Background
Moving and interacting in the world requires rapid processing of the visual environment to identify potential motor goals, select a movement and finally move in a timely manner. For example, when packing groceries, we must decide where to put items based on their shape, size, fragility and other features. The selection, planning and execution of motor actions must be done rapidly to keep pace with the flow of groceries from the cashier.
There is growing evidence that sensory feedback is rapidly integrated into motor decisions [
1‐
3]. Sensory feedback is integrated with higher-level behavioural goals to make rapid decisions on how to move and interact in the environment. Selective attention refines spatial representations of the environment into potential movement targets [
1,
4]. The choice between these internal representations is then based on ‘decisional factors’ [
1]. One such factor is the recognition of combinations of visual features and their behavioural relevance [
1,
5,
6]. Thus, the sensorimotor system rapidly integrates information on the environment to guide motor decisions.
Another important aspect of voluntary motor control is the ability to inhibit a motor action [
7]. When instructed, it is very automatic to simply reach towards spatial targets as they appear in the workspace [
8]. In contrast, it can be hard to avoid reaching towards a target when instructed to move in the opposite direction. In this anti-reach condition, subjects can make erroneous initial motor responses to the spatial goal and are delayed in moving in the opposite direction. This task requires the voluntary override of an automatic response to reach towards the target and involves many brain areas including frontal and parietal cortex [
7,
9‐
12]. This ability can be impaired in persons with stroke [
12], mild cognitive impairment [
13], Alzheimer’s Disease [
14], and a history of concussion [
15], Thus, successful voluntary motor control involves processing sensory feedback not only to select motor actions but also to avoid making others.
Post-stroke disability stems from a variety of motor, sensory, and/or cognitive deficits [
16]. The ability to pack groceries described above highlights that impairments in these functional tasks may reflect not only motor impairments but also cognitive impairments. When driving, one must quickly decide on actions to apply pressure to the brake or accelerator pedals, or turn the wheel based on information from street signs, traffic signals, other traffic, and pedestrians. However, neuropsychological tests or cognitive screening tools generally separate motor and cognitive assessments – the latter often requiring verbal or written responses – and typically do not impose time limits to perform the tasks [
17,
18]. Few neuropsychological assessments focus on rapid motor decisions beyond simple reaction time tests [
18,
19], or timed cognitive tasks such as trail making [
20], even though complex and time sensitive demands are often required for everyday activities.
Furthermore, many standard assessments of post-stroke functioning have problems of subjectivity, coarse ordinal scales, criteria-based scoring, and lack of responsiveness (including floor and ceiling effects) [
21]. Thus, we developed a novel approach of using a robotic assessment to provide objective, continuous measures of performance that are compared to a normative model of healthy control performance.
We recently used an object hit task to quantify simultaneous upper limb bimanual sensorimotor performance [
22]. Although this task quantified rapid motor skills, decisional processes required to perform the task were limited to identifying the trajectory of an object and selecting a limb to hit the object. As all objects were targets in this task, it did not require cognitive processes related to attending to object qualities (rather than just spatial location) to select a motor action nor require inhibiting inappropriate motor responses. These processes can be impaired following stroke [
9,
23,
24].
The goal of the present study was to develop a task that examined rapid motor skills with both arms that also required greater cognitive processing. We developed a variant of the object hit task [
22] by requiring subjects to hit 2 possible targets while avoiding all other objects in the workspace. We hypothesize that individual subjects with stroke will be impaired in enacting or inhibiting a motor response to a potential target based on sensory feedback of the object’s features and their relevance to the ongoing task. The performance of subjects with stroke was compared to a large cohort of non-disabled control subjects.
Clinically, knowledge of impairments in these more complex visuomotor skills can guide novel rehabilitation strategies to regain the ability to rapidly process sensory information for motor actions. As well, it may help to identify if individuals should return to more complex daily activities such as driving.
Discussion
The current study quantified impairments in stroke survivors to rapidly hit certain objects (targets) while avoiding all other objects (distractors). Up to 78 % of subjects with stroke had impairments in individual global, spatial, temporal, or hand-specific task parameters. The task instructions were simple, minimizing the impact of comorbid language impairment [
39]. The task was completed in ~3 min yet provided a wide range of information related to sensorimotor and cognitive function. Most parameters had high inter-rater reliability providing an objective approach to measure impairments and track recovery.
The object hit and avoid task is a variant of an object hit task in which subjects had to rapidly locate and hit all objects moving in the workspace [
22]. The present task extended this approach by requiring the subject to select amongst many options when moving and interacting in the environment. Total objects hit quantified each subject’s ability to make rapid motor actions, regardless of whether they hit the correct objects or not. Subjects with stroke almost always hit fewer objects with their more affected side, and this arm’s performance was more correlated with FIM scores than the unaffected side. Thus, the reduction and asymmetry of the ability to make rapid motor actions is quantitatively measured by the object hit and avoid task, and may have importance in the ability to complete activities of daily living.
We used a large number of parameters to quantify a broad range of sensory, motor and cognitive functions necessary to perform this task. For healthy subjects, some of these measures were highly correlated, but nevertheless captured different functions. For instance, the correlation between target hits and object hits was very strong for controls (r = 0.81). The reason why both parameters were measured rather than choosing only one was because it was important to differentiate between the ability to make fast and accurate movements, and the ability to make correct motor decisions om whether an object was a correct reach target or not. Thus, these metrics represent different domains of performance. Furthermore, subjects with stroke do not necessarily follow this typical pattern of performance. As shown in Fig.
