Abstract
The results of this study demonstrate that the initiation of dual-tasking is curtailed in the nondominant and paretic upper extremities in the context of the performance of activities of daily living (ADLs) among adults with and without stroke, which may reflect a demand on neural resources that is exceeded when these limbs are used.
Over the course of a day, a person may dual-task, or carry out two actions simultaneously, in the performance of activities of daily living (ADLs) or instrumental ADLs. For example, a person may plan out their day while washing their hair (cognitive– motor dual-tasking) or scroll on a smartphone while holding onto a bus railing (motor–motor dual-tasking). Although activities can be performed without dual-tasking, and dual-tasking can degrade motor performance relative to execution of a single task (Baddeley et al., 1986; Pashler, 1994), it may be used as a strategy to increase efficiency when the cost of poorer performance is low (Adler & Benbunan-Fich, 2012). Successful dual-tasking is believed to reflect a person’s overall processing capacity or the ability to simultaneously manage two programs by the same processing channel (Koch et al., 2018). Thus, the ability to dual-task or its return with rehabilitation training may signal the presence of neural structures with sufficient integrity or functional capacity to support this complex processing, which is of interest to occupational therapy practitioners.
Dual-tasking has been mainly examined in laboratory settings with paradigms that artificially enforce the sustained and simultaneous execution of two actions (Baddeley et al., 1986; Kemper et al., 2006; Strenge & Niederberger, 2008). This artifice may limit the generalizability of laboratory-based findings to more naturalistic settings, where the volitional integration of dual-tasking may be more sporadic or influenced by overall processing capacity. Examining dual-tasking during performance of ADLs could thus directly read out functionally limiting abnormalities that could be targeted with clinical interventions. It is thus important to understand how this laboratory-based phenomenon maps to real-world strategy and to identify ecologically valid markers of dual-tasking among patients with stroke.
Previously, we found that ADLs can be broken down into functional primitives: singular motions or minimal motions made with respect to a single object (Schambra et al., 2019). Single-object primitives (SOPs), categorized as reaches, repositions, transports, stabilizations, and idles, are sequentially strung together to complete a full ADL as the upper extremity (UE) engages one target object at a time. We also observed instances when the UE performs two motor actions while engaging two objects simultaneously, which we call dual-object primitives (DOPs; Figure 1). DOPs entail the UE holding onto an object (the DOP object) while reaching to, transporting, or stabilizing a new object (the target object). For example, the hand may hold a toothbrush while simultaneously transporting a faucet handle to turn on the water, or the UE may hold a water bottle between the trunk and arm while stabilizing a plate of food.
Single-object primitives (SOPs) and their dual-object primitive (DOP) counterparts.
Because DOPs require parallel actions on two objects, we interpret their execution as motor–motor dual-tasking. In the toothbrushing example used previously, execution of the faucet-directed action (turning on water) occurs during a simultaneous toothbrush- directed action (holding for later reincorporation into the activity). A motor command produces this concurrent hold of the DOP object with potential in-hand reorientation or grasp change (e.g., from four to two fingers) to facilitate action on the new target object (Feix et al., 2016; Pehoski et al., 1997).
Here, we sought to understand how motor–motor dual-tasking, as manifested by DOPs, may be volitionally incorporated into the execution of daily activities. We examined the use of DOPs by control participants and participants with stroke as they performed two exemplar ADLs: feeding and toothbrushing. We also examined the effects of dominance and paresis on DOP performance to identify whether findings from laboratory-based studies are borne out in a real-world context. In these previous dual-tasking studies, researchers found that motor performance degrades more prominently on the nondominant than dominant side of healthy participants (Strenge & Niederberger, 2008) and among patients with stroke compared with healthy participants (Kemper et al., 2006; Regnaux et al., 2005; Yang et al., 2007). Finally, we explored the DOP characteristics of the participant groups to identify whether execution strategies are altered in stroke.
