Daniel J. Goble

Proprioceptive sensibility in the elderly: Degeneration, functional consequences and plastic-adaptive processes

As the percentage of individuals over the age of 60 years continues to rise, determining the extent and functional significance of age-related declines in sensorimotor performance is of increasing importance. This review examines the specific contribution of proprioceptive feedback to sensorimotor performance in older adults. First, a global perspective of proprioceptive acuity is provided assimilating information from studies where only one of several aspects of proprioceptive function (e.g. sense of position, motion or dynamic position) was quantified, and/or a single joint or limb segment tested. Second, the consequences of proprioceptive deficits are established with particular emphasis placed on postural control. Lastly, the potential for plastic changes in the aging proprioceptive system is highlighted, including studies which relate physical activity to enhanced proprioceptive abilities in older adults. Overall, this review provides a foundation for future studies regarding the proprioceptive feedback abilities of elderly individuals. Such studies may lead to greater advances in the treatment and prevention of the sensorimotor deficits typically associated with the aging process.

Proprioceptive Acuity Assessment Via Joint Position Matching: From Basic Science to General Practice

Over the past several decades, studies of use-dependent plasticity have demonstrated a critical role for proprioceptive feedback in the reorganization, and subsequent recovery, of neuromotor systems. As such, an increasing emphasis has been placed on tests of proprioceptive acuity in both the clinic and the laboratory. One test that has garnered particular interest is joint position matching, whereby individuals must replicate a reference joint angle in the absence of vision (ie, using proprioceptive information). On the surface, this test might seem straightforward in nature. However, the present perspective article informs therapists and researchers alike of multiple insights gained from a recent series of position matching studies by the author and colleagues. In particular, 5 factors are outlined that can assist clinicians in developing well-informed opinions regarding the outcomes of tests of position matching abilities. This information should allow for enhanced diagnosis of proprioceptive deficits within clinical settings in the future.

The biological and behavioral basis of upper limb asymmetries in sensorimotor performance

Asymmetries in upper limb performance are a fundamental aspect of human behavior. This phenomenon, commonly known as handedness, has inspired a great deal of research over the course of the past century garnering interest across a multitude of scientific domains. In the present paper, a thorough review of this literature is provided focusing on the current state of knowledge regarding neuro-anatomical and behavior-based arm asymmetries. It is hoped that this information will provide a basis for new insights regarding the design and implementation of future studies regarding arm laterality.

Upper limb asymmetries in the utilization of proprioceptive feedback

Despite the importance of proprioception during upper limb movement, the extent to which arm/hemisphere asymmetries exist in the utilization of proprioceptive feedback remains unclear. In the present study, movement accuracy and arm dynamics were examined in 20 right-handed adults during a proprioceptive matching task that required subjects to actively match remembered target positions of the elbow with the contralateral arm. As hypothesized, the results indicated an accuracy advantage in favor of the non-preferred left arm reflected by smaller absolute matching errors when compared to the preferred right arm. This advantage was most pronounced for larger amplitude movements and was not associated with any limb-specific difference in movement strategy as indicated by the dynamics of the matching movement. These results extend current theories of handedness by demonstrating that, in right-handed individuals, the non-preferred arm/hemisphere system is more adept at utilizing position-related proprioceptive information than the preferred arm/hemisphere system.

Brain Activity during Ankle Proprioceptive Stimulation Predicts Balance Performance in Young and Older Adults

Proprioceptive information from the foot/ankle provides important information regarding body sway for balance control, especially in situations where visual information is degraded or absent. Given known increases in catastrophic injury due to falls with older age, understanding the neural basis of proprioceptive processing for balance control is particularly important for older adults. In the present study, we linked neural activity in response to stimulation of key foot proprioceptors (i.e., muscle spindles) with balance ability across the lifespan. Twenty young and 20 older human adults underwent proprioceptive mapping; foot tendon vibration was compared with vibration of a nearby bone in an fMRI environment to determine regions of the brain that were active in response to muscle spindle stimulation. Several body sway metrics were also calculated for the same participants on an eyes-closed balance task. Based on regression analyses, multiple clusters of voxels were identified showing a significant relationship between muscle spindle stimulation-induced neural activity and maximum center of pressure excursion in the anterior–posterior direction. In this case, increased activation was associated with greater balance performance in parietal, frontal, and insular cortical areas, as well as structures within the basal ganglia. These correlated regions were age- and foot-stimulation side-independent and largely localized to right-sided areas of the brain thought to be involved in monitoring stimulus-driven shifts of attention. These findings support the notion that, beyond fundamental peripheral reflex mechanisms, central processing of proprioceptive signals from the foot is critical for balance control.

Task-dependent asymmetries in the utilization of proprioceptive feedback for goal-directed movement

Whereas the majority of studies regarding upper limb asymmetries in motor performance have focused on preferred arm dominance for producing motor output, studies exploring the role of sensory feedback have suggested that the preferred and non-preferred arms are specialized for different aspects of movement. A recent study by Goble et al. (2006) found evidence of a non-preferred left arm (and presumably right hemisphere) proprioceptive dominance for a target matching task that required subjects to both memorize and transfer across hemispheres proprioceptive target information. This paradigm contrasted previous studies of proprioceptive matching asymmetry that explored only memory-based matching and produced equivocal results. The purpose of the present study, therefore, was to examine task-dependent asymmetries in proprioceptive matching performance, including differences related to active versus passive presentation of the matching target. It was found that the non-preferred left arm of right handers matched target elbow angles more accurately than the preferred arm, but only in the matching condition that required both memory and interhemispheric transfer. Task-dependent asymmetries were not affected by the mode of target presentation and assessment of matching kinematics revealed differences in strategy for both the speed and smoothness of targeted movements. Taken together, these results suggest that the non-preferred arm/hemisphere system is specialized for the processing of movement-related proprioceptive feedback.

