Lower Cognitive Set Shifting Ability Is Associated With Stiffer Balance Recovery Behavior and Larger Perturbation-Evoked Cortical Responses in Older Adults

Abstract

The mechanisms underlying associations between cognitive set shifting impairments and balance dysfunction are unclear. Cognitive set shifting refers to the ability to flexibly adjust behavior to changes in task rules or contexts, which could be involved in flexibly adjusting balance recovery behavior to different contexts, such as the direction the body is falling. Prior studies found associations between cognitive set shifting impairments and severe balance dysfunction in populations experiencing frequent falls. The objective of this study was to test whether cognitive set shifting ability is expressed in successful balance recovery behavior in older adults with high clinical balance ability (N = 19, 71 ± 7 years, 6 female). We measured cognitive set shifting ability using the Trail Making Test and clinical balance ability using the miniBESTest. For most participants, cognitive set shifting performance (Trail Making Test B-A = 37 ± 20 s) was faster than normative averages (46 s for comparable age and education levels), and balance ability scores (miniBESTest = 25 ± 2/28) were above the threshold for fall risk (23 for people between 70 and 80 years). Reactive balance recovery in response to support-surface translations in anterior and posterior directions was assessed in terms of body motion, muscle activity, and brain activity. Across participants, lower cognitive set shifting ability was associated with smaller peak center of mass displacement during balance recovery, lower directional specificity of late phase balance-correcting muscle activity (i.e., greater antagonist muscle activity 200–300 ms after perturbation onset), and larger cortical N1 responses (100–200 ms). None of these measures were associated with clinical balance ability. Our results suggest that cognitive set shifting ability is expressed in balance recovery behavior even in the absence of profound clinical balance disability. Specifically, our results suggest that lower flexibility in cognitive task performance is associated with lower ability to incorporate the directional context into the cortically mediated later phase of the motor response. The resulting antagonist activity and stiffer balance behavior may help explain associations between cognitive set shifting impairments and frequent falls.

The cortical N1 response to balance perturbation is associated with balance and cognitive function in different ways between older adults with and without Parkinson’s disease

“…In the noPD group, larger N1 amplitudes were correlated with lower balance confidence (Figure 3A, p=0.026, R 2 =0.26, F 2 =0.35). As reported previously (Payne et al 2021), larger N1 amplitudes were correlated with lower cognitive set shifting ability (p=0.006, R 2 =0.37, F 2 =0.57). Balance confidence was not associated cognitive set shifting ability (p=0.25).…”

“…Distinct features of the N1 responses were associated with dissociable balance and cognitive constructs in Parkinson’s disease, suggesting the N1 response may reflect a coordination of separable mechanisms related to balance and cognitive impairments. Based on associations between balance and cognitive decline in aging populations (Allcock et al 2009; Camicioli and Majumdar 2010; Gleason et al 2009; Herman et al 2010; Mak et al 2014; Mirelman et al 2012), and prior associations between the N1 and balance (Payne and Ting 2020a) and cognitive (Payne et al 2021) abilities, we hypothesized that the N1 response might reflect a single mechanism linking balance and cognition. Instead, our construct analysis, which resolved issues of multiple comparisons across covarying measures, revealed that our balance and cognitive measures were largely dissociable, and related to distinct features of the N1 response.…”

“…A series of 48 translational support-surface perturbations of unpredictable timing, direction, and magnitude were delivered during quiet standing (Payne et al 2021). Perturbations consisted of forward and backward perturbation directions and three magnitudes.…”

“…Perturbations consisted of forward and backward perturbation directions and three magnitudes. The low magnitude (0.15 g, 11.1 cm/s, 5.1 cm) was identical across participants, while the medium (0.21-0.22 g, 15.2-16.1 cm/s, 7.0-7.4 cm) and high (0.26-0.29 g, 19.1-21.0 cm/s, 8.9-9.8 cm) magnitudes were adjusted according to participant height as previously described (Payne et al 2021) to account for the effect of height on the cortical responses (Payne et al 2019a) and to ensure that the more challenging perturbations were more mechanically similar across different body sizes. Perturbation characteristics for an example participant are shown in Figure 1.…”

“…While studies in older populations have been limited, older adults generally have smaller and later cortical N1s (Duckrow et al 1999; Ozdemir et al 2018), with changes in temporal characteristics including the appearance of multiple component peaks in some individuals with reduced mobility (Duckrow et al 1999). We recently reported associations between larger N1 amplitudes, lower cognitive set shifting ability, stiffer balance recovery behavior, and increased antagonist muscle activity in older adults (Payne et al 2021), further implicating the cortical N1 in the relationship between balance and cognitive problems with aging. We now investigate the cortical N1 responses in a population of older adults with Parkinson’s disease, who have both balance and cognitive impairments.…”