Repeated exposure to the threat of perturbation induces emotional, cognitive, and postural adaptations in young and older adults
Introduction
Research has examined the influence of fall-related anxiety on postural control by manipulating the perceived consequences or likelihood of instability. This is often accomplished through experimental manipulation of the height at which individuals stand (Adkin and Carpenter, 2018). When standing at or close to the edge of an elevated platform, healthy young and older adults lean away from the edge and adopt an ankle stiffening strategy characterized by reductions in centre of pressure (COP) amplitude and increases in COP frequency (Carpenter et al., 2006; Cleworth and Carpenter, 2016; Cleworth et al., 2012; Davis et al., 2009; Hauck et al., 2008; Zaback et al., 2015).
Postural threat has also been manipulated by altering the expectation of receiving an unpredictable perturbation to balance. When standing in anticipation of receiving an unpredictable anteroposterior (AP) support surface translation, young adults lean forward and demonstrate increases in the amplitude and frequency of COP displacements (Johnson et al., 2017). Unlike the similar postural strategies observed in young and older adults with height-induced threat (Carpenter et al., 2006), age-related differences have been revealed in response to postural perturbation threat. When standing in anticipation of receiving unexpected forward or backward nudges to the trunk, young adults increase trunk sway whereas older adults reduce lateral trunk sway despite similar increases in self-reported feelings of anxiety (Shaw et al., 2012). However, in this study, vision was removed to facilitate the delivery of unexpected trunk perturbations and base-of-support was constrained (i.e., feet were placed together) to maximize postural threat. These methodological limitations may have confounded the results as older compared to young adults rely more on visual information to maintain stability (Bugnariu and Fung, 2007) and require more attention to maintain challenging stance positions (Lajoie et al., 1996). Therefore, further evaluation of threat-induced responses in older adults is warranted to confirm the findings of Shaw et al. (2012) and obtain a more comprehensive understanding of age effects on the relationship between anxiety and postural control in different threat scenarios.
While changes in postural control with different postural threat manipulations have been well characterized, particularly in young adults, the mechanisms contributing to these changes are not clear. Recent work has suggested that changes in attention focus may contribute to changes in postural control when threatened. Young adults report broad changes in attention focus in threatening compared to non-threatening conditions, including increased attempts to consciously control or monitor posture, increased attention to threat-related stimuli, and increased use of coping strategies to alleviate anxiety, which have been associated with specific changes in static and dynamic postural control (Huffman et al., 2009; Johnson et al., 2017; Zaback et al., 2016). Research has shown that similar to young adults, older adults demonstrate an anxiety-induced attentional bias to threat-related stimuli (Fox and Knight, 2005). However, older adults may regulate negative emotions using cognitive strategies such as attentional deployment (i.e., distraction) more efficiently than young adults (Wirth and Kunzmann, 2018). Furthermore, older adults, who have also been shown to report increased conscious control of movement when threatened (Young et al., 2016), maintain a greater attentional prioritization of postural stability than young adults when standing under conditions of postural threat and performing a secondary cognitive task (Brown et al., 2002). This collection of evidence suggests that age-related differences in attention focus emerge with increases in state anxiety; these changes in attention may contribute to previously reported differences in threat-induced postural modifications between young and older adults (Shaw et al., 2012). However, to our knowledge, broad changes in attention focus beyond increases in conscious movement control (Young et al., 2016) have not been quantified in older adults within the context of postural threat.
Limited research has shown that young adults can modulate threat-induced postural control changes based on prior threat experience (Brown and Frank, 1997; Johnson et al., 2017; Maki and Whitelaw, 1993). For instance, after gaining perturbation threat experience, young adults further increase COP frequency and reduce COP amplitude relative to their initial threat-induced postural strategy (Johnson et al., 2017). Over longer periods of exposure to an AP perturbation threat, young adults demonstrate gradual reductions in anticipatory forward leaning; this adaptation is associated with reductions in arousal (Maki and Whitelaw, 1993). Moreover, displacement of the body's centre of mass becomes gradually less restricted as young adults respond to a series of forward pushes to the trunk while standing under height-related threat (Brown and Frank, 1997). It was suggested that individuals relax with experience as the perceived threat of falling gradually decreases following initial threat exposure. This premise is foundational to behavioural sensitization techniques, which systematically expose individuals to a threatening stimulus (e.g., increased heights) to reduce or normalize the emotional response to that threat (Lang and Craske, 2000).
