Stefania Sozzi

Sensorimotor integration during stance: Processing time of active or passive addition or withdrawal of visual or haptic information

Vision (V) and touch (T) help stabilize our standing body, but little is known on the time-interval necessary for the brain to process the sensory inflow (or its removal) and exploit the new information (or counteract its removal). We have estimated the latency of onset and the time-course of the changes in postural control mode following addition or withdrawal of sensory information and the effect of anticipation thereof. Ten subjects stood in tandem position. They wore LCD goggles that allowed or removed vision, or lightly touched (eyes-closed) with the index finger (haptic stimulation) a pad that could be suddenly lowered (passive task). In different sessions, sensory shifts were deliberately produced by opening (or closing) the eyes or touching the pad (or lifting the finger) (active task). We recorded eyelid movement and finger force (<1N), sway of center of foot pressure (CoP), electromyogram (EMG) of soleus, tibialis and peroneus muscle, bilaterally, and of extensor indicis. The latency of the CoP and EMG changes following the shifts were statistically estimated on the averaged traces of 50 repetitions per condition. Muscle activity and sway adaptively decreased in amplitude on adding stabilizing visual or haptic information. The time-interval from the sensory shift to decrease in EMG and sway was ∼0.5-2 s under both conditions. It was shorter for tibialis than peroneus or soleus and shorter for visual than haptic shift. CoP followed the tibialis by ∼0.2 s. Slightly shorter intervals were observed following active sensory shifts. Latencies of EMG and postural changes were the shortest on removal of both haptic and visual information. Subsequently, the time taken to reach the steady-state was ∼1-3 s under both active and passive tasks. A startle response at ∼100 ms could precede EMG changes. Reaction-time contractions in response to sensory shifts appeared at ∼200 ms, earlier than the adaptive changes. Changes in postural behavior require a finite amount of time from visual or haptic shift, much longer than reflexes or rapid voluntary responses, suggesting a time-consuming central integration process. This process is longer on addition than removal of haptic information, indicating a heavier computational load. These findings should be taken into account when considering problems of sensorimotor integration in elderly subjects or patients and when designing simulation models of human balance.

Leg muscle activity during tandem stance and the control of body balance in the frontal plane

OBJECTIVES We investigated the pattern of activity of the tibialis anterior (TA), soleus (SOL) and peroneus longus (PER) muscles of both legs during tandem stance, in order to highlight their respective role in maintaining balance. METHODS Twelve young healthy subjects were asked to stand with feet in line for successive 15s-epochs, on a dynamometric platform with (EO) and without (EC) vision. EMG was recorded from the six muscles simultaneously. Collected signals were displacement of the centre of feet pressure (CoP) and EMG. Variables calculated for each recorded epoch were mean level, variability and distribution between legs of EMG, and cross-correlation between EMG and CoP traces and between EMG of homonymous muscles. RESULTS CoP motion was larger along the medio-lateral (M-L) than antero-posterior (A-P) axis, and larger with EC than EO particularly in the M-L axis. Muscle activity was larger in the rear than in the front leg, as expected, except for PER. Activity increased with the increase in M-L CoP oscillations, except for SOL, which was tonically active, both legs, regardless of the amplitude of the oscillations. Manipulating vision had no effect on the variability of the EMG for equal mean levels of activity, for any muscle. Cross-correlation between EMG of rear leg muscles and M-L CoP sway gave higher coefficients for TA and PER than SOL, and appropriate time-delays between TA or PER and CoP motion, indicating a role of these muscles in the control of M-L sway. Except for the tonically active SOL, the homonymous muscles of the two legs were active out-of-phase, indicating a mutual push-pull action of the pairs. This was confirmed by the reciprocal activation of TA and PER of the same leg. CONCLUSIONS Overall, in spite of a large inter-trial and inter-subject variability, the neural command to the leg muscles during tandem stance implies a task-sharing rule, whereby SOL keeps the body upright while the reciprocal PER and TA activities produce the alternate impulses necessary for body stabilization in the frontal plane. SIGNIFICANCE Knowledge of the normal mode of control of balance in frontal plane can foster new investigation in both posture and gait control, in addition to offering tools for understanding balance problems of elderly persons and patients at risk of fall.

