Sensory Reweighting: A Rehabilitative Mechanism?

Chapter 35 Sensory Reweighting: A Rehabilitative Mechanism? Eric Anson and John Jeka History and Background Falls in the elderly are dangerous, debilitating, and costly. Of the population over 65 years of age, one-third to one-half experiences falls annually; of these, half do so repeatedly. Falls are the leading cause of injury in older adults and the primary cause of accidental death in those over age 85. Five percent of falls lead to a fracture, with hip fractures being the most common (greater than 200,000 annually). One in 10 of these individuals will die of complications, and 25% of survivors will never regain their previous mobility. An additional 10% of all older adults who fall will sustain other serious injuries requiring medical care. The cost of direct care for hip fracture patients alone is now estimated to be in excess of 10 billion dollars a year. Imbalance is a major cause of falls. Further, imbalance in older adults is strongly associated with functional decline and frailty. Certain activities of daily living can no longer be performed or are avoided due to a fear of falling. Unstable elderly persons become increasingly sedentary, homebound, and isolated. Fall-prone elderly persons may display greater than typical reduction in strength and power needed during corrective movements, to recover from E. Anson
J. Jeka (&) Department of Kinesiology, Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD 20742-2611, USA e-mail: [email protected] perturbations or tripping, compared to healthy elderly and are at increased risk offalling (for review, see [1]). Falls and instability contribute to 40% of nursing home admissions. While mild declines in balance are associated with advancing age, falls are not a normal part of aging. Prior research has led to the understanding that elderly fallers are different than their healthy, age-matched counterparts. According to geriatrician Mary Tinetti falls “should be treated as an entity in their own right” [2]. The issue of just how older adults who fall should be treated is currently of great interest to clinicians and researchers alike. Because the mechanisms of postural control and their decline in older adults who fall are not fully understood, the design of therapeutic interventions is severely hampered. Presently, there exists a large gap between research into postural control mechanisms and interventions for preventing falls in the elderly. This may be partially due to the multi-faceted nature of postural control. Earlier in the century posture research focused primarily on defining the parallel and hierarchical reflexive pathways that were thought to control upright stance (e.g., [3, 4]). This reflexive perspective has been supplanted in the last 20 years with the view that posture is a complex interaction among multiple neural subsystems which support sensory orientation [5], multi-joint coordination [6], task constraints [7], and cognitive inputs such as attention (e.g., [8]). Because the mechanisms of postural control and their decline in older adults who fall are not fully understood, it remains a challenge to translate this modern view into effective rehabilitative programs for those © Springer Nature Switzerland AG 2019 C. L. Armstrong and L. A. Morrow (eds.), Handbook of Medical Neuropsychology, https://doi.org/10.1007/978-3-030-14895-9_35 789 790 with balance problems. A review of balance training studies [9] points out that “. . .there have been few attempts to improve balance in older adults with theory-based intervention strategies” (p. 355). Here we focus on one of the major underlying mechanisms of postural control, namely sensory integration, but within an intervention context to foster a better theoretical understanding of how one critical component of such a multifaceted program – sensory integration – may improve balance control. Sensory training may add to our theoretical understanding of postural control and its relationship to sensory information as well as inform the design of clinical interventions. Sensory Reweighting in Older Adults Control of human upright stance requires sensory input from multiple sources to detect center of gravity excursions and to generate appropriate muscle responses for upright stance control. Without appropriate knowledge of self-orientation, equilibrium control is severely compromised [10]. Patients or elderly individuals with sensory deficits who perceive their stability limits incorrectly may show inappropriate postural responses or strategies to maintain equilibrium. For example, some individuals may not take a step necessary to recover equilibrium when their center of mass is displaced outside their limits of stability because they misperceive their stability boundaries. In contrast, others may make exaggerated compensatory responses to very small perturbations because they misperceive themselves to be at their limits of stability and therefore at risk for a fall. Successful responses to balance loss are first predicated on the ability to detect