John J. Jeka

Dynamic reweighting of three modalities for sensor fusion.

We simultaneously perturbed visual, vestibular and proprioceptive modalities to understand how sensory feedback is re-weighted so that overall feedback remains suited to stabilizing upright stance. Ten healthy young subjects received an 80 Hz vibratory stimulus to their bilateral Achilles tendons (stimulus turns on-off at 0.28 Hz), a ±1 mA binaural monopolar galvanic vestibular stimulus at 0.36 Hz, and a visual stimulus at 0.2 Hz during standing. The visual stimulus was presented at different amplitudes (0.2, 0.8 deg rotation about ankle axis) to measure: the change in gain (weighting) to vision, an intramodal effect; and a change in gain to vibration and galvanic vestibular stimulation, both intermodal effects. The results showed a clear intramodal visual effect, indicating a de-emphasis on vision when the amplitude of visual stimulus increased. At the same time, an intermodal visual-proprioceptive reweighting effect was observed with the addition of vibration, which is thought to change proprioceptive inputs at the ankles, forcing the nervous system to rely more on vision and vestibular modalities. Similar intermodal effects for visual-vestibular reweighting were observed, suggesting that vestibular information is not a “fixed” reference, but is dynamically adjusted in the sensor fusion process. This is the first time, to our knowledge, that the interplay between the three primary modalities for postural control has been clearly delineated, illustrating a central process that fuses these modalities for accurate estimates of self-motion.

Explicit and implicit knowledge of environment states induce adaptation in postural control

The aim of this study was to investigate the effects of explicit and implicit knowledge about visual surrounding manipulation on postural responses. Twenty participants divided into two groups, implicit and explicit, remained in upright stance inside a moving room. In the fourth trial participants in the explicit group were informed about the movement of the room while participants in the implicit group performed the trial with the room moving at a larger amplitude and higher velocity. Results showed that postural responses to visual manipulation decreased after participants were told that the room was moving as well as after increasing amplitude and velocity of the room, indicating decreased coupling (down-weighting) of the visual influences. Moreover, this decrease was even greater for the implicit group compared to the explicit group. The results demonstrated that conscious knowledge about environmental state changes the coupling to visual information, suggesting a cognitive component related to sensory re-weighting. Re-weighting processes were also triggered without awareness of subjects and were even more pronounced compared to the first case. Adaptive re-weighting was shown when knowledge about environmental state was gathered explicitly and implicitly, but through different adaptive processes.

Perspectives on Aging Vestibular Function

Much is known about age-related anatomical changes in the vestibular system. Knowledge regarding how vestibular anatomical changes impact behavior for older adults continues to grow, in line with advancements in diagnostic testing. However, despite advancements in clinical diagnostics, much remains unknown about the functional impact that an aging vestibular system has on daily life activities such as standing and walking. Modern diagnostic tests are very good at characterizing neural activity of the isolated vestibular system, but the tests themselves are artificial and do not reflect the multisensory aspects of natural human behavior. Also, the majority of clinical diagnostic tests are passively applied because active behavior can enhance performance. In this perspective paper, we review anatomical and behavioral changes associated with an aging vestibular system and highlight several areas where a more functionally relevant perspective can be taken. For postural control, a multisensory perturbation approach could be used to bring balance rehabilitation into the arena of precision medicine. For walking and complex gaze stability, this may result in less physiologically specific impairments, but the trade-off would be a greater understanding of how the aging vestibular system truly impacts the daily life of older adults.

