LAUSR

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. 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.