one’s own body position and sense instability and second the ability to generate the appropriate corrective response. Estimation of body position is heavily dependent upon the integration of information from multiple sensory systems including visual, vestibular (inner ear), and somatosensory (touch, pressure). The ability to select and reweight alternative orientation references adaptively is considered one of the most critical factors for postural control in the elderly [11]. Elderly E. Anson and J. Jeka individuals who are unable to quickly select the appropriate sensory cue may be prone to balance loss whenever the sensory environment changes. These individuals may also be less able to use alternative combinations of sensory information to compensate for sensory losses or impairments. The reweighting of sensory information may determine whether an older adult can compensate for mild sensory degradation and retain good postural control despite advanced age. Multisensory reweighting (MSR) is generally held to be impaired in older adults and more so in the fall-prone versus healthy elderly. Teasdale et al. [12] screened both young and (presumably healthy) older subjects to insure intact peripheral somatosensation, then measured their postural sway during the sudden withdrawal and re-insertion [addition] of visual information. As expected, both age groups had increased postural sway with the sudden removal of visual information. For young subjects, postural sway decreased when vision was suddenly added after a period with eyes closed. However, for older subjects sudden addition of visual information led to increased postural sway. Considering that peripheral somatosensation was intact in both groups, these results may point to deficient central MSR mechanisms in the older group. According to Teasdale et al. [12], compared to younger adults, older adults have “poorer central integrative mechanisms responsible for reconfiguring the postural set” (p. 695). Healthy older adults are as stable as healthy young adults in conditions where only a single sense is altered, but are less stable in conditions where two senses are manipulated simultaneously [13–16]. Although even healthy older adults may lose their balance when first exposed to conditions where both visual and somatosensory inputs are altered, they show improved stability on repeated trials of the same conditions [7, 17, 18]. These findings indicate that healthy older adults can, with little practice, rapidly adapt to changing environments. Compared to healthy older adults, fall-prone older adults demonstrate instability in conditions where only one sensory input is changing [8, 19, 20]. Fall-prone older adults do not show rapid adaptation to changes in the environment, continuing to lose their balance despite repeated exposure [11, 21]. Fall-prone elders are hypothesized to be more visually 35 Sensory Reweighting: A Rehabilitative Mechanism? dependent, failing to use reliable somatosensory cues in environments where visual inputs are unstable [22, 23]. Thus, there may be age-related decline in MSR abilities, with further MSR deficits reported in fall-prone older adults. This implies that impaired MSR is associated with increased fall risk. Sensory deficits associated with aging and poor balance control have two potential sources: (1) loss or degradation of one or more peripheral sensory systems; and (2) degradation of central nervous system processing which integrates information from peripheral sensory systems. Age-related changes in peripheral functioning may adversely affect balance control, particularly with vision, but the healthy central nervous system may also adapt to such changes, especially if these declines are gradual. Moreover, there is no direct evidence that age-related reduction in somatosensory and vestibular sensitivity is related to the balance changes in the elderly [24]. Central processing deficits may be the more likely candidate for age-related balance decrement. Studies show that elderly persons are at a disadvantage when required to control upright stance with the slower, higher level sensory integrative mechanisms [25] . Balance Training A number of controlled studies have been undertaken to investigate various intervention strategies to reduce the number and risk of falls (for a review, see [9, 26]). Several of these studies have demonstrated that activity-based interventions can significantly improve balance and reduce the risk for falls in older adults. But most of these intervention approaches lack a theoretical framework, and as yet there is no clearly superior, standardized approach to exercise interventions for fall-risk reduction in the elderly. Moreover, the mechanisms by which activities such as exercise affect postural control processes are not well understood. Until a better understanding of postural control processes and their decline in older adults who fall is achieved, a scientific foundation for activity-based interventions will remain elusive. Likewise, knowledge of the mechanisms through which interventions effect postural control processes is needed before optimal intervention strategies can be developed. 