Method
Participants
We studied participants who were enrolled in an unrelated observational study to develop a rehabilitation measurement tool (Kaku et al., 2021). We screened 22 and 748 adults with and without stroke, respectively, enrolling 19 control participants and 43 participants with chronic stroke. All participants were right-handed (premorbid in stroke), age ≥18 yr, and able to give informed consent. We included participants with stroke if they had unilateral motor stroke and contralateral UE weakness with a Medical Research Council score <5 (of 5) in at least one major muscle group. We used physical examination, medical records, and clinical scales to evaluate for the following exclusions: nonstroke conditions (e.g., Parkinson’s disease, neuropathy, myopathy) that interfere with motor function, visuospatial neglect, apraxia (Test for Upper-Limb Apraxia; Vanbellingen et al., 2011), global inattention, legal blindness, truncal ataxia or moderate UE dysmetria (Scale for the Assessment and Rating of Ataxia; Subramony, 2007), and UE contracture (>3 on the Modified Ashworth Scale; Bohannon & Smith, 1987). The local institutional review board approved the study, and participants gave written informed consent to participate.
Study Design
In this observational study, we examined the videotaped performance of participants performing two ADLs to identify SOPs and DOPs (see Figure 1). A trained assessor also evaluated for motor and cognitive impairment with the UE Fugl-Meyer Assessment (UE–FMA; Fugl-Meyer et al., 1975) and the Montreal Cognitive Assessment (MoCA; Nasreddine et al., 2005), respectively. We did not assess sensory impairment.
Task Performance
Participants performed five trials each of a feeding and a toothbrushing activity. For feeding, participants sat at a table with a plate, fork, knife, and slice of bread in a plastic sandwich bag. We instructed participants to remove the bread from the bag and place it on the plate, butter and cut the bread, and eat a piece. For toothbrushing, participants sat in front of a sink with a toothbrush, toothpaste, and cup of water. We instructed participants to wet and apply toothpaste to the toothbrush, brush their teeth, and rinse with the cup of water. For each activity, we outlined the main components of the task before it started but did not otherwise instruct each step.
Video Recording
We recorded the activities with two video cameras (Ninox 125; Noraxon, Scottsdale, AZ; 60 frames per second, 1088 × 74 resolution) positioned orthogonal to the participant. Trained coders examined the video recordings using video review software (myoMOTION) to identify SOPs and DOPs. In an SOP, a participant engages one target object (see Figure 1A). In a DOP, a participant engages a target object while another object, the DOP object, is already in hand (see Figure 1B).
Primitive Identification
Using a previously established functional motion taxonomy (Schambra et al., 2019), we identified the five following classes of SOPs: reach, reposition, transport, stabilize, and idle. A reach is a UE motion to move into contact with a target object; reposition is a UE motion to move proximate to a target object; transport is a UE motion to convey a target object; stabilize is a minimal motion to keep a target object still; and idle is a minimal motion to stand at the ready near a target object (Schambra et al., 2019). We additionally identified DOPs, which can occur during reach, transport, and stabilize—primitives in which objects are already engaged.
We counted the SOPs and DOPs performed by the bilateral UEs of control participants and the paretic UE of participants with stroke. We note that the paretic UE could be either left or right side and that the nonparetic UE was not examined. For each DOP, we also recorded the primitive type (reach, transport, or stabilization), target object, and grasp type on the target object (prehensile or nonprehensile). Prehensile grasps use ≥2 points of contact to generate opposing forces to secure the target object, for example, grasping the toothpaste in hand. Nonprehensile grasps use one point of contact to secure the object against an opposing external force such as gravity or the normal force of a surface, for example, pinning down a slice of bread to a plate (Schambra et al., 2019). We characterized DOP grasp types for only transports and stabilizations, because grasp is not fully manifest in reaches (Schambra et al., 2019).
Analyses
We assessed dual-tasking in each control participant and participant with stroke using two DOP performance outcomes: DOP initiation and DOP frequency. We examined DOP initiation to ascertain whether a participant used dual-tasking overall as a strategy in activity execution. We operationalized DOP initiation as the performance of at least one DOP in either activity. We examined DOP frequency to ascertain how often a participant used dual-tasking if used altogether (i.e., we excluded participants who did not initiate DOPs). We operationalized DOP frequency as the total DOP count normalized to the total primitive count (SOP + DOP) in each activity, then averaged across activities. Normalization adjusted for the variable number of primitives performed by each participant.
To assess whether dominance affects dual-tasking, we compared DOP performance outcomes in the right (dominant) versus left (nondominant) sides of the same control participants, and in the right (dominant) versus left (nondominant) paretic sides of different participants with stroke (nonparetic data were unavailable). To assess whether stroke affects dual-tasking, we compared DOP performance outcomes of control UEs versus side-matched paretic UEs. We used Fisher’s exact test to examine DOP initiation within and between participant groups, and the Mann–Whitney U test to examine DOP frequency (non-normally distributed) within and between participant groups.
