Proprioception in aging: Effects of a healthy active lifestyle and Parkinson’s disease on ankle position sense

Abstract

Introduction: Proprioceptive afferents are processed at multiple levels of the central nervous system and give rise to the conscious perception of body and limb position (i.e. the proprioceptive sense) and unconscious regulation of muscle tone. Proprioceptive function declines in typical aging. This cumulative dissertation concerns the proprioceptive sense in two neurologically polar aging populations: healthy active adults (Project 1) and people with Parkinson’s disease (PD, Project 2). Project 1: Emerging evidence indicates that physical activity may spare older adults from age-related proprioceptive decline. However, the role of physical activity in preserving position sense at the ankle was unknown, in part because objective and precise measures of ankle proprioception have not been available. Aim 1: Determine the influence of a physically active lifestyle on ankle position sense acuity in healthy aging adults. Methods: This study applied sensory psychophysics to obtain a just-noticeable-difference (JND) threshold and Uncertainty Area (UA) as measures of ankle position sense acuity in young, middle-aged, and older adults. Participants were tested at two reference positions, 15° and 25°. Results: At the 15° reference, younger adults had smaller JND thresholds than both older groups (χ2(2) = 7.953, p = 0.019, η2 = 0.048). The effect size was small as 74% and 71% of middle-aged and older adults, respectively, had thresholds within the range of controls. No differences between groups were found for JND threshold at the 25° reference position nor for UA at either reference position. Only a subset of participants adhered to Weber’s law (young adults: 81%, middle-aged: 67%, older adults: 52%), which is a principle in psychophysics stating that the JND threshold is proportional to the magnitude of the stimulus. Project 2: Parkinson’s disease alters the processing of proprioceptive information resulting in impaired limb proprioception and increased muscle rigidity. Research has not firmly established that ankle proprioception is systematically impaired in people with PD, nor has the relationship been delineated between ankle proprioception and muscle rigidity. Aim 2a: Determine the extent to which ankle position sense is impaired in people with mild-to-moderate PD. Aim 2b: Examine the relationship between ankle position sense acuity and lower extremity rigidity in mild-to-moderate PD. Methods: Using the same methods established in Project 1, JND threshold and UA were obtained as measures of ankle position sense acuity in people with mild-to-moderate PD and age-matched controls. The MDS-UPDRS was used to obtain a clinical impression of rigidity. The more affected leg was assessed for both ankle position sense acuity and rigidity in people with PD. Results: Median ankle position sense JND threshold and UA were significantly larger in the Parkinsonian group than controls (JND threshold: z = 66, p = 0.020, r = 0.413; UA: z = 68.5, p = 0.044, r = 0.366). Yet, 62.5% and 80% of participants with PD had JND thresholds and UA values, respectively, within the range of the controls. JND threshold correlated with lower extremity rigidity (ρ = 0.50, p = 0.047). Disease duration was moderately correlated with JND threshold (r = 0.52, p = 0.039) and the clinical assessment of rigidity (ρ = 0.57, p = 0.020). JND threshold also correlated moderately with levodopa equivalent dosage (r = 0.54, p = 0.03). Discussion and conclusion: This dissertation challenges prevailing assumptions about ankle proprioceptive decline in aging, demonstrating that a habitually active lifestyle can preserve ankle proprioceptive function. In contrast, people with PD showed evidence of impaired position sense. Importantly, proprioceptive decline was associated with Parkinsonian muscle rigidity, establishing for the first time, a link between abnormal proprioceptive perception and abnormal control of muscle tone.