Review Proprioceptive control of posture: a review of new concepts

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Gait and Posture 8 (1998) Review Proprioceptive control of posture: a review of new concepts J.H.J. Allum a, *, B.R. Bloem b, M.G. Carpenter c, M. Hulliger d, M. Hadders-Algra e a Department of
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Gait and Posture 8 (1998) Review Proprioceptive control of posture: a review of new concepts J.H.J. Allum a, *, B.R. Bloem b, M.G. Carpenter c, M. Hulliger d, M. Hadders-Algra e a Department of ORL, Uni ersity Hospital, Basel, Switzerland b Department of Neurology, Leiden Uni ersity Medical Center, Leiden, The Netherlands c Department of Kinesiology, Uni ersity of Waterloo, Waterloo, Ont., Canada d Department of Clinical Neurosciences, Uni ersity of Calgary, Calgery, Alta., Canada e Department Medical Physiology, Uni ersity of Groningen, Groningen, The Netherlands Received 26 February 1998; received in revised form 27 May 1998; accepted 8 June 1998 Abstract The assumption that proprioceptive inputs from the lower legs are used to trigger balance and gait movements is questioned in this review (an outgrowth of discussions initiated during the Neural Control of Movement Satellite meeting held in Cozumel, Mexico, April 1997). Recent findings presented here suggest that trunk or hip inputs may be more important in triggering human balance corrections and that proprioceptive input from the lower legs mainly helps with the final shaping and intermuscular coordination of postural and gait movements. Three major questions were considered. First, what role, if any, do lower-leg proprioceptive inputs play in the triggering of normal balance corrections? If this role is negligible, which alternative proprioceptive inputs then trigger balance corrections? Second, what is the effect of proprioceptive loss on the triggering of postural and gait movements? Third, how does proprioceptive loss affect the output of central pattern generators in providing the final shaping of postural movements? The authors conclude that postural and gait movements are centrally organized at two levels. The first level involves the generation of the basic directionally-specific response pattern based primarily on hip or trunk proprioceptive input and secondarily on vestibular inputs. This pattern specifies the spatial characteristics of muscle activation, that is which muscles are primarily activated, as well as intermuscular timing, or the sequence in which muscles are activated. The second level is involved in the shaping of centrally set activation patterns on the basis of multi-sensorial afferent input (including proprioceptive input from all body segments and vestibular sensors) in order that movements can adapt to different task conditions Elsevier Science B.V. All rights reserved. Keywords: Balance corrections; Infant development; Leg movements; Locomotion; Postural control; Proprioceptive feedback; Sensory neuropathy Introduction Our present concepts regarding the influence of normal proprioceptive function (propriocepsis) on human postural responses stem, first of all, from clinical observations. Epidemiological surveys have established that a reduction of leg propriocepsis is a risk factor for falls in the elderly [82,102,115]. The importance of intact * Corresponding author. Present address: University HNO-Klinik, Petersgraben 4, CH-4031 Basel, Switzerland. Tel.: ; fax: ; propriocepsis for maintaining upright stance is further underscored by the sometimes devastating clinical consequences induced by a loss of propriocepsis, for example in patients with peripheral neuropathy. The resultant balance disorder can be very impressive, and accounts of such patients continue to reach not only the scientific literature [25,30,47], but also the popular press [38,107]. These clinical observations raise a number of scientific questions: If our footing slips, we trip on some unforeseen obstacle, or if we miss a stairway step, is the ensuing proprioceptive information from the ankle joints the most important factor shaping the balance /98/$ - see front matter 1998 Elsevier Science B.V. All rights reserved. PII S (98) J.H.J. Allum et al. / Gait and Posture 8 (1998) correction or are other sensory inputs, more directly related to the primary task of posture and gait, to maintain a stable torso of greater importance? If proprioceptive signals from other joints such as the knee, hip and neck together with vestibular signals are more important in triggering and modulating balance corrections, how does ankle proprioceptive input contribute to balance corrections and modify gait patterns? Given that the central nervous system (CNS) must integrate these sensory signals together to yield a single motor output how is the process acquired during development or reacquired following sensory loss? These and related questions are explored in five original contributions which examined the role of proprioceptive inputs in the control of posture and gait. These contributions examined: 1. The interactions