Among participants with stroke, we also assessed whether degree of motor or cognitive impairment affects dual-tasking. We used logistic regression and Spearman’s correlation, respectively, to examine the relationship between DOP initiation and frequency and ordinal UE–FMA and MoCA scores.
Finally, we explored whether participant groups differed in their strategies for DOP execution, characterizing primitive types, target objects, and grasp type for each participant who initiated DOPs. We combined data from both activities for this analysis. Per participant, we calculated primitive type as the percentage of reaches, transports, or stabilizes that were performed as a DOP. We also identified the most common target objects by calculating their frequency of use in DOPs. Finally, we identified the frequency of grasp types used in transport and stabilize DOPs. We set significance at p < .05, and we report observations as mean or median and range. All analyses were performed with JMP Pro 15 (JMP, Cary, NC).
Results
Participants
We studied 19 control participants and 43 participants with chronic stroke, with the following demographic and clinical characteristics: control participants—10 men and 9 women, mean age = 62.0 yr (range = 42.0–82.9), mean FMA score = 65.5 points (range = 62–66), mean MoCA score = 27.1 points (range = 23–30); participants with chronic stroke—23 men and 20 women (24 with left paresis), mean age = 57.5 yr (range = 21.2–85.0), mean time after stroke = 5.7 yr (range = 0.3–38.4), mean FMA score = 48.2 points (range = 26–65), mean MoCA score = 25.4 points (range = 18–30).
Initiation of Dual-Object Primitives
Among control participants and participants with stroke, we compared the initiation of DOPs within and across groups (Figure 2). Among control participants, DOPs were initiated on 19 of 19 (100%) right sides and 12 of 19 (63%) left sides. Among participants with stroke, DOPs were initiated on 11 of 19 (58%) right paretic sides and 8 of 16 (50%) left paretic sides. We examined whether dominance affected DOP initiation, comparing right (dominant) versus left (nondominant) sides. In the UEs of control participants, DOP initiation was higher on the right than left side (p = .008). In the paretic UEs of participants with stroke, however, DOP initiation was not significantly different between paretic right and paretic left sides (p = .132). We also examined whether stroke reduced the initiation of DOPs, comparing the matched sides of control participants and participants with stroke. On the right side, DOP initiation was lower in paretic UEs than control UEs (p = .003). On the left side, DOP initiation was not significantly different between paretic UEs and control UEs, although a trend was found (p = .069).
Initiation of dual-object primitives (DOPs) in control and paretic upper extremities (UEs), split by side, during performance of feeding and toothbrushing tasks.
Frequency of Dual-Object Primitives
In the subset of control participants and participants with stroke who initiated DOPs, we compared DOP frequency within and across groups (Figure 3). Although DOPs were initiated, they were not commonly performed by either control participants or participants with stroke: control participants—median frequency of total primitives for the right side = 5.9% (range = 0.3%–11.3%), median frequency of total primitives for the left side = 1.7% (range = 0.4%–18.1%); participants with stroke—median frequency of total primitives for the paretic right side = 1.9% (range = 0.6%–8.7%), median frequency of total primitives for the paretic left side = 2.3% (range = 0.6%–5.6%). We examined whether dominance affects DOP frequency, comparing right versus left sides. In both control and paretic UEs, DOP frequency was comparable between right and left sides (control participants: Z = −1.1, p = .283; participants with stroke: Z = −0.4, p = .710). We also examined whether stroke reduced DOP frequency, comparing the matched sides of control participants versus participants with stroke. On both right and left sides, DOP frequency was comparable between control and paretic UEs (right: Z = −1.4, p = .155; left: Z = −0.1, p = .908).
Frequency of dual-object primitives (DOPs) in control and paretic upper extremities that initiated DOPs, split by side.
