Motor dexterity and strength depend upon integrity of the attention-control system

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Motor dexterity and strength depend upon integrity of the attention-control system

 Authors

1. Paul Rinne^a,¹,
2. Mursyida Hassan^a,^b,¹,
3. Cristina Fernandes^a,
4. Erika Han^a,
5. Emma Hennessy^a,
6. Adam Waldman^a,
7. Pankaj Sharma^c,
8. David Soto^d,^e,
9. Robert Leech^a,
10. Paresh A. Malhotra^a, and
11. Paul Bentley^a,²

1. ^aDivision of Brain Sciences, Charing Cross Hospital Campus, Imperial College London, London, W6 8RF, United Kingdom;
2. ^bSpeech Science Program, School of Rehabilitation Sciences, Faculty of Health Sciences, Universiti Kebangsaan Malaysia, 50300 Kuala Lumpur, Malaysia;
3. ^cSchool of Biological Sciences, Royal Holloway University of London, Egham, Surrey, TW20 0EX, United Kingdom;
4. ^dBasque Center on Cognition, Brain and Language, 20009 Donostia, Spain;
5. ^eIkerbasque, Basque Foundation for Science, 48011 Bilbao, Spain

1. Edited by Peter L. Strick, University of Pittsburgh, Pittsburgh, PA, and approved November 15, 2017 (received for review September 7, 2017)

Significance

Simple voluntary movements (e.g., reaching or gripping) deteriorate with distraction, suggesting that the attention-control system—which suppresses distraction—influences motor control. Here, we tested the causal dependency of simple movements on attention control, and its neuroanatomical basis, in healthy elderly and patients with focal brain lesions. Not only did we find that attention control correlates with motor performance, correcting for lesion size, fatigue, etc., but we found a revealing pattern of dissociations: Severe motor impairment could occur with normal attention control whereas impaired attention control never occurred with disproportionately milder motor impairment—suggesting that attention control is required for normal motor performance. One implication is that a component of stroke paralysis arises from poor attentional control, which could itself be a therapeutic target.

 

Next Section

Abstract

Attention control (or executive control) is a higher cognitive function involved in response selection and inhibition, through close interactions with the motor system. Here, we tested whether influences of attention control are also seen on lower level motor functions of dexterity and strength—by examining relationships between attention control and motor performance in healthy-aged and hemiparetic-stroke subjects (n = 93 and 167, respectively). Subjects undertook simple-tracking, precision-hold, and maximum force-generation tasks, with each hand. Performance across all tasks correlated strongly with attention control (measured as distractor resistance), independently of factors such as baseline performance, hand use, lesion size, mood, fatigue, or whether distraction was tested during motor or nonmotor cognitive tasks. Critically, asymmetric dissociations occurred in all tasks, in that severe motor impairment coexisted with normal (or impaired) attention control whereas normal motor performance was never associated with impaired attention control (below a task-dependent threshold). This implies that dexterity and force generation require intact attention control. Subsequently, we examined how motor and attention-control performance mapped to lesion location and cerebral functional connectivity. One component of motor performance (common to both arms), as well as attention control, correlated with the anatomical and functional integrity of a cingulo-opercular “salience” network. Independently of this, motor performance difference between arms correlated negatively with the integrity of the primary sensorimotor network and corticospinal tract. These results suggest that the salience network, and its attention-control function, are necessary for virtually all volitional motor acts while its damage contributes significantly to the cardinal motor deficits of stroke.

• motor
• attention
• cognitive control
• stroke
• fMRI

Stroke is one of the commonest causes of adult disability, resulting in impairments of both physical (e.g., hemiparesis) and cognitive (e.g., aphasia and neglect) function (1). These two broad types of impairment are commonly regarded as having distinct neuroanatomical bases, entailing different therapeutic strategies, whereas, in fact, physical and cognitive functions may share mechanisms, and their measures interdepend. A well-known example of this is motor neglect (2), in which unilateral motor dysfunction arises from a lateralized attentional bias, rather than because of primary motor, or corticospinal tract, disruption. However, focal brain lesions also impair nonspatial forms of attention, such as alertness (1), that are associated with motor function (3, 4) although the nature of this relationship is unclear.

Associations could occur because lesions tend to overlap anatomically adjacent, yet functionally independent, motor and attention pathways (5) or because of general illness effects on mood or fatigue. Alternatively, motor disability or fatigue demands extra attentional resources, which may secondarily impair performance on tests of attention (6, 7). In the current study, we sought to distinguish these possibilities from the third reason for an association: That nonspatial attentional deficits are a cause of motor impairment.

The type of attention focused on here is attention control (also termed “executive control” or “cognitive control”), which refers to the ability to maintain performance as challenges increase, be they competitive choices or distraction (8, 9). It is an everyday observation that distraction worsens motor performance (e.g., on strength (10) or tracking (11) tasks), indicating that the motor system competes for finite attentional resources. Increasing evidence suggests that a distinct control system manages such resource allocation and is recruited during motor acts, even in the absence of experimental challenges, because purposeful movements entail inhibition of irrelevant or competing motor plans (12, 13), distractor suppression (14), rule following (15), error monitoring, and correction (16). In keeping with this, functional–anatomical associations have been found between basic motor functions (e.g., strength and dexterity) and cerebral regions involved in attention control, particularly cingulate, inferior frontal, and temporoparietal cortices (17, 18), that become more apparent with aging or brain injury (19⇓⇓–22). Such findings extend studies showing that higher motor functions (e.g., drawing, speech, object use, and walking) commonly engage executive systems (23⇓⇓–26). However, while imaging studies suggest anatomical overlap of motor with attention-control functions, they have not to date shown whether attention control is a requisite for basic motor functions—as is the objective here.

Given evidence for motor and attention-control interactions, and noting that stroke-induced impairments in these two functions are associated behaviorally (3, 4), and anatomically (5), we hypothesized that one component of stroke hemiparesis arises from damage to a domain-general, attention-control system, thereby implying that normal motor performance requires intact attention control. To test this, we observed the pattern of dissociations between motor and attention-control performance in a large cohort of hemiparetic stroke patients that, by random distribution, should include lesions with variable differential overlap of motor versus attention-control systems. We reasoned that, if attention control is necessary for motor function, then attention-control impairments would always be associated with motor deficits that are proportionate or worse (i.e., we would not find dissociations where severe attentional impairment coexists with relatively mild motor impairment). Conversely, if poor motor performance increases distractibility (6, 7), then severe motor impairment would always be associated with impaired attention control (i.e., we would not find dissociations of severe motor impairment and preserved attention control). A third possibility—that associations occur because of anatomical proximity, but not functional interaction, between attention-control and motor systems (5)—allows for both types of dissociation because, by chance, some lesions are likely to target either system solely or preferentially. To increase the likelihood of discovering such dissociations, we focused on subjects with mild-moderate deficits who had small lesions that are likely to result in variable relative overlap of two adjacent networks and without confounding cognitive deficits: e.g., gross executive impairments, neglect, or apraxia.

In the following experiments we (i) characterize motor performance in healthy subjects and hemiparetic stroke patients in terms of separable bilateral and unilateral components; (ii) show how these motor components relate to distractibility during motor and nonmotor cognitive tasks, correcting for lesion size and other potential confounds; (iii) characterize the profile of motor/attention-control dissociations; and (iv) ascertain how the two motor components and attention control relate to lesion overlap and functional connectivity, of a putative attention-control (“salience”) network (9), as opposed to other cognitive or motor networks.