between proprioceptive and vestibular inputs in generating human balance corrections; 2. how these trunk proprioceptive and vestibular interactions change balance corrections in different directions; 3. the changes in balance corrections caused by loss of proprioceptive input from the lower legs; 4. the changes in gait coordination in cats caused by global proprioceptive loss; 5. how the developing human infant gradually develops a fixed pattern of balance corrections appropriate for the direction of perturbed trunk motion. The quintessence of these contributions is that ankle proprioceptive inputs are not essential for triggering balance corrections and gait movements but may play some role in shaping the final form of the muscle synergy underlying both types of movements. The new synthesis presented in these contributions highlights the control by CNS in the selection of appropriate balance correcting and gait timing and amplitude patterns. This central processing implies a central synthesis of relevant afferent information which could be simplified by relegating one or more parts of this task to central pattern generators (CPG). One of these task simplifications would be for the CPG to select the basic timing of postural responses of balance corrections [42] prior to selection of the response scaling at different muscles. Allum et al. [7] have argued that in man this timing pattern selection is set on the basis of a number of links that the body is forced to move with at the onset of a balance disturbance. For example, if the disturbance forces the knees into a locked position so that the legs move as one rather than two elements, it is to be expected that trunk, knee and ankle muscles will provide different proprioceptive trigger signals than if the knees are not locked but flexing. Another way the CNS may simplify the task of computing the correct amplitude response shaping is to pre-weight groups of muscles to receive more proprioceptive or more vestibular weighting. Presumably the selection of which muscles are more shaped by vestibular inputs and which have emphasized proprioceptive weighting during the control of trunk forward pitching preventing total body rearward falling, is based on a learning process in early infancy in which the growing infant employs these muscles to prevent a backwards fall as Hadders and Forssberg [58 60] point out in their contribution. The fact that subjects who suffer vestibular loss or proprioceptive loss as adults cannot switch this weighting between muscles to prevent a fall even after years of experience controlling falls [12], implies that this basic level of pre-processing of balance corrections cannot be modified and is pre-set. Thus, the final central computation of the metrics of the balance-correcting synergy would be the selection of a base-level amplitude of muscle activation about which proprioceptive and vestibular inputs would interact by increasing or decreasing this base-level of activation. We hypothesize that this basic activation level is rapidly selected using prediction of the amplitudes with which the trunk and legs will move as the balance correction occurs. With this organization sequence the CNS would have the advantage of a rapid reaction to any postural disturbance and have computational freedom to make minor postural adjustments during the following stabilizing period when the body is repositioned in a new upright position with low levels of muscle activity. Originally, it was proposed that for balance corrections ankle inputs trigger responses in stretched lowerleg muscles and that this trigger signal is then transmitted in a distal-to-proximal fashion upwards to elicit a balance-correcting muscle response synergy with onsets of ms across a number of links [36,68,94,95]. The movement of the body which resulted was attributed to resemble the action of an inverted pendulum-the so-called ankle strategy [67]. The first feature of this concept that was called into question concerns the distal-to-proximal triggered activation of automatic balance-correcting muscle responses. Allum et al., and Keshner et al. [7,75] used similar supportsurface induced balance perturbations noted triggered responses in the trunk and neck muscles that occurred at the same time as the proposed triggering response at 100 ms in gastrocnemius [67,94]. Moreover, the proposed triggering response at 100 ms in gastrocnemius is delayed compared with the earlier 50 ms latency of soleus muscles to stretch of the ankle muscles and the next response observed at 80 ms in stretched quadriceps muscles [7]. Thus, it appears that proprioceptive reflex systems in other than the ankle muscles could well trigger postural responses with onsets of ms. Following this line of reasoning, a number of authors have suggested that rotation of the trunk [9,42] rotation of the knee [7] or more distally, stretch of the intrinsic foot muscles [113] could trigger postural responses. It 216 J.H.J. Allum et al. / Gait and Posture 8 (1998) was therefore, the role of proprioceptive signals other than those