Adaptation to continuous perturbation of balance: progressive reduction of postural muscle activity with invariant or increasing oscillations of the center of mass depending on perturbation frequency and vision conditions.

We investigated the adaptation of balancing behavior during a continuous, predictable perturbation of stance consisting of 3-min backward and forward horizontal sinusoidal oscillations of the support base. Two visual conditions (eyes-open, EO; eyes-closed, EC) and two oscillation frequencies (LF, 0.2 Hz; HF, 0.6 Hz) were used. Center of Mass (CoM) and Center of Pressure (CoP) oscillations and EMG of Soleus (Sol) and Tibialis Anterior (TA) were recorded. The time course of each variable was estimated through an exponential model. An adaptation index allowed comparison of the degree of adaptation of different variables. Muscle activity pattern was initially prominent under the more challenging conditions (HF, EC and EO; LF, EC) and diminished progressively to reach a steady state. At HF, the behavior of CoM and CoP was almost invariant. The time-constant of EMG adaptation was shorter for TA than for Sol. With EC, the adaptation index showed a larger decay in the TA than Sol activity at the end of the balancing trial, pointing to a different role of the two muscles in the adaptation process. At LF, CoM and CoP oscillations increased during the balancing trial to match the platform translations. This occurred regardless of the different EMG patterns under EO and EC. Contrary to CoM and CoP, the adaptation of the muscle activities had a similar time-course at both HF and LF, in spite of the two frequencies implying a different number of oscillation cycles. During adaptation, under critical balancing conditions (HF), postural muscle activity is tuned to that sufficient for keeping CoM within narrow limits. On the contrary, at LF, when vision permits, a similar decreasing pattern of muscle activity parallels a progressive increase in CoM oscillation amplitude, and the adaptive balancing behavior shifts from the initially reactive behavior to one of passive riding the platform. Adaptive balance control would rely on on-line computation of risk of falling and sensory inflow, while minimizing balance challenge and muscle effort. The results from this study contribute to the understanding of plasticity of the balance control mechanisms under posture-challenging conditions.

Sensori-motor integration during stance: time adaptation of control mechanisms on adding or removing vision.

Sudden addition or removal of visual information can be particularly critical to balance control. The promptness of adaptation of stance control mechanisms is quantified by the latency at which body oscillation and postural muscle activity vary after a shift in visual condition. In the present study, volunteers stood on a force platform with feet parallel or in tandem. Shifts in visual condition were produced by electronic spectacles. Ground reaction force (center of foot pressure, CoP) and EMG of leg postural muscles were acquired, and latency of CoP and EMG changes estimated by t-tests on the averaged traces. Time-to-reach steady-state was estimated by means of an exponential model. On allowing or occluding vision, decrements and increments in CoP position and oscillation occurred within about 2s. These were preceded by changes in muscle activity, regardless of visual-shift direction, foot position or front or rear leg in tandem. These time intervals were longer than simple reaction-time responses. The time course of recovery to steady-state was about 3s, shorter for oscillation than position. The capacity of modifying balance control at very short intervals both during quiet standing and under more critical balance conditions speaks in favor of a necessary coupling between vision, postural reference, and postural muscle activity, and of the swiftness of this sensory reweighing process.

Processing time of addition or withdrawal of single or combined balance-stabilizing haptic and visual information

We investigated the integration time of haptic and visual input and their interaction during stance stabilization. Eleven subjects performed four tandem-stance conditions (60 trials each). Vision, touch, and both vision and touch were added and withdrawn. Furthermore, vision was replaced with touch and vice versa. Body sway, tibialis anterior, and peroneus longus activity were measured. Following addition or withdrawal of vision or touch, an integration time period elapsed before the earliest changes in sway were observed. Thereafter, sway varied exponentially to a new steady-state while reweighting occurred. Latencies of sway changes on sensory addition ranged from 0.6 to 1.5 s across subjects, consistently longer for touch than vision, and were regularly preceded by changes in muscle activity. Addition of vision and touch simultaneously shortened the latencies with respect to vision or touch separately, suggesting cooperation between sensory modalities. Latencies following withdrawal of vision or touch or both simultaneously were shorter than following addition. When vision was replaced with touch or vice versa, adding one modality did not interfere with the effect of withdrawal of the other, suggesting that integration of withdrawal and addition were performed in parallel. The time course of the reweighting process to reach the new steady-state was also shorter on withdrawal than addition. The effects of different sensory inputs on posture stabilization illustrate the operation of a time-consuming, possibly supraspinal process that integrates and fuses modalities for accurate balance control. This study also shows the facilitatory interaction of visual and haptic inputs in integration and reweighting of stance-stabilizing inputs.