Using the Wii Fit as a tool for balance assessment and neurorehabilitation: the first half decade of “Wii-search”

The Nintendo Wii Fit was released just over five years ago as a means of improving basic fitness and overall well-being. Despite this broad mission, the Wii Fit has generated specific interest in the domain of neurorehabilitation as a biobehavioral measurement and training device for balance ability. Growing interest in Wii Fit technology is likely due to the ubiquitous nature of poor balance and catastrophic falls, which are commonly seen in older adults and various disability conditions. The present review provides the first comprehensive summary of Wii Fit balance research, giving specific insight into the system’s use for the assessment and training of balance. Overall, at the time of the fifth anniversary, work in the field showed that custom applications using the Wii Balance Board as a proxy for a force platform have great promise as a low cost and portable way to assess balance. On the other hand, use of Wii Fit software-based balance metrics has been far less effective in determining balance status. As an intervention tool, positive balance outcomes have typically been obtained using Wii Fit balance games, advocating their use for neurorehabilitative training. Despite this, limited sample sizes and few randomized control designs indicate that research regarding use of the Wii Fit system for balance intervention remains subject to improvement. Future work aimed at conducting studies with larger scale randomized control designs and a greater mechanistic focus is recommended to further advance the efficacy of this impactful neurorehabilitation tool.

The neural control of bimanual movements in the elderly: Brain regions exhibiting age‐related increases in activity, frequency‐induced neural modulation, and task‐specific compensatory recruitment

Coordinated hand use is an essential component of many activities of daily living. Although previous studies have demonstrated age‐related behavioral deficits in bimanual tasks, studies that assessed the neural basis underlying such declines in function do not exist. In this fMRI study, 16 old and 16 young healthy adults performed bimanual movements varying in coordination complexity (i.e., in‐phase, antiphase) and movement frequency (i.e., 45, 60, 75, 90% of critical antiphase speed) demands. Difficulty was normalized on an individual subject basis leading to group performances (measured by phase accuracy/stability) that were matched for young and old subjects. Despite lower overall movement frequency, the old group “overactivated” brain areas compared with the young adults. These regions included the supplementary motor area, higher order feedback processing areas, and regions typically ascribed to cognitive functions (e.g., inferior parietal cortex/dorsolateral prefrontal cortex). Further, age‐related increases in activity in the supplementary motor area and left secondary somatosensory cortex showed positive correlations with coordinative ability in the more complex antiphase task, suggesting a compensation mechanism. Lastly, for both old and young subjects, similar modulation of neural activity was seen with increased movement frequency. Overall, these findings demonstrate for the first time that bimanual movements require greater neural resources for old adults in order to match the level of performance seen in younger subjects. Nevertheless, this increase in neural activity does not preclude frequency‐induced neural modulations as a function of increased task demand in the elderly. Hum Brain Mapp, 2010.

The neural basis of central proprioceptive processing in older versus younger adults: An important sensory role for right putamen

Our sense of body position and movement independent of vision (i.e., proprioception) relies on muscle spindle feedback and is vital for performing motor acts. In this study, we first sought to elucidate age‐related differences in the central processing of proprioceptive information by stimulating foot muscle spindles and by measuring neural activation with functional magnetic resonance imaging. We found that healthy older adults activated a similar, distributed network of primary somatosensory and secondary‐associative cortical brain regions as young individuals during the vibration‐induced muscle spindle stimulation. A significant decrease in neural activity was also found in a cluster of right putamen voxels for the older age group when compared with the younger age group. Given these differences, we performed two additional analyses within each group that quantified the degree to which age‐dependent activity was related to (1) brain structure and (2) a behavioral measure of proprioceptive ability. Using diffusion tensor imaging, older (but not younger) adults with higher mean fractional anisotropy were found to have increased right putamen neural activity. Age‐dependent right putamen activity seen during tendon vibration was also correlated with a behavioral test of proprioceptive ability measuring ankle joint position sense in both young and old age groups. Partial correlation tests determined that the relationship between elderly joint position sense and neural activity in right putamen was mediated by brain structure, but not vice versa. These results suggest that structural differences within the right putamen are related to reduced activation in the elderly and potentially serve as biomarker of proprioceptive sensibility in older adults. Hum Brain Mapp, 2012.

The influence of horizontal velocity on interlimb symmetry in normal walking

Changes in horizontal velocity (HV) are known to influence many biomechanical characteristics of human locomotion. The purpose of the present study was to investigate this phenomenon with respect to the interlimb symmetry of walking in a normal population. Peak and temporal ground reaction force data from both feet of 20 able-bodied males were collected at each of three relative velocity conditions (slow, normal and fast). These data were analyzed using of a series of 2 x 3 repeated measures ANOVAs, which revealed a high degree of interlimb (bilateral) symmetry across HV conditions despite significant intralimb (unilateral) changes. In contrast to this primary finding were two significant interaction effects for the stance time and peak vertical force at push-off measures respectively. These interactions indicated greater asymmetries at the slow HV condition with a trend toward improved symmetry at higher velocities. Although these results may provide some theoretical insight into the underlying nature of symmetry in gait, their overall magnitude does not seem to invalidate the current widespread use of symmetry assumptions in clinical and research settings today.