Sensorimotor learning deficits observed in children with sports-related concussion

Introduction

Pediatric concussions have been shown to negatively affect neurocognitive function, including poor attention span, impaired memory and learning difficulties^1–3. However, the association between pediatric concussion and sensorimotor function has not been investigated. Understanding motor learning impairment following sport-related concussion in children may be critical in guiding safe return to play. In this short observational/case study, we investigated the pattern of adaptation to a novel visuomotor condition in three children who suffered a concussion while playing sports, and compared their adaptation patterns to those obtained from three children without a concussion. A research paradigm in which individuals adapt to a novel visuomotor condition during reaching movements has been employed extensively in the neuroscience community to understand the neural processes that underlie motor learning in both adults^4,5 and children^6,7.

We also examined neurocognitive function of both the concussed children and the control children using an assessment technique called the trail making test (TMT). TMT (part B) is a traditional paper assessment that times subjects as they draw lines to connect numbers and letters alternately on a page. TMT is a validated assessment of concussion, and tests cognitive demands that are also important for sports, including psychomotor processing, visual motor/spatial abilities and mental flexibility^8,9.

The purpose of this observational/case study was to determine qualitatively whether concussed children with neurocognitive impairments, as indicated by the TMT scores, would also demonstrate sensorimotor deficits, as indicated by the visuomotor adaptation patterns.

Methods

Three children (15 years old, one male (cc3)), who presented to the Emergency Department at the Children’s Hospital of Wisconsin within 24 hours from the time of injury and who received a diagnosis of concussion (Glasgow Coma Scale ≥ 14), participated in this study. None of the three children had a concussion previously. They visited the Neuromechanics Laboratories at the University of Wisconsin-Milwaukee (UWM) 5~8 days following the concussion. Their symptoms were not assessed on the day they visited UWM, although one of the patients (cc1) was not able to speak or walk normally at that time. Three children (12 (cc1), 14 (cc3) and 17 (cc2) years old, all males), who were recruited from the Milwaukee Metropolitan area, served as controls. Selection criteria for subjects were the same for both patients and controls (except their concussion status), which were: subject was 10–17 years of age, regularly participated in an athletic activity, was English-speaking, was right handed, and had no neurological disease or peripheral disorder affecting movement of the right arm. All subjects were recruited and tested in May 2015.

Upon arrival at UWM, the subjects were first administered with the TMT^8,9. Following that, they participated in the visuomotor adaptation experiment in which they performed rapid reaching movements from a start circle to a target repeatedly under a normal visuomotor condition (baseline) first, then under a novel visuomotor condition (adaptation). The baseline session (40 trials) was provided for the subjects to become familiarized with the general reaching task with unperturbed visual feedback. In the adaptation session (80 trials), the visual display of reaching movements was rotated 30 degrees counterclockwise about the start circle, such that a hand movement made in the “12 o’clock” direction resulted in a cursor movement made in the “11 o’clock” direction. Continuous visual feedback (in the form of a cursor) was provided throughout the movement in both sessions. A robotic exoskeleton called KINARM (BKIN Technologies Ltd, Kingston, ON, Canada) was used to provide the visuomotor rotation during the experiment and also to collect movement data. The 2-D position of arm segments was sampled at 1,000Hz, low-pass filtered at 15Hz, and differentiated to yield resultant velocity values. Data were processed and analyzed using MATLAB (The Mathworks Inc., Natick, MA) and SPSS.

To examine performance accuracy, we calculated direction error (DE), which was the angular difference between a vector from the start circle to the target and another vector from the hand position at movement start to that at peak arm velocity. Using the direction error data, we obtained the following measures for each subject: (1) DE at trial 1 in the adaptation session; (2) the first block of DE (i.e., mean of five consecutive trials) in the adaptation session that is not statistically different from the last block of DE in the baseline session; and (3) the rate of performance change during the adaptation session. To obtain the second measure, a priori pairwise comparisons, using t-tests, were made between DE at block 8 from the baseline session and DE at each of the 16 blocks from the adaptation session (starting from block 1). The alpha level was set at .05. To obtain the third measure, a line of approximation was constructed by fitting a logarithmic regression line to the adaptation data, and the slope value was used.

