A postural unloading task to assess fast corrective responses in the upper limb following stroke

Abstract

BackgroundRobotic technologies to measure human behavior are emerging as a new approach to assess brain function. Recently, we developed a robot-based postural Load Task to assess corrective responses to mechanical disturbances to the arm and found impairments in many participants with stroke compared to a healthy cohort (Bourke et al, J NeuroEngineering Rehabil 12: 7, 2015). However, a striking feature was the large range and skewed distribution of healthy performance. This likely reflects the use of different strategies across the healthy control sample, making it difficult to identify impairments. Here, we developed an intuitive “Unload Task”. We hypothesized this task would reduce healthy performance variability and improve the detection of impairment following stroke.MethodsPerformance on the Load and Unload Task in the KINARM exoskeleton robot was directly compared for healthy control (n = 107) and stroke (n = 31) participants. The goal was to keep a cursor representing the hand inside a virtual target and return “quickly and accurately” if the robot applied (or removed) an unexpected load to the arm (0.5–1.5 Nm). Several kinematic parameters quantified performance. Impairment was defined as performance outside the 95% of controls (corrected for age, sex and handedness). Task Scores were calculated using standardized parameter scores reflecting overall task performance.ResultsThe distribution of healthy control performance was smaller and less skewed for the Unload Task compared to the Load Task. Fewer task outliers (outside 99.9 percentile for controls) were removed from the Unload Task (3.7%) compared to the Load Task (7.4%) when developing normative models of performance. Critically, more participants with stroke failed the Unload Task based on Task Score with their affected arm (68%) compared to the Load Task (23%). More impairments were found at the parameter level for the Unload (median = 52%) compared to Load Task (median = 29%).ConclusionsThe Unload Task provides an improved approach to assess fast corrective responses of the arm. We found that corrective responses are impaired in persons living with stroke, often equally in both arms. Impairments in generating rapid motor corrections may place individuals at greater risk of falls when they move and interact in the environment.

Maintaining arm control during self‐triggered and unpredictable unloading perturbations

“…Key to our design is its naturalism—motivated by our previous work in the jaw (Johansson, Pruszynski, Edin, & Westberg, ; Johansson, Westburg, & Edin, )—where the participants are in active control of the force increase needed to trigger the sudden and unpredictable decrease in resistive force. This is in contrast to previous studies along these lines where unloading was triggered by an external source (Angel, Eppler, & Iannone, ; Asatryan & Feldman, ; Dufossé, Hugon, & Massion, ; Grago, Houk, & Hasan, ; Latash & Gottlieb, ; Lowrey, Bourke, Bagg, Dukelow, & Scott, ; Paulignan, Dufossé, Hugon, & Massion, ). For example, in Angel and colleagues’ seminal study of reactions to unloading (1965) the participant counteracts a preset force level while controlling their position and passively waits for the unpredictable unloading event to be triggered by the experimenter cutting a wire.…”

“…Unloading paradigms have been used by many previous groups to study a variety of behavioral phenomena. Some studies have used unloading events triggered by an experimenter to evoke postural perturbations (Angel et al., ; Lowrey et al., ) or investigate muscle characteristics under do‐not‐intervene instructions (Archambault, Mihaltchev, Levin, & Feldman, ). Other studies have used self‐triggered unloading perturbations to investigate preparation for expected perturbations to the upper limb (Johannson & Westling, ; Kennedy & Schwartz, ; Lum et al., ) or whole body (Aruin & Latash, ), or to trigger perturbations with unknown directions (Piscitelli, Falaki, Solnik, & Latash, ).…”

Maintaining arm control during self-triggered and unpredictable unloading perturbations

“…Key to our design is its naturalism -motivated by our previous work in the jaw (Johansson 2014a,b) -where the participants are in active control of the force increase needed to trigger the sudden and unpredictable decrease in resistive force. This is contrast to previous studies along these lines where unloading was triggered by an external source (Angel et al 1965, Asatryan & Feldman 1965, Crago et al 1976, Dufossé et al 1985, Paulignan et al 1989, Latash & Gottlieb 1991, Lowrey et al 2019. For example, in Angel and colleagues' seminal study of reactions to unloading (1965) the participant counteracts a preset force level while controlling their position and passively waits for the unpredictable unloading event to be triggered by the experimenter cutting a wire.…”

“…Unloading paradigms have been used by many previous groups to study a variety of behavioral phenomena. Some studies have used unloading events triggered by an experimenter to evoke postural perturbations (Angel et al 1965, Lowrey et al 2019 or investigate muscle characteristics under do-not-intervene instructions (Archambault et al 2005). Other studies have used self-triggered unloading perturbations to investigate preparation for expected perturbations to the upper limb (Lum et al 1992, Johansson & Westling 1988, Kennedy & Schwartz 2018 or whole body (Aruin & Latash 1995), or to trigger perturbations with unknown directions (Piscitelli et al 2017).…”

Robotic tests for position sense and movement discrimination in the upper limb reveal that they each are highly reproducible but not correlated in healthy individuals

“…The potential caveat with this approach is the assumption that proprioceptive and motor function of the other arm is not impaired. However, ipsilesional impairments can be observed in some individuals (~30%) following stroke [30][31][32][33][34]. Further, bilateral impairments are common in other diseases such as ALS [35][36][37].…”