Rapid processing of haptic cues for postural control in blind subjects

OBJECTIVES Vision and touch rapidly lead to postural stabilization in sighted subjects. Is touch-induced stabilization more rapid in blind than in sighted subjects, owing to cross-modal reorganization of function in the blind? METHODS We estimated the time-period elapsing from onset of availability of haptic support to onset of lateral stabilization in a group of early- and late-onset blinds. Eleven blind (age 39.4 years±11.7SD) and eleven sighted subjects (age 30.0 years±10.0SD), standing eyes closed with feet in tandem position, touched a pad with their index finger and withdrew the finger from the pad in sequence. EMG of postural muscles and displacement of centre of foot pressure were recorded. The task was repeated fifty times, to allow statistical evaluation of the latency of EMG and sway changes following the haptic shift. RESULTS Steady-state sway (with or without contact with pad, no haptic shift) did not differ between blind and sighted. On adding the haptic stimulus, EMG and sway diminished in both groups, but at an earlier latency (by about 0.5 s) in the blinds (p <0.01). Latencies were still shorter in the early-than late-blinds. When the haptic stimulus was withdrawn, both groups increased EMG and sway at equally short delays. CONCLUSIONS Blinds are rapid in implementing adaptive postural modifications when granted an external haptic reference. Fast processing of the stabilizing haptic spatial-orientation cues may be favoured by cortical plasticity in blinds. SIGNIFICANCE These findings add new information to the field of sensory-guided dynamic control of equilibrium in man.

Calibration of the Leg Muscle Responses Elicited by Predictable Perturbations of Stance and the Effect of Vision.

Motor adaptation due to task practice implies a gradual shift from deliberate control of behavior to automatic processing, which is less resource- and effort-demanding. This is true both for deliberate aiming movements and for more stereotyped movements such as locomotion and equilibrium maintenance. Balance control under persisting critical conditions would require large conscious and motor effort in the absence of gradual modification of the behavior. We defined time-course of kinematic and muscle features of the process of adaptation to repeated, predictable perturbations of balance eliciting both reflex and anticipatory responses. Fifty-nine sinusoidal (10 cm, 0.6 Hz) platform displacement cycles were administered to 10 subjects eyes-closed (EC) and eyes-open (EO). Head and Center of Mass (CoM) position, ankle angle and Tibialis Anterior (TA) and Soleus (Sol) EMG were assessed. EMG bursts were classified as reflex or anticipatory based on the relationship between burst amplitude and ankle angular velocity. Muscle activity decreased over time, to a much larger extent for TA than Sol. The attenuation was larger for the reflex than the anticipatory responses. Regardless of muscle activity attenuation, latency of muscle bursts and peak-to-peak CoM displacement did not change across perturbation cycles. Vision more than doubled speed and the amount of EMG adaptation particularly for TA activity, rapidly enhanced body segment coordination, and crucially reduced head displacement. The findings give new insight on the mode of amplitude- and time-modulation of motor output during adaptation in a balancing task, advocate a protocol for assessing flexibility of balance strategies, and provide a reference for addressing balance problems in patients with movement disorders.

Stepping in Place While Voluntarily Turning Around Produces a Long-Lasting Posteffect Consisting in Inadvertent Turning While Stepping Eyes Closed