Visual control of trunk translation and orientation during locomotion

Previous studies have suggested distinct control of gait characteristics in the anterior–posterior (AP) and medial–lateral (ML) directions in response to visual input. Responses were larger to a ML visual stimulus, suggesting that vision plays a larger role in stabilizing gait in the ML direction. Here, we investigated responses of the trunk during locomotion to determine whether a similar direction dependence is observed. We hypothesized that translation of the trunk would show a similar ML dependence on vision, but that angular deviations of the trunk would show equivalent responses in all directions. Subjects stood or walked on a treadmill at 5xa0km/h while viewing a virtual wall of white triangles that moved in either the AP or ML direction according to a broadband input stimulus. Frequency response functions between the visual scene motion and trunk kinematics revealed that trunk translation gain was larger across all frequencies during walking compared with standing. Trunk orientation responses were not different from standing at very low frequencies; however, at high frequencies, trunk orientation gain was much higher during walking. Larger gains in response to ML visual scene motion were found for all trunk movements. Higher gains in the ML direction while walking suggest that visual feedback may contribute more to the stability of trunk movements in the ML direction. Vision modified trunk movement behavior on both a slow (translation) and fast (orientation) time scale suggesting a priority for minimizing angular deviations of the trunk. Overall, trunk responses to visual input were consistent with the theme that control of locomotion requires higher-level sensory input to maintain stability in the ML direction.

Loss of peripheral sensory function explains much of the increase in postural sway in healthy older adults

Postural sway increases with age and peripheral sensory disease. Whether, peripheral sensory function is related to postural sway independent of age in healthy adults is unclear. Here, we investigated the relationship between tests of visual function (VISFIELD), vestibular function (CANAL or OTOLITH), proprioceptive function (PROP), and age, with center of mass sway area (COM) measured with eyes open then closed on firm and then a foam surface. A cross-sectional sample of 366 community dwelling healthy adults from the Baltimore Longitudinal Study of Aging was tested. Multiple linear regressions examined the association between COM and VISFIELD, PROP, CANAL, and OTOLITH separately and in multi-sensory models controlling for age and gender. PROP dominated sensory prediction of sway across most balance conditions (βs = 0.09–0.19, ps < 0.001), except on foam eyes closed where CANAL function loss was the only significant sensory predictor of sway (β = 2.12, p < 0.016). Age was not a consistent predictor of sway. This suggests loss of peripheral sensory function explains much of the age-associated increase in sway.

Identification of the Unstable Human Postural Control System

Maintaining upright bipedal posture requires a control system that continually adapts to changing environmental conditions, such as different support surfaces. Behavioral changes associated with different support surfaces, such as the predominance of an ankle or hip strategy, is considered to reflect a change in the control strategy. However, tracing such behavioral changes to a specific component in a closed loop control system is challenging. Here we used the joint input–output (JIO) method of closed-loop system identification to identify the musculoskeletal and neural feedback components of the human postural control loop. The goal was to establish changes in the control loop corresponding to behavioral changes observed on different support surfaces. Subjects were simultaneously perturbed by two independent mechanical and two independent sensory perturbations while standing on a normal or short support surface. The results show a dramatic phase reversal between visual input and body kinematics due to the change in surface condition from trunk leads legs to legs lead trunk with increasing frequency of the visual perturbation. Through decomposition of the control loop, we found that behavioral change is not necessarily due to a change in control strategy, but in the case of different support surfaces, is linked to changes in properties of the plant. The JIO method is an important tool to identify the contribution of specific components within a closed loop control system to overall postural behavior and may be useful to devise better treatment of balance disorders.

A central processing sensory deficit with Parkinson’s disease

Parkinson’s disease (PD) is a progressive degenerative disease manifested by tremor, rigidity, bradykinesia, and postural instability. Deficits in proprioceptive integration are prevalent in individuals with PD, even at early stages of the disease. These deficits have been demonstrated primarily during investigations of reaching. Here, we investigated how PD affects sensory fusion of multiple modalities during upright standing. We simultaneously perturbed upright stance with visual, vestibular, and proprioceptive stimulation, to understand how these modalities are reweighted so that overall feedback remains suited to stabilizing upright stance in individuals with PD. Eight individuals with PD stood in a visual cave with a moving visual scene at 0.2xa0Hz while an 80-Hz vibratory stimulus was applied bilaterally to their Achilles tendons (stimulus turns on–off at 0.28xa0Hz) and a ±1xa0mA bilateral monopolar galvanic stimulus was applied at 0.36xa0Hz. The visual stimulus was presented at different amplitudes (0.2°, 0.8° rotation about ankle axis) to measure: the change in gain (weighting) to vision, an intramodal effect; and a simultaneous change in gain to vibration and galvanic stimulation, both intermodal effects. Trunk/leg gain relative to vision decreased when visual amplitude was increased, reflecting an intramodal visual effect. In contrast, when vibration was turned on/off, leg gain relative to vision was equivalent in individuals with PD, indicating no reweighting of visual information when proprioception was disrupted through vibration (i.e., no intermodal effect). Trunk and leg angle gain relative to GVS also showed no reweighting in individuals with PD. These results are in contrast to previous results with healthy adults, who showed clear intermodal effects in the same paradigm, suggesting that individuals with PD not only have a proprioceptive deficit during standing, but also have a cross-modal sensory fusion deficit that is crucial for upright stance control.