from the ankle joint which we wished to explore in this set of contributions. Patterns of proprioceptive and vestibular interactions underlying human balance corrections J.H.J. Allum, F. Honegger Department of ORL, Uni ersity Hospital, Basel, Switzerland Balance corrections must be triggered from sensory sources which early and reliably detect the disturbance to the upright stance. Ideally, this sensory information would also be employed to establish the timing and metrics of balance corrections. Instability in human balance can be registered very early by proprioceptive sensory systems responding to motion and muscle stretch at the ankle, knee and trunk joints, as well as by head linear and angular accelerations [7]. Once balance corrections are triggered it is generally accepted that a confluence of proprioceptive and vestibular modulation to the basic centrally initiated template of activity establishes the amplitude pattern of the muscle response synergy [9,35,42,70]. Visual inputs appear to primarily influence later stabilizing reactions to the initial balance corrections [5,7,74]. It is generally assumed that the contributions of one sensory input can be assessed by testing subjects suffering from a deficit of the to-betested sensory input [9,42,71], or by perturbing one sensory input alone while holding the others constant [12,36,41] or by perturbing one sensory input a constant amount and allowing other inputs to vary [6,7]. Most of these techniques have inherent disadvantages as we will document. The deficit approach assumes, for example, that absence of vestibular input does not affect proprioceptive stretch reflexes prior to balance corrections and therefore the body movements and proprioceptive modulation during balance corrections. Furthermore, when perturbing one sensory input alone, the metrics of the perturbation are seldom exactly those encountered during a stance disturbance with multiple inputs. Lastly multiple sensory inputs, for example, trunk and vestibular inputs, may be required for a third input at the knee to have a fully developed modulating effect. By specifically controlling for variations at the ankle and knee joints, and comparing responses of normal and vestibular-loss subjects to stance perturbations we hoped to overcome some of these disadvantages and shed some light onto the complexity of proprioceptive and vestibular interactions during balance corrections. 1. Methods The techniques used to probe balance control mechanisms in human subjects have been described in Refs. [5,7]. Subjects stood on a support-surface which could either rotate about the ankle joints or translate horizontally. Stimuli consisted of one of three types of balance perturbations which were presented in random order 10 times for a total of 30 in a series. The first series was presented under eyes-open conditions and, after a 5 10 min pause, the second identical series was presented with eyes closed. The three types of stimuli were 4 dorsi-flexion rotation ( normal ankle angle protocol), or a combined 4 cm rearward translation and 4 plantar-flexion rotation to yield approximately 0 of ankle dorsi-flexion ( nulled ankle angle protocol), or a combined 4 cm rearward translation and 4 dorsi-flexion to yield approximately 6 of ankle dorsi-flexion ( enhanced ankle angle protocol). Stimulus durations were 150 ms. Over the first 200 ms of the nulled and enhanced ankle angle protocols, a separate microprocessor provided extra servo-rotation of the support-surface. The purpose of this rotation was to keep ankle angle as measured between the lower-leg and the support-surface zero for the nulled protocol and equal to the average measured profile of normals for the enhanced protocol. The subjects (15 normal subjects and five otherwise healthy subjects who had a bilateral peripheral vestibular deficit) were asked to return to upright as quickly as possible in response to each stimulus. Several measurements were recorded as in previous studies in the pitch plane: trunk angular velocity (Watson Industries 200 /s range, 50 Hz bandwidth); upper leg angular velocity (Watson Industries 100 /s range); lower leg angle with respect to vertical (using a potentiometer system); and ankle torque about the left and right ankle joints (from the outputs of strain gauges imbedded in the support-surface). Surface electromyographic (EMG) recordings were obtained from the left and right tibialis anterior (TA) and soleus muscles, and from the right medial gastrocnemius, right quadriceps, paraspinals (PARAS) and upper trapezius (TRAP) muscles, using pairs of surface electrodes placed 3 cm apart along the muscle belly. For data analysis purposes, the first three responses were ignored to avoid adaptation effects entering population responses [74]. The remaining nine responses from each subject to the same rotation translation protocol were averaged together once a zero latency for the responses had been defined. Zero latency (stimulus onset) was defined using the computed velocity of ankle dorsi-flexion. The first inflexion of this velocity