Sex-related differences in visuomotor skill recovery following concussion in working-aged adults

Abstract

Background: The ability to perform visually-guided motor tasks requires the transformation of visual information into programmed motor outputs. When the guiding visual information does not align spatially with the motor output, the brain processes rules to integrate somatosensory information into an appropriate motor response. Performance on such rule-based, "cognitive-motor integration" tasks is affected in concussion. Here, we investigate the relationship between visuomotor skill performance, concussion history, and sex during the course of a post-concussion management program.

Methods: Fifteen acutely concussed working-aged adults, 11 adults with a history of concussion, and 17 healthy controls all completed a recovery program over the course of 4 weeks. Prior to, mid-way, and following the program, all participants were tested on their visuomotor skills.

Results: We observed an overall change in visuomotor behaviour in all groups, as participants completed the tasks faster and more accurately. Specifically, we observed significant visuomotor skill improvement between the first and final sessions in participants with a concussion history compared to no-concussion-history controls. Notably, we observed a stronger recovery of these skills in females.

Conclusions: Our findings indicate that (1) concussion impairs visuomotor skill performance, (2) the performance of complex, rule-based tasks showed improvement over the course of a recovery program, and (3) stronger recovery in females suggests sex-related differences in the brain networks controlling skilled performance, and the effect of injury on these networks.

Keywords: Concussion; Eye-hand coordination; Human; Motor control; Psychophysics; Recovery; Sex differences.

Fig. 1

Research procedure flow diagram

Fig. 2

Illustration of the cognitive-motor integration task. The green circle denotes the central home target in which all movements begin. A red target appears in one of 4 peripheral direction (top, bottom, left, or right of centre) after 2000 ms which serves as the ‘Go’ cue. A The standard (ST) condition, in which eye and arm movements are congruent (moved to the same peripheral target). B The non-standard cognitive-motor integration (CMI) condition, in which vision and movement are decoupled to a plane dissociation (eyes look at the vertical screen while hand moves along the horizontal screen), and visual feedback reversal (cursor movement 180° rotated from hand motion)

Fig. 3

Examples of typical full hand movement trajectories for both healthy (left) and concussed (right) individuals, at start (top) and end (bottom) of the program. Trajectories begin at the central target (red dots) and move towards one of four peripheral targets, where each green line represents a single movement trajectory. Blue ellipses denote the 95% C.I. for the final end point of the finger movements (blue dots). Correct trials (green lines) are shown. Any target with less than 5 trajectories indicates error trials (not shown). Ballistic measures are taken from initial slowing point (“ballistic movement point”, < 10% peak velocity)

Fig. 4

A Percent of trials in the CMI condition resulting in direction reversals, by session and group. The percent of direction reversals is significantly greater between the concussion group and the healthy and history groups during session 1. Following the program time, the concussion group experiences a significant improvement. B Difference in Movement Time in the CMI and Standard Condition, by session and group. The difference is significantly greater between the concussion group and the healthy and history groups during session 1 (delta MT). Following the program time, the concussion group experiences a significant improvement. *p < 0.05

Fig. 5

A Unstandardized predicted improvement in reaction time over a concussion recovery program in the CMI condition, as a function of number of concussions. Participants with a history of 2 concussions improved their reaction times significantly more than healthy controls. B Unstandardized predicted improvements in ballistic and C full movement time over a concussion recovery program in the CMI condition, as a function of sex. Females improved their full and ballistic movement times significantly more than males. D Unstandardized predicted improvement in peak velocity over a concussion recovery program in the Standard condition, as a function of number of concussions. Participants with a history of 2 concussions improved their peak velocities significantly more than healthy controls. *p < 0.05

Fig. 6

A Initial relationship between the % of trials in the CMI condition resulting in a direction reversal and the number of SCAT symptoms. B Initial relationship between the % of trials in the CMI condition resulting in a direction reversal and the SCAT symptom severity score. Following the program, there was no longer a relationship between the number of concussion symptoms or severity and CMI performance