791 Experimental studies have suggested that poor sensory integration in older adults is a potential source of falls (for review, see [11]). Many older adults may fall not because they are too weak or stiff to respond, but because they do not correctly perceive their spatial position, or changes in their spatial position, preceding a fall. This inaccurate perception may result in inappropriate compensatory responses to correct for loss of stability. Based upon such findings, enhancement of multisensory interactions has been suggested as a potentially fruitful area for new interventions [9]. However, to date, we know of only one study that focused specifically on sensory input manipulation as an intervention approach (i.e., [27]). Despite the positive effect on balance from sensory training in this study, little has been done to expand the multisensory training approach. The neurophysiological mechanism through which sensory training may effect the postural control system is unknown, but a likely candidate is neuroplasticity. Recent studies indicate that in response to practice or training, the brain reorganizes far more quickly [28] and at a much later age than previously thought possible [29]. Studies with primates indicate that repetitive, goal-directed activity leads to changes in cortical sensory mapping, which in turn affects motor responses [30]. Preliminary work with individuals who have developed hand dystonia related to manual overuse, and in individuals post-stroke, indicates that interventions geared toward sensory re-organization result in improved motor capabilities [31]. Neuroplastic change may be one mechanism by which sensory training improves balance. It is possible that interventions geared toward improving the use of sensory inputs for perception of position in and movement through space may result in improved balance and reduced risk of falls in the elderly. Current views of postural control recognize the critical role of multisensory integration for accurate perception of body orientation and subsequently appropriate motor behavior. Clinical practice has begun to reflect this view by expanding balance evaluation methods to include tests of peripheral sensory reception and central sensory organization and by developing multi-dimensional intervention programs that include manipulation of environmental constraints to challenge sensory integration processes [32–34]; (for review, see [1]). These comprehensive 792 interventions are more successful at reducing the risk of falls in the unstable elderly than previous uni-dimensional approaches [9]. However, studies using multidimensional interventions and global balance measures do not permit investigation of the specific mechanisms that may change due to intervention. Until a greater understanding of these particular processes is gained, the individual components of a comprehensive program cannot be optimally developed and maximal benefit from such programs will not be achieved. Below we summarize studies which explore perceptual postural control mechanisms in elderly individuals with and without a history or high risk of falls and the changes – if any – in balance control that may result specifically from interventions designed to promote central sensory integration processes in unstable older adults. With this information, improved intervention approaches may be designed and the risk of falls subsequently reduced. Multisensory Integration: The Light-Touch/Vision Paradigm One of the primary methods to investigate “sensorimotor integration” in postural control is motivated from linear systems analysis. Subjects are typically “driven” by an oscillating pattern of sensory information. The resulting postural or orientation responses of the body are measured to determine “system” control properties. For example, the sinusoidal vertical axis rotation (SVAR) technique rotates seated subjects at a range of frequencies to measure the gain and phase of eye movements in the dark, as an assessment of vestibular function [35, 36]. Likewise, an oscillating visual “moving room” has been used to demonstrate the coupling of visual information with whole-body posture [37–43]. These techniques have determined that rate information is derived from sensory stimuli, that is, the vestibular system provides information about angular acceleration of the head and linear acceleration of the body [44], while the visual system is sensitive to the velocity of a stimulus [39, 45]. We have developed similar techniques to study the properties of somatosensory coupling to posture. E. Anson and J. Jeka A series of studies have demonstrated that somatosensory cues derived from light-touch fingertip contact to a stationary surface provide orientation information for improved control of upright stance [46–49]. Subjects stand in a tandem stance while maintaining fingertip contact with a stationary plate that measures the applied forces. Ultrasound receivers or infrared