trace was used as zero latency (the vertical line at 0 ms in Fig. 1). Average responses from all subjects in the same population tested under the same condition (eyes open J.H.J. Allum et al. / Gait and Posture 8 (1998) Fig. 1. Differences between the responses of normal and vestibular-loss subjects to a simultaneous rearward translation and dorsi-flexion of the support-surface yielding a 6 ankle dorsi-flexion. The balance correcting responses in soleus and gastrocnemius are not altered by vestibular loss but those of paraspinals are profoundly changed. Muscle activation patterns of five subjects with bilateral peripheral vestibular-loss (thick traces) are compared to the average responses of 15 normal subjects (thin traces). The traces are aligned in time with the first deflection of ankle angular velocity (similar to the first deflection in ankle torque). Rearward rotations of angles and angular velocities are plotted as positive (upward) deflection of traces as is decreased ankle torque on the platform. The insert shows the time course of head linear and angular accelerations over the first 150 ms. Upward linear accelerations are plotted as a positive trace deflections as is head backwards pitching angular acceleration. Other methodological details may be found in Ref. [12]. 218 J.H.J. Allum et al. / Gait and Posture 8 (1998) or closed) were used to create the population averages shown in Fig Results This report concentrates on the responses to combined rearward translation and dorsi-flexion rotation of the support-surface ( enhanced ankle angle protocol). As Fig. 1 shows this produced identical profiles of a rapid 6 ankle flexion, identical traces of first a knee flexion followed by a rapid knee extension as the upper leg rotated forward, and similar ankle torque recordings over the first 200 ms for the two populations and conditions. Despite these identical lower and upper leg movement profiles significant differences were observed in the way muscle activity was modulated following vestibular loss. Furthermore, trunk angular velocity traces had dissimilar profiles for normal and vestibularloss subjects and were accompanied by paraspinal responses different in latency and amplitude modulation. The differences (or lack thereof) between the muscle activity in normal and vestibular-loss subjects could be classified into three types of modulation. Triceps surae muscles were not influenced by vestibular loss. Fig. 1 shows that the soleus and gastrocnemius activity were practically overlapping in both normal and vestibularloss subjects for eyes open and closed conditions. The activity consisted of two bursts, the first at 56 ms was larger in amplitude in soleus, and the second at 106 ms was larger in amplitude in gastrocnemius. These onset latencies are for normals with eyes closed. The onset latencies were on average 2 ms, respectively, 5 ms shorter for vestibular-loss subjects. The earlier onset in vestibular-loss subjects was probably due to the slightly forward leaning posture adopted by these subjects as can be observed from the increased baseline activity in soleus over the 100 ms prior to the stimulus onset. It is worth noting that the difference in latency onsets of the first and second burst of triceps surae activity is similar to the latency of onset of upper leg rotation suggesting that the second burst of activity may be a stretch reflex response to knee reextension. The second type of vestibular modulation pattern appeared in quadriceps. It consisted of a triphasic change in the difference between normal and vestibularloss responses. The most noticeable aspect of the response difference was the change in the amplitude of the stretch reflex response in quadriceps induced by knee flexion. The amplitude of this activity commencing at 80 ms was reduced in patients compared to controls during the time that the head was accelerated downwards (see insert at the top right of Fig. 1). Responses in TA, PARAS and TRAP muscles presented a third type of modulation. The pattern was characterised by an early reduction in activity after 120 ms in the muscle responses of vestibular-loss subjects, followed by a major increase in activity. Although there was no significant shift in latency for TA and TRAP muscles, the overall impression was a shift in the onset of the balance correcting responses in vestibular-loss subjects. This overall impression could be confirmed in the case of PARAS as latencies of the balance correcting responses were significantly later, some 22 ms on average. This change was accompanied by a reduction in the early extension velocity of the trunk and by an elongation of the period of early decreased PARAS activity present for vestibular-loss subjects. That is, the early decreased activity commencing at ca. 80 ms is an unloading reflex caused by early trunk extension. The main effect of the balance correcting activity in PARAS is presumably to break the forward flexion of the trunk. As this is some 30% faster at 250 ms in vestibular-loss subjec
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