Training subjects to step in place on a rotating platform while maintaining a fixed body orientation in space produces a posteffect consisting in inadvertent turning around while stepping in place eyes closed (podokinetic after-rotation, PKAR). We tested the hypothesis that voluntary turning around while stepping in place also produces a posteffect similar to PKAR. Sixteen subjects performed 12 min of voluntary turning while stepping around their vertical axis eyes closed and 12 min of stepping in place eyes open on the center of a platform rotating at 60°/s (pretests). Then, subjects continued stepping in place eyes closed for at least 10 min (posteffect). We recorded the positions of markers fixed to head, shoulder, and feet. The posteffect of voluntary turning shared all features of PKAR. Time decay of angular velocity, stepping cadence, head acceleration, and ratio of angular velocity after to angular velocity before were similar between both protocols. Both postrotations took place inadvertently. The posteffects are possibly dependent on the repeated voluntary contraction of leg and foot intrarotating pelvic muscles that rotate the trunk over the stance foot, a synergy common to both protocols. We propose that stepping in place and voluntary turning can be a scheme ancillary to the rotating platform for training body segment coordination in patients with impairment of turning synergies of various origin.

Haptic Cues for Balance: Use of a Cane Provides Immediate Body Stabilization

Haptic cues are important for balance. Knowledge of the temporal features of their effect may be crucial for the design of neural prostheses. Touching a stable surface with a fingertip reduces body sway in standing subjects eyes closed (EC), and removal of haptic cue reinstates a large sway pattern. Changes in sway occur rapidly on changing haptic conditions. Here, we describe the effects and time-course of stabilization produced by a haptic cue derived from a walking cane. We intended to confirm that cane use reduces body sway, to evaluate the effect of vision on stabilization by a cane, and to estimate the delay of the changes in body sway after addition and withdrawal of haptic input. Seventeen healthy young subjects stood in tandem position on a force platform, with eyes closed or open (EO). They gently lowered the cane onto and lifted it from a second force platform. Sixty trials per direction of haptic shift (Touch → NoTouch, T-NT; NoTouch → Touch, NT-T) and visual condition (EC-EO) were acquired. Traces of Center of foot Pressure (CoP) and the force exerted by cane were filtered, rectified, and averaged. The position in space of a reflective marker positioned on the cane tip was also acquired by an optoelectronic device. Cross-correlation (CC) analysis was performed between traces of cane tip and CoP displacement. Latencies of changes in CoP oscillation in the frontal plane EC following the T-NT and NT-T haptic shift were statistically estimated. The CoP oscillations were larger in EC than EO under both T and NT (p < 0.001) and larger during NT than T conditions (p < 0.001). Haptic-induced effect under EC (Romberg quotient NT/T ~ 1.2) was less effective than that of vision under NT condition (EC/EO ~ 1.5) (p < 0.001). With EO cane had little effect. Cane displacement lagged CoP displacement under both EC and EO. Latencies to changes in CoP oscillations were longer after addition (NT-T, about 1.6 s) than withdrawal (T-NT, about 0.9 s) of haptic input (p < 0.001). These latencies were similar to those occurring on fingertip touch, as previously shown. Overall, data speak in favor of substantial equivalence of the haptic information derived from both “direct” fingertip contact and “indirect” contact with the floor mediated by the cane. Cane, finger and visual inputs would be similarly integrated in the same neural centers for balance control. Haptic input from a walking aid and its processing time should be considered when designing prostheses for locomotion.

Temporal features of postural adaptation strategy to prolonged and repeatable balance perturbation

Aim of this study was to get insight into the features of the postural adaptation process, occurring during a continuous 3-min and 0.6Hz horizontal sinusoidal oscillation of the body support base. We hypothesized an ongoing temporal organization of the balancing strategy that gradually becomes fine-tuned and more coordinated with the platform movement. The trial was divided into oscillation cycles and for each cycle: leg muscles activity and temporal relationship between Centre of Mass and Centre of Pressure A-P position were analyzed. The results of each cycle were grouped in time-windows of 10 successive cycles (time windows of 16.6s). Muscle activity was initially prominent and diminished progressively. The major burst of Tibialis Anterior (TA) muscle always occurred at the same time instant of the platform oscillation cycle, in advance with respect to the platform posterior turning point. This burst produced a body forward rotation that was delayed throughout the task. During prolonged and repeatable balance perturbation, an ongoing postural adaptation process occurs. When the effects of the perturbation become predictable, the CNS scales the level of muscle activity to counteracting the destabilizing effects of the perturbations. Furthermore, the CNS tunes the kinematics and the kinetic responses optimally by slightly delaying the onset of the body forward rotation, maintaining unchanged the time-pattern of postural muscle activation.