cameras measure head and approximate center of mass movement. An auditory alarm sounds if above threshold fingertip forces are applied, signaling the subject to reduce applied force without losing contact with the plate. This level of fingertip force is not mechanically supportive, but provides sensory information that the nervous system can use to correct deviations of the body from an upright posture. In general, the task is easy for healthy young subjects. After one practice trial, subjects rarely set off the alarm. The results have consistently shown that light-touch contact (<1 Newton (N)) with the fingertip to a rigid surface attenuates postural sway just as well as mechanical contact of 10–20 N. Furthermore, the influence of fingertip contact with a moving surface on whole-body posture is as dramatic as with full-field visual displays [50, 51]. When the contact surface moves sinusoidally, postural sway adopts the frequency of contact surface motion. Predictions of a second order model support the hypothesis that body sway is coupled to the contact surface through the velocity of the somatosensory stimulus at the fingertip. Other studies have replicated and extended these light-touch findings to other task situations [52–55]. We have developed a multisensory experimental paradigm using light-touch contact in combination with vision as sources of sensory information for postural control [56]. Figure 35.1 shows the experimental setup. An advantage of using light-touch contact as a sensory source is that, like vision, it is easily manipulated (i.e., it is easy to add, remove, or vary its movement frequency and amplitude), making it possible to precisely vary vision and touch relative to one another and to investigate multisensory integration with regard to postural control. Subjects stood within the visual cave with light contact of a small force plate with the right index fingertip. The visual scene and the touch plate moved simultaneously at 0.2 and 0.28 Hz, respectively, in five conditions that manipulated the relative amplitudes of visual and touch motion. Touch and vision 35 Sensory Reweighting: A Rehabilitative Mechanism? 793 Fig. 35.1 Two-frequency vision and touch experimental paradigm were presented at different frequencies so that the body’s response to each could be measured separately. We then calculated “gain” to each sensory input. Gain is calculated as the ratio of the center of mass amplitude over the sensory stimulus amplitude at the frequency of the stimulus. If the gain to vision is one, this means that the body’s response is the same amplitude as the visual stimulus. In other words, the center of mass of the body is moving side-to-side at the same amplitude as the visual stimulus. If the gain is less than one, then the body’s response is smaller than the sensory stimulus amplitude. Gain is interpreted as a measure of the coupling or “weighting” of the sensory stimulus. Higher (lower) gain is interpreted as higher (lower) weighting, reflecting how much the nervous system is using the information from that particular input in estimating the position and velocity of the body. Figure 35.2 plots center of mass (COM) gain in two subjects, who showed both an intra- and inter-modality dependence on vision and touch amplitude. The x-axis denotes the relative amplitude of the two stimuli (vision:touch in mm) in each condition. Comparing, for example, condition 2:8–2:4, note how decreasing the amplitude of touch stimulus motion increased the gain to touch (an intra-modality dependence), while at the same time, gain to vision decreased (an inter-modality dependence), even though visual amplitude was held constant at 2 mm across conditions. We refer to this effect as inverse gain reweighting, meaning, that as stimulus amplitude goes up, the response to that stimulus goes down. This reflects that as a sensory stimulus increases in amplitude, the nervous system must decrease (downweight) its influence to remain upright. Without downweighting, a stimulus of increasing amplitude would 794 Fig. 35.2 Center of mass gain to vision and light touch showing both intra-modality and intermodality reweighting eventually lead to loss of equilibrium. At the same time, the nervous system increases (upweights) the influence of a stimulus that decreases in amplitude because more sensory information enhances its accuracy of self-motion estimation and a smaller stimulus does not threaten equilibrium. The techniques summarized above have allowed intermodality reweighting to be identified rigorously. A crucial aspect of the design was to present stimuli from different modalities at different frequencies so that the response to each stimulus could be quantified separately, thus revealing their inherent interdependence. As we illustrate below, these same techniques can now be applied to populations which have been hypothesized previously to have deficits in sensory reweighting, namely the unstable elderly. Sensory Reweighting in the Fall-Prone Elderly Population Are central sensory reweighting deficits responsible