Many fall-prevention studies have subjected older adults to repeated trials of unexpected support surface translations to explore adaptation of postural reactions over time. Despite some differences in postural strategy compared to young adults (Maki et al., 2000; Mille et al., 2005), older adults maintain the ability to adapt postural control (Dijkstra et al., 2015). For example, older adults initially exhibit poorer compensatory stepping responses compared to young adults but can adapt these responses to match performance of young adults with repeated AP perturbations (Dijkstra et al., 2015). Similarly, older adults are more likely to fall from initial slip perturbations delivered during a sit-to-stand movement, but both young and older adults can improve compensatory responses with repeated exposure (Pavol et al., 2002). Compensatory responses to perturbations are influenced by pre-perturbation postural strategy (Rajachandrakumar et al., 2018; Tokuno et al., 2006), so age-related differences in standing postural control, like compensatory responses, could presumably emerge during initial threat exposure but attenuate over the course of threat exposure. However, older adults' capacity to adapt standing balance in anticipation of receiving a perturbation has not been explored. Understanding how fall-related anxiety influences adaptive postural control processes may have important implications for the assessment of balance and the design and evaluation of interventions for older adults progressively debilitated by pathological anxiety or fear of falling (Zijlstra et al., 2007).
The current study investigated the extent to which age influences emotional, cognitive, and postural adaptations to initial and repeated postural threat exposure. Postural threat was manipulated through the expectation of receiving an unpredictable support surface translation during stance. We predicted that postural threat would elicit an emotional response in young and older adults that would return toward no threat levels with repeated threat exposure. In addition, we hypothesized that when threatened, young and older adults would demonstrate broad changes in attention focus with older adults directing more attention to specific elements of attention focus (e.g., movement processes, threat-related stimuli and/or self-regulatory strategies) compared to young adults (Brown et al., 2002; Fox and Knight, 2005; Wirth and Kunzmann, 2018; Young et al., 2016), all of which would decrease toward no threat levels with repeated threat exposure. Finally, we hypothesized that age-related differences in postural control would emerge when initially threatened but would gradually diminish with repeated threat exposure, and young and older adults would adapt threat-induced changes in postural control with repeated threat exposure toward no threat levels (Maki and Whitelaw, 1993).
Section snippets
Participants
Twenty-seven healthy older adults (13 female, mean ± one standard deviation [SD] age = 70.0 ± 4.1 years, height = 170.9 ± 8.6 cm, mass = 75.6 ± 14.4 kg) and twenty-seven healthy young adults (16 female, mean ± SD age = 22.2 ± 3.9 years, height = 171.4 ± 9.4 cm, mass = 69.8 ± 12.2 kg) living independently in the community volunteered to participate in this study. Exclusion criteria included any self-reported neurological or musculoskeletal condition that could influence postural control. All
Results
Descriptive statistics and mean differences for all emotional, cognitive, and postural measures collapsed across age for all conditions are presented in Table 1. Unless stated otherwise, there were no significant main effects of age or age by threat interaction effects.
Discussion
This study 1) replicates previous research which has shown that the threat of perturbation elicits an emotional response, broad changes in attention focus, and changes in postural control in healthy young adults (Johnson et al., 2017); 2) extends our understanding of postural threat effects in healthy older adults; and 3) provides insight into adaptation of threat-related responses with repeated threat exposure in healthy young and older adults. Postural threat effects were similar between
Conclusion
This study explored emotional, cognitive, and postural adaptations to initial and repeated postural threat exposure in healthy young and older adults. Young and older adults demonstrated similar adaptations to initial and repeated threat exposure. Despite significant adaptation of individuals' emotional and cognitive responses to threat following repeated threat exposure, only some threat-related changes in standing postural control demonstrated adaptation. This suggests that some
Declarations of interest
None.
Funding
This work was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Grants to CDT (386609), MGC (326910) and ALA (288164).
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