2d, some subjects with stroke hit a high proportion of distractors and others do not, showing the value of each parameter to identify different impairments that do not necessarily co-occur in some individuals with stroke.
The inclusion of both target and distractor objects in the current task added an additional cognitive load to the previous object hit task. This is important as many different cognitive processes are necessary to perform daily activities, and their impairment after stroke is a significant cause of disability [
40]. The present object hit and avoid task focused on a few key processes.
First, demands on the attentional system are high in a visual search task, as it requires differentiating target and distractor stimuli [
41]. Rapid parallel processing of the entire visual workspace can be employed to find a target amongst many distractors with minimal effort if the target has a unique feature separate from distractors that makes it ‘pop out’. In contrast, focused attention is required to serially analyze each stimulus if the target can only be differentiated from the distractors by a conjunction of features. The greater attentional demands required for a conjunction versus a feature visual search task results in greater reaction time for both controls and subjects with stroke who do not have visuospatial neglect [
23]. Subjects with visuospatial neglect also show significantly increased times to detect targets in a conjunction search task (regardless of which side of the workspace was tested), when compared to the performance of controls and subjects with stroke. The object hit and avoid task is representative of a conjunctive visual search as targets could only be differentiated from distractors by attending to the geometry (circular, three- or four-sided) and relative dimensions (tall, wide or equal) of each object (see Methods-
Behavioural Task). Correspondingly, BIT scores correlated with many individual task parameters, as well as the total number of parameters impaired. Although correlations were weak to moderate, all were in the expected direction: greater task impairment associated with greater clinical impairment.
In the current study, participants are required to either enact a reach toward the target, or actively avoid hitting a distractor. Despite visual feedback, haptic feedback, and initial reminders on the need to hit only two types of objects and avoid the rest, over half of the subjects with stroke hit a greater proportion of distractors than 95 % of controls. Subjects with stroke were twice as likely to be impaired in this parameter if they also had neglect.
The ability to inhibit a motor action is an important cognitive function of voluntary motor behaviour [
7]. Motor decisional processes mediate the initiation of an automatic motor response to a new stimulus with the voluntary response required by the task [
42]. This ability to inhibit stimulus-driven and enact task-driven motor responses can be measured by eye movements in the anti-saccade task [
43] and arm movements in an anti-pointing task [
8]. In both tasks, subjects must inhibit a movement to the appearance of a visual stimulus and move to the equal and opposite location. Subjects with stroke having damage to frontal lobes have been shown to make erroneous saccades towards a stimulus in an anti-saccade task [
9]. Subjects with stroke and visual neglect show greater endpoint errors and longer reaction times in an anti-pointing condition (on both sides of space) than controls or subjects with stroke who do not have visuospatial nelgect [
24]. Distractor proportion in the current study correlated with BIT scores just as anti-pointing impairments correlated with the severity of neglect.
The assessment of rapid visuomotor skills post-stroke has potentially useful applications when rehabilitation goals are to regain high function. The object hit and avoid task may be very predictive of the ability to drive, return to work, or maintain complete independence as these skills require the ability to make many rapid motor decisions daily. We show that impairments in these skills are not always captured by currently used pen and paper cognitive screening tools such as the MoCA. Also, since this task relies on many domains of function to be successful, it may be a good indicator of overall stroke recovery.
The measurement of cognitive function after stroke, as measured by the MoCA, correlated moderately with distractor proportion, but only modestly with the number of distractor hits. As well distractor proportion also identified more subjects as impaired as compared to distractor hits. These differences reflect the fact that some control subjects hit a substantive number of distractors, but they also hit many targets. This is why we measured distractor proportion which quantified the ratio between distractors hit and total objects hit.
This task is also part of a larger research program to design a battery of robotic assessment tasks to create a quantitative diagnostic assessment of sensory, motor, and cognitive impairments post-stroke [
21]. The use of a robotic assessment provides objective, continuous measures of performance that are responsive to small changes and compared to a normative model of healthy control performance. This overcomes issues of subjectivity, coarse ordinal scales, criteria-based scoring, and lack of responsiveness (including floor and ceiling effects) seen in many standard assessments of post-stroke functioning. We have also developed assessments of visually-guided reaching [
44], bimanual control [
30], limb position sense [
26], kinesthesia [
45], and limb afferent feedback for action [
46]. The goal is that information from this assessment battery may be used collectively to provide more precise and responsive tools to guide individualized rehabilitation care.
Successful performance in the current task requires many sensorimotor and cognitive skills, thus failure can reflect many potential impairments in sensory, motor and cognitive functions. In order to identify unique impairments in individual participants, it is important to consider the type of parameters that show poor performance. For example, subjects who have impairments in the number objects hit, but not distractor proportion, may have underlying sensorimotor impairments, but no cognitive impairments. These subjects may be better candidates for sensorimotor rather than more cognitive-related rehabilitation. Future work is required to identify whether these patterns of impairment can predict the best type of rehabilitation for each individual.
Acknowledgements
The authors would like to thanks S Appaqaq, H Bretzke, MJ Demers, M Metzler, K Moore, J Peterson, M Piitz, and J Yajure for their help with data collection, patient recruitment, and technical support.