at least in part for the postural control problems seen in healthy and fall-prone older adults? Conclusions from previous research seem to indicate so. Earlier studies, however, have typically used postural sway measures such as mean sway amplitude that may not be as discerning for the processes underlying sensory reweighting (e.g., [7, 19, 57]; see [58]). Using the two-frequency light-touch/vision paradigm described above, we investigated sensory reweighting deficits in E. Anson and J. Jeka fall-prone older adults [59]. Elderly subjects were excluded from the study if they had any medical diagnoses known to produce sensory deficits (diabetes, macular degeneration, vestibulopathy, etc.) or if they are found to have sensory loss on a clinical neurologic screening. Subjects performed both the Sensory Organization Test (SOT) and the two-frequency light-touch/vision tests. The SOT uses a hydraulically controlled support platform and visual surround which may be servo-linked to body sway. Measurement of changes in ankle angle that typically accompany forward and backward movements of the body can be attenuated by rotating the support surface around the axis of the ankle. Similarly, the visual surround can also move forward and backward with anterior– posterior body sway, negating any visual flow that typically accompanies such body movements. This is referred to as “sway-referencing” to the movements of the body. The SOT consists of a series of six different conditions that allow postural performance to be compared under various combinations of visual, vestibular, and somatosensory information. For example, when the support surface is sway-referenced and the eyes are closed (SOT condition #5) or both the support surface and the visual surround are sway-referenced (SOT condition #6), one is left with primarily vestibular information to maintain upright stance. Many patient populations and elderly individuals with balance problems fall immediately in SOT condition #5 and #6, while young healthy individuals are able to maintain upright stance [60], albeit with significantly greater postural sway. Results indicated that our subjects’ performance on the SOT is consistent with prior research, that is, they had great difficulty remaining stable under conditions where vision and somatosensory inputs are altered simultaneously (SOT conditions #5 and #6). Because subjects with vestibular deficits were excluded from the study, poor performance on SOT conditions 5 and 6 implied that they have difficulty with sensory reweighting. In contrast to the SOT results, the same group of subjects displayed clear evidence of multisensory reweighting on the two-frequency light-touch/vision experiment. Vision and touch gains for the fall-prone older adults versus a group of healthy young adults are shown in Fig. 35.3. For the fall-prone older adults, 35 Sensory Reweighting: A Rehabilitative Mechanism? intra-modality reweighting is apparent for both modalities. Note the sharp decline in vision gain as the visual stimulus amplitude increases from 2:2 to 8:2 and the rise in touch gain as the touch stimulus amplitude decreases from 2:8 to 2:2. Inter-modality reweighting is evident for vision, as there is a significant decrease in the vision gain when the vision stimulus amplitude is constant while the touch stimulus amplitude is decreasing. Mean touch gains also 795 rise, in conditions when constant touch stimulus amplitudes are paired with increasing vision stimulus amplitudes. Thus, fall-prone elderly subjects show a very similar pattern of gain change across conditions when compared to healthy young adults. These data do not support the assumption that multisensory reweighting is deficient in fall-prone older adults. Dynamics of Sensory Reweighting. One explanation for the discrepancy in these results is that prior Fig. 35.3 Center of mass gain to vision and light touch in young, healthy older, and fall-prone older adults 796 E. Anson and J. Jeka Fig. 35.4 Long-term changes in center of mass gain in young, healthy older, and fall-prone adults after a change in the visual amplitude from (a) high-to-low and (b) low-to-high studies used relatively short trials (typically 10–30 s) while Allison et al. [59] employed longer trials (2 min). Healthy and fall-prone older adults may be able to reweight visual and somatosensory information, but perhaps not as quickly as young adults. Support for this view comes from a subsequent study which investigated the “dynamics of reweighting” in older adults. In this study, we measured how quickly older adults responded to a change in a visual stimulus [61]. Subjects stood in front of a visual screen in a standardized foot position and were instructed to stand as steadily as possible without stiffening. The subjects began each trial by looking straight ahead at the blank area on the front wall. The visual scene oscillated sinusoidally in the anterior–posterior direction at a constant frequency of 0.4 Hz. The initial amplitude was either 3 or 12 mm. After 60 s the oscillation amplitude switched from 3 