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

Abstract

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.

Ankle proprioceptive acuity is associated with objective as well as self-report measures of balance, mobility, and physical function

“…Ankle proprioceptive information is used to generate and modulate muscle contractions aimed at maintaining vertical standing balance (Fitzpatrick and McCloskey 1994;Colledge et al 1994;Goble et al 2011). During gait, the proprioceptive signal is integrated in a phasic and context-specific manner to precisely control movements of the swing limb and appropriately move the center of mass using the supporting limb (Sorensen et al 2002;Pearson 2004).…”

“…During gait, the proprioceptive signal is integrated in a phasic and context-specific manner to precisely control movements of the swing limb and appropriately move the center of mass using the supporting limb (Sorensen et al 2002;Pearson 2004). Consequently, impaired ankle proprioception has been associated with poor balance and falls in older persons (Lord et al 1991;Goble et al 2009Goble et al , 2011. Due to its critical role in standing and dynamic postural control, deterioration in ankle proprioception may also contribute to decline in global mobility and overall physical function.…”

Short-term effects of additional sensory information in mobility and gait speed in older fallers

“…The main hypothesis, found in studies, suggests the increase of afferents by constant cutaneous stimulation, greater stimulation to the superficial skin receptors and local receptors, with consequent improvement of the articular proprioceptive response (12)(13)(14)(15)(16)22) . Older fallers present reduced mobility and are more likely to decrease muscle strength caused by aging and inactivity, with consequent impact on walking and stabilization of the ankle and hip (36). The stimulus increase coming from the sub-patellar strip can favor the kinematics of the knee joint and produce beneficial results in the mobility and walking speed of this population (13,35) .…”

“…The stimulus increase coming from the sub-patellar strip can favor the kinematics of the knee joint and produce beneficial results in the mobility and walking speed of this population (13,35) . The activated brain areas for postural balance maintenance receive less stimuli in aging, and for this reason they present less activation in these regions (36) . The addition of sensory information can increase the stimuli for the less activated regions and thus improving the proprioceptive response in postural control (13,36) .…”

“…The activated brain areas for postural balance maintenance receive less stimuli in aging, and for this reason they present less activation in these regions (36) . The addition of sensory information can increase the stimuli for the less activated regions and thus improving the proprioceptive response in postural control (13,36) . In agreement with Globe et al (37) , the proprioceptive feedback has a strong influence on the maintenance of postural control.…”