Relationship Between Dual-Object Primitive Performance and Impairment in Stroke
Among participants with stroke, we next examined whether motor or cognitive impairments influenced DOP performance by the paretic UE, collapsing the right and left sides. We first examined whether DOP initiation related to motor impairment, finding a positive relationship between DOP initiation and UE–FMA score, χ2(22) = 37.5, p = .021 (Figure 4). DOPs were consistently absent among participants with UE–FMA scores ≤38, but they were initiated by 61% of participants with scores ≥42. We found a similar trend for a relationship between DOP initiation and the UE–FMA hand subscore, χ2(10) = 17.3, p = .067 (Figure 4). DOPs were consistently absent among participants with hand subscores ≤3, but they were initiated by 53% of participants with subscores ≥5. We also examined whether DOP frequency related to motor impairment among participants with stroke who initiated DOPs, but we found no relationship to the overall UE–FMA score (ρ = .22, p = .356; Figure 4) or hand subscore (ρ = .21, p = .386; data not shown). Finally, we examined whether DOP performance related to cognitive impairment, but we found no relationship between DOP initiation, χ2(22) = 18.3, p = .687, or DOP frequency (ρ = −.11, p = .666), and MoCA score (data not shown).
Relationship between dual-object primitive (DOP) performance and motor impairment in stroke.
Dual-Object Primitive Strategy With Respect to Primitive Type, Target Object, and Grasp Type
Among control participants and participants with stroke, we collapsed data across sides and explored whether DOP strategies differed across groups. Both groups most commonly performed DOPs during reaches (mean percentage of primitive class per participant group: control, 13.6%; stroke, 7.9%), followed by stabilizations (control, 6.9%; stroke, 3.1%) and transports (control, 3.5%; stroke, 1.5%). Both groups also commonly targeted the same objects during DOP performance: the toothpaste tube (mean percentage of DOPs per participant group: control, 34.7%; stroke, 48.4%), faucet handle (control, 13.9%; stroke, 10.1%), toothbrush (control, 8.5%; stroke, 14.2%), toothpaste cap (control, 13.7%; stroke, 11.8%), and bread (control, 17.1%; stroke, 9.9%). Finally, both groups more commonly used prehensile grasps (mean percentage of DOPs per participant group: control, 77.8%; stroke, 78.7%) than nonprehensile grasps (control, 22.2%; stroke, 21.3%) for DOP execution.
Discussion
In this cross-sectional, observational study of control participants and participants with stroke, we newly describe DOPs, a functional motion strategy to manage two objects simultaneously during ADLs. DOPs entail the reach to, transport of, or stabilization of a new object while another object is already held. We used DOPs as a behavioral marker of dual-tasking in real-world activities. In this study, we found that the strategy of dual-tasking, as measured with DOPs, was used infrequently by both control participants and participants with two typical ADLs (<19% of total primitives). We also found that both dominance and paresis affected DOP initiation but not DOP frequency. Among participants with stroke, only motor impairment influenced DOP initiation. Finally, control participants and participants with stroke shared similar performance strategies to execute DOPs. These findings collectively suggest that dual-tasking is a conserved behavioral strategy that is more cautiously used when a less-skilled or more impaired UE is used.
When dual-tasking is examined in laboratory settings, the focus is typically on how task performance degrades (Baddeley et al., 1986; Pashler, 1994) rather than how dual-tasking is integrated into performing an activity. In previous laboratory-based work with healthy participants, researchers found that dual- tasking of cognitive and motor actions causes greater motor slowing on the nondominant than dominant side (e.g., Strenge & Niederberger, 2008). Our finding of less DOP initiation by the nondominant side of control participants could suggest a motor strategy to limit DOPs to avoid slowing task completion. Among participants with stroke, the effect of dominance in the setting of dual-tasking has not been previously examined. We found no notable dominance effect on DOP initiation by the paretic UEs, which could be explained in part by the overall reduction of initiation in the setting of paresis, as discussed next.
Stroke challenges the use of dual-tasking. In laboratory studies in which cognitive–motor or motor– motor dual-tasking paradigms were used, motor performance was worse among participants with stroke compared with control participants (Kemper et al., 2006; Regnaux et al., 2005; Yang et al., 2007). In the investigation of motor–motor dual-tasking (Yang et al., 2007), researchers examined effects only on ambulation performance and not UE performance. The investigation of motor–motor dual-tasking on UE performance has not been previously examined. Here, we showed that DOP initiation was generally lower in the paretic UE compared with side-matched control UEs. We also showed that DOP initiation was less common among participants with stroke with lower UE–FMA scores, in keeping with previous findings that patients with greater motor impairment also had greater motor performance decrements on a cognitive–motor dual-task (Bank et al., 2018). It is possible that limiting DOP initiation by the paretic limb is a motor strategy to ensure successful performance of an activity, especially if the limb is more impaired.