to 12 mm or vice versa and remained at this amplitude for 120 s. Figure 35.4 shows the results. All groups showed an initial rapid change in gain that reflected reweighting of vision. When the visual stimulus changed from low-to-high, all subjects showed decreased gain, indicating a reduced coupling to vision when the visual amplitude was large. When the stimulus changed from high-to-low, all subjects showed increased gain, indicating an increased coupling to vision when the visual amplitude was small. No differences were observed between groups, suggesting that the initial rapid reweighting process is not dependent on age or fall-prone status. However group differences were observed for long-term changes in gain. For young adults and healthy older adults, few changes were observed after the initial change in gain implying that the MSR process was completed relatively quickly in young subjects. For fall-prone adults, gains continued to change over the duration of all time segments, demonstrating relatively slow adaptation and implying that the reweighting process in fall-prone adults is not fully achieved during the rapid change in gain. These results may have functional implications for fall risk. Deviations from upright vertical were small and clearly did not approach stability limits. However, fall-prone older adults displayed a prolonged reweighting process that is clearly different than 35 Sensory Reweighting: A Rehabilitative Mechanism? young and healthy older adults, which may contribute to less stable postural control while navigating through the environment. A Multisensory Intervention A subsequent study investigated whether an intervention could change how older adults respond to multisensory information. Participants attended two, 45-min exercise sessions each week for 8 weeks. Prior studies incorporating sensory-challenge exercises and using a similar schedule have demonstrated significant improvements in balance performance [62, 63]. Exercise sessions were “one-on-one” with one of the three “trainers” (two licensed physical therapists and one physical therapist assistant) had been trained in the research exercise protocol. The exercise program was designed to facilitate MSR processes. The purposes of the balance exercise program were to improve (1) estimation of body position and motion in space and (2) adaptation to changing sensory environments. All exercises were performed on a SMART Balance Master®, a computerized balance testing and training device that permits operator controlled surface and/or visual environment motion and, if desired, provides visual feedback about center of gravity position and motion. Participants were asked to stand as steadily as they could without stiffening. No dynamic balance training (volitional weight shifting) or functional balance activities (transfers, gait 797 training, etc.) were practiced; no strengthening or stretching exercises were given. Hence, this was not a multi-dimensional exercise program designed to maximally reduce fall risk, but a uni-dimensional, impairment-oriented exercise program designed to enhance MSR. All subjects followed the same standardized exercise progression; however, the initial difficulty level of the exercises was adjusted for each subject based on their balance abilities. Exercises were made progressively more difficult over the 16 sessions by decreasing standing surface and/or visual environment motion, making it harder to detect surface or visual motion. Visual center of gravity feedback was initially provided, then progressively delayed and withdrawn over the first eight training sessions. Advancement of conditions/tasks and/or reduction of feedback occurred as soon as the participant was successful at that exercise four of five tries or better. The effect of the sensory-challenge balance exercise program is seen in Fig. 35.5a, b which shows that both vision and touch gain values decreased post-training. This post-training reduction in gain values reflects less coupling to the sensory stimulus. The reduced gain values may indicate a change in the ability to discriminate and dissociate self- versus environmental motion, suggesting that sensory estimation processes can be accessed and trained. The fall-prone elderly have been shown to be overly reliant upon visual information. Training to reduce this reliance has potential beneficial effects for balance control. Fig. 35.5 Effect of training on center of mass gain to (a) touch and (b) vision 798 Conclusions Current views of postural control recognize the critical role of multisensory integration for accurate perception of body orientation and subsequently appropriate motor behavior. Clinical practice has begun to reflect this view by expanding balance evaluation methods to include tests of peripheral sensory reception and central sensory organization and by developing multi-dimensional intervention programs that include manipulation of environmental constraints to challenge sensory integration processes [26, 32, 33]. 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