankle joint which is prevented by activity in the soleus and gastrocnemius muscles. It has long been assumed that when people sway forwards the calf muscles are stretched and conversely that they shorten with backward sway. Consequently, for many years, two explanations for standing stabilization have flourished. First, tonic muscle activity itself may generate adequate intrinsic ankle stiffness. Second, if intrinsic ankle stiffness is inadequate, the resistance to stretch of the calf muscles may be augmented by stretch reflexes or by central control. These explanations require that the passive tissue (Achilles' tendon, foot) transmitting the calf muscle tension is stiff. However, our recent measurements have indicated that this passive tissue is not stiff during standing. Accordingly, we predicted a counterintuitive mode of control where the muscles and body must, on average, move in opposite directions (paradoxical movements). Here we use dynamic ultrasound imaging in vivo with novel automated tracking of muscle length to test our hypothesis. We show that soleus and gastrocnemius do indeed move paradoxically, shortening when the body sways forward and lengthening when the body returns. This confirms that intrinsic ankle stiffness is too low to stabilize human standing. Moreover, it shows that the increase in active tension is associated with muscle shortening. This pattern cannot be produced by muscle stretch reflexes and can only arise from the anticipatory neural control of muscle length that is necessary for balance.

Achilles Tendon↗

PubMed2003

Human balancing of an inverted pendulum with a compliant linkage: neural control by anticipatory intermittent bias.

These experiments were prompted by the recent discovery that the intrinsic stiffness of the ankle is inadequate to stabilise passively the body in standing. Our hope was that showing how a large inverted pendulum was manually balanced with low intrinsic stiffness would elucidate the active control of human standing. The results show that the pendulum can be satisfactorily stabilised when intrinsic stiffness is low. Analysis of sway size shows that intrinsic stiffness actually plays little part in stabilisation. The sway duration is also substantially independent of intrinsic stiffness. This suggests that the characteristic sway of the pendulum, rather than being dictated by stiffness and inertia, may result from the control pattern of hand movements. The key points revealed by these experiments are that with low intrinsic stiffness the hand provides pendulum stability by intermittently altering the bias of the spring and, on average, the hand moves in opposition to the load. The results lead to a new and testable hypothesis; namely that in standing, the calf muscle shortens as the body sways forward and lengthens as it sways backwards. These findings are difficult to reconcile with stretch reflex control of the pendulum and are of particular relevance to standing. They may also be relevant to postural maintenance in general whenever the CNS controls muscles which operate through compliant linkages. The results also suggest that in standing, rather than providing passive stability, the intrinsic stiffness acts as an energy efficient buffer which provides decoupling between muscle and body.

Adult↗

PubMed2002

Direct measurement of human ankle stiffness during quiet standing: the intrinsic mechanical stiffness is insufficient for stability.

During quiet standing the human "inverted pendulum" 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' 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.

Adult↗

PubMed2002

Human balancing of an inverted pendulum: position control by small, ballistic-like, throw and catch movements.

In standing, there are small sways of the body. Our interest is to use an artificial task to illuminate the mechanisms underlying the sways and to account for changes in their size. 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. By giving full attention to minimising sway subjects could systematically reduce pendulum movement. The pendulum position, the torque generated at each ankle and the soleus and tibialis anterior EMGs were recorded. Explanations about how the human inverted pendulum is balanced usually ignore the fact that balance is maintained over a range of angles and not just at one angle. Any resting equilibrium position of the pendulum is unstable and in practice temporary; movement to a different resting equilibrium position can only be accomplished by a biphasic 'throw and catch' pattern of torque and not by an elastic mechanism. Results showed that balance was achieved by the constant repetition of a neurally generated ballistic-like biphasic pattern of torque which can control both position and sway size. A decomposition technique revealed that there was a substantial contribution to changes in torque from intrinsic mechanical ankle stiffness; however, by itself this was insufficient to maintain balance or to control position. Minimisation of sway size was caused by improvement in the accuracy of the anticipatory torque impulses. We hypothesise that examination of centre of mass and centre of pressure data for quiet standing will duplicate these results.

Adult↗