Interestingly, we found that after DOPs could be initiated, the frequency of their performance was unaffected by dominance or paresis. We note that the use of DOPs was infrequent for the two sampled activities, so we may be underpowered to detect subtle group differences. Alternatively, DOP initiation and integration into activities may be determined by the availability of a sufficient neural substrate. In healthy participants, brain activation increases during performance of dual-tasks compared with single-tasks (Herath et al., 2001; Holtzer et al., 2011; Schubert & Szameitat, 2003). Similarly, brain activation increases with motor performance by the nondominant versus dominant side in healthy participants (Kapreli et al., 2006; Kawashima et al., 1993; Verstynen et al., 2005) and paretic versus nonparetic UE in participants with stroke (Chollet et al., 1991; Grefkes et al., 2008).
It is thus conceivable that dual-tasking with the nondominant side or paretic UE requires extra processing capabilities. If neural resources are sufficiently available to the person, DOPs can be initiated and used freely. If neural resources are outstripped, DOP initiation is curtailed. Although this explanation is speculative, future functional neuroimaging or electroencephalography studies could be used to investigate the neural activity correlates of DOP performance, particularly in the context of dominance and stroke.
Finally, we found that DOP execution strategies were conserved across participant groups. Both control participants and participants with stroke performed DOPs most commonly as a reach, targeted the same objects during activity performance, and used prehensile grasps during DOP performance. These findings suggest that after DOPs are initiated, their strategic integration into activity performance is preserved after stroke, despite the potential for disruption to movement planning or sequencing. This preservation could also be related to the milder motor and cognitive impairment levels of our participant cohort.
Study Limitations
We note some limitations of our study. We examined DOPs in two ADLs, which do not represent the full repertoire of UE activities and, therefore, may not capture the range of DOP performance in everyday life. We also did not assess DOP performance of the nonparetic UEs of participants with stroke. It is possible that the nonparetic UE may increase DOP performance as a compensatory strategy while reducing paretic DOP use. Nonparetic data may also inform whether reduced DOP initiation on the paretic side is because of weakness versus altered motor planning and sequencing after stroke, which would be expected to have more global (i.e., bilateral) effects. We also did not assess for sensory impairments and their influence on DOP performance. It is possible that DOP execution requires intact light touch, pressure, and proprioceptive sensation to successfully engage a DOP object when not under direct visual guidance. Finally, we did not capture the kinematic characteristics of DOPs. The quality of DOP execution may reveal more subtle differences in nondominant and paretic UE performance that are not captured by our current metrics, which is an area for future study.
Implications for Occupational Therapy Practice
The results of this study have the following implications for occupational therapy practice: DOPs serve as a behavioral marker of dual-tasking ability and provide occupational therapy practitioners with the ability to evaluate this strategy in a real-world context rather than in a laboratory-based setting. A lack of their incorporation into daily activities may indicate diminished neural capacity. Participants with stroke were less likely to initiate DOPs with their paretic UE than side-matched control UEs. To train a person’s complex processing abilities using dual-tasking, occupational therapy practitioners may consider purposefully training on tasks that have single target objects versus DOP objects that require in-hand grasp or manipulation. Occupational therapy practitioners may consider using verbal cuing, action observation, or hand-over-hand assistance to aid patients in incorporating DOPs into ADL execution. DOPs may provide an alternative form of dual-task training during occupational therapy sessions that does not require ambulation or cognitive tasks.
Conclusion
In this study, we characterized the ability of control participants and participants with stroke to dual-task during ADLs, indicated by the engagement of two objects simultaneously. We found that DOP initiation was reduced when the nondominant side or paretic UE was used, which may point to a strategy to ensure successful task performance. Because DOPs are noncued, volitional, and executed during ADLs, they could help assess how dual-tasking is naturally integrated into task performance in a real-world context.
Footnotes
Acknowledgments
The study was supported by American Heart Association Grant 19AMTG35210398 (awarded to Avinash R. Parnandi), National Library of Medicine Grant R01-LM-013316 (awarded to Heidi M. Schambra), and National Institute of Neurological Disorders and Stroke Grant K02-NS-104207 (awarded to Heidi M. Schambra). We thank the following people for their assistance coding the videos: Candace Cameron, Nungari Gachoka, Sirajul Islam, Elissa Kim, Nichole Amalia Korniyenko, Sanya Rastogi, Ronak Trivedi, Adisa Velovic, and Vivian Zhang.