Visual feedback during treadmill walking improves balance for older adults: A preliminary report

The majority of falls occur during walking. This begs the question, “Why are most balance training exercises performed when standing still?” Visual feedback for balance training is becoming more prevalent in rehabilitation, but is often performed while standing still. Five subjects have completed an eight week intervention study, part of an ongoing randomized controlled clinical trial. All subjects are tested for balance and walking ability at the beginning, middle and end of the eight week period using clinical tests to assess balance ability. Preliminary results suggest that balance improves only for the experimental group.

Development of adaptive sensorimotor control in infant sitting posture

A reliable and adaptive relationship between action and perception is necessary for postural control. Our understanding of how this adaptive sensorimotor control develops during infancy is very limited. This study examines the dynamic visual-postural relationship during early development. Twenty healthy infants were divided into 4 developmental groups (each n=5): sitting onset, standing alone, walking onset, and 1-year post-walking. During the experiment, the infant sat independently in a virtual moving-room in which anterior-posterior oscillations of visual motion were presented using a sum-of-sines technique with five input frequencies (from 0.12 to 1.24 Hz). Infants were tested in five conditions that varied in the amplitude of visual motion (from 0 to 8.64 cm). Gain and phase responses of infants postural sway were analyzed. Our results showed that infants, from a few months post-sitting to 1 year post-walking, were able to control their sitting posture in response to various frequency and amplitude properties of the visual motion. Infants showed an adult-like inverted-U pattern for the frequency response to visual inputs with the highest gain at 0.52 and 0.76 Hz. As the visual motion amplitude increased, the gain response decreased. For the phase response, an adult-like frequency-dependent pattern was observed in all amplitude conditions for the experienced walkers. Newly sitting infants, however, showed variable postural behavior and did not systemically respond to the visual stimulus. Our results suggest that visual-postural entrainment and sensory re-weighting are fundamental processes that are present after a few months post sitting. Sensorimotor refinement during early postural development may result from the interactions of improved self-motion control and enhanced perceptual abilities.

Complementary mechanisms for upright balance during walking

Lateral balance is a critical factor in keeping the human body upright during walking. Two important mechanisms for balance control are the stepping strategy, in which the foot placement is changed in the direction of a sensed fall to modulate how the gravitational force acts on the body, and the lateral ankle strategy, in which the body mass is actively accelerated by an ankle torque. Currently, there is minimal evidence about how these two strategies complement one another to achieve upright balance during locomotion. We use Galvanic vestibular stimulation (GVS) to induce the sensation of a fall at heel-off during gait initiation. We found that young healthy adults respond to the illusory fall using both the lateral ankle strategy and the stepping strategy. The stance foot center of pressure (CoP) is shifted in the direction of the perceived fall by ≈2.5 mm, starting ≈247 ms after stimulus onset. The foot placement of the following step is shifted by ≈15 mm in the same direction. The temporal delay between these two mechanisms suggests that they independently contribute to upright balance during locomotion, potentially in a serially coordinated manner. Modeling results indicate that without the lateral ankle strategy, a much larger step width is required to maintain upright balance, suggesting that the small but early CoP shift induced by the lateral ankle strategy is critical for upright stability during locomotion. The relative importance of each mechanism and how neurological disorders may affect their implementation remain an open question.