Results

Figure 1c illustrates neurocognitive data from all subjects, indicated by TMT scores. One concussed child (cc1) showed some cognitive slowing on visit 1, as compared with the controls, while the others did not.

The overall pattern of visuomotor adaptation, illustrated in Figure 1a and b, was somewhat similar between the patients and the controls. In fact, the patients’ baseline performances do not appear to be worse than those of the controls. However, a close examination of the adaptation data revealed the following differences:

Figure 1.

(a) Improvements in performance across trials during baseline and adaptation sessions. Upper panel depicts data from 3 controls, lower panel data from 3 concussed children. (b) Improvements in performance across blocks during the baseline (last block only) and adaptation sessions. Numbers under arrows indicate first block of DE that was not statistically different from last block of DE from the baseline phase. (c) TMT scores for every subject. (d) DE at trial 1 during the adaptation session. (e) First block of DE in the adaptation session that was not different from last block of DE in the baseline session. (f) Rate of performance change in the adaptation session. Vertical boxes in red (c–f) indicate variability within each subject group.

Discussion

TMT is a validated neurocognitive assessment of pediatric concussion^8,9. The average time to complete the TMT part B is 75 seconds in neurologically intact individuals; if the time is longer than 273 seconds, it is considered deficient^10,11. One concussed child who participated in our study completed the TMT part B in 98 seconds; and the other two children completed it in less than 50 seconds. According to the TMT scores, thus, one may conclude that all of the children who had a concussion 5 to 8 days prior to their participation in this study did not seem to have neurocognitive impairments.

The patterns of visuomotor adaptation observed in the patients, however, appear to be somewhat different from those observed in the controls. Specifically, the first block of DE in the adaptation session that was significantly different from the last block of DE of the baseline session occurred later in the patients than in the controls; and the rate of performance change was higher (i.e., slower adaptation) in the patients as well. These data indicate that the patients had more difficulty than the controls while adapting to the novel visuomotor rotation, which points to the possibility of sensorimotor learning deficits in the concussed children.

The present study has several limitations. First, all the children tested in this study were recruited in the Milwaukee Metropolitan area, which raises a possibility that they may not be the best representative of all children of the same age group. Second, we did not collect any information regarding our subjects’ demographic and social statuses, which could be considered as potential confounding characteristics. Third, age and sex were not matched perfectly between the patients and the controls tested in the present study. However, we are not aware of any findings that indicate significant differences between boys and girls within the age range of 12–17 years with regard to their visuomotor adaptation capabilities. In addition, it has been shown that during targeted reaching movements under a visuomotor rotation condition, visuomotor representations of children who were 6 or 8 years old differed from those of adults, although those of 11 year-old children did not¹². Our data do not seem to indicate sex-related differences either, in that the adaptation pattern of cc2 (15 year-old female) was very similar to that of ctls 1 and 3 (12 and 14 year-old males, respectively). Thus, while the potential effects of age- and sex-related differences between the patients and the controls cannot be completely excluded, it seems unlikely that our results were substantially influenced by such effects. Finally, we did not conduct statistical analyses to quantify the differences between the children with concussion and those without concussion, because the statistical results would not be very meaningful given the small sample size. Nevertheless, our data exhibited qualitative differences between the two groups of children that suggest sensorimotor deficits in concussed children. Further investigation is warranted to demonstrate quantitative differences between children with and children without concussion by utilizing a larger sample size.

In conclusion, the results from this study provide preliminary data indicating that children with concussion may have sensorimotor impairments even when they do not seem to have neurocognitive impairments. Given the importance of children’s ability to rapidly adapt to the dynamic environments and task requirements throughout a sport, our findings suggest that examination of sensorimotor function, in addition to that of neurocognitive function, may provide valuable information when determining whether children are ready to return to play sports or not.

Data availability

F1000Research: Dataset 1. Kinematic data from visuomotor adaptation task, 10.5256/f1000research.6575.d48984¹³