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Abstract

Background

Concussion represents a growing concern in sports participation for adults and youth alike. Studies exploring the neurocognitive sequelae of concussion, such as speed of processing typically compare mean reaction time scores to a control group. Intraindividual variability measures the consistency of reaction times between trials and has been previously explored in adults post-concussion. Some adult studies show increased variability following injury. Developmentally youth show higher intraindividual variability than adults, which may put them at higher risk of increased intraindividual variability change post-concussion. Exploring intraindividual variability may provide additional insight into fluctuating performance reported following injury. Despite preliminary findings of slowed reaction time in youth, a pre-/post-concussion comparison of intraindividual variability of reaction time has not been explored.

Objective

To describe and compare pre- and post-concussion measures of processing speed and intraindividual variability in youth.

Methods

A pre-/post-concussion design was used to compare mean reaction time and the coefficient of variation before and after sports-related concussion in 18 youth athletes aged 10–14 years using verbal and nonverbal working memory tasks. Pre-/post-concussion reaction time and coefficient of variation were compared using t-tests.

Results

The coefficient of variation for nonverbal working memory was significantly higher following concussion, but no changes in average reaction time were found.

Conclusions

Preliminary findings suggest that average response times are unchanged following concussion, but the fluctuation across response times is more variable during a nonverbal working memory task in youth. Increased variability in speed of reaction times could have implications for safe return to sports and reduced academic performance.

Keywords

Concussion children cognition intraindividual variability processing speed working memory sports-related concussion hockey adolescent

Introduction

Sports-related concussion represents a growing concern in youth and it has been found to account for almost 9% of high school sport-related injuries.¹ A common finding following concussion in youth is slowed reaction time (RT),^2–7 which can affect many activities of daily living such as return to school and sports.^8–10

Slowed RT has been demonstrated in youth,^4,5,11 and university-aged athletes post-concussion.^2,3,6 RT slowing has been demonstrated in simple RT tasks^5,11 as well as throughout attentional or executive functioning tasks.^2–4,6 A study by Ellemberg et al.³ found that a group following concussion only had slowed RT for a complex task requiring decision making, with simple RT being unchanged. Previous studies have reported slowed RT on the Immediate Post-concussion Assessment and Cognitive Testing (ImPACT) tool, a computerized assessment that explores symptoms and cognitive performance following concussion in youth.^5,11–13 Although a recent pre-/posttest study by Kriz et al.¹² showed evidence that slowing of RT on the ImPACT may be due to a learning strategy employed by participants who took the test multiple times. To the authors’ knowledge, no studies have specifically reported pre-/post-concussion processing speed change in working memory (WM) tasks, despite changes in WM performance being found.^14–16 Yet, a recent study of youth post-mild traumatic brain injury (TBI) reported nonsignificant differences in RT during a WM task.¹⁵ The study by Keightley et al.¹⁵ compared the injury group to a control group to infer the potential for individual-level change following injury. While group comparison is often more efficient in terms of data collection (many baseline tests do not have to be completed among groups with high risk of injury) it does not reflect individual change like a pre-/post-injury study. Youth studies are further complicated by the inherent performance change occurring with development.^17,18 The fluctuations of performance within typically developing youth make group comparisons even less reliable at estimating change in performance following injury. Thus, when exploring processing speed following concussion, a pre-/post-injury design is necessary to accurately describe injury-related change.

Average RT is the most common measurement of speed of information processing, providing an overall summary of how quickly an individual processed information during a task. Processing speed has also been measured in terms of intraindividual variability (IIV), which examines the consistency of RT across trials within one task, across multiple administrations of the same task, or across multiple test administrations (e.g. during a neuropsychological battery). Given reports from patients of fluctuating performance during activities following concussion, inclusion of IIV measures may provide additional insight into how processing speed is impacted after injury.^19,20 IIV is considered a marker of neurological stability¹⁹ and preliminary evidence suggests that consistency in RT may be reflective of cognitive functioning independent of mean performance or average speed.²⁰ Previous work has demonstrated higher IIV after TBI,²¹ including concussion.^22–25 Examining consistency of processing speed may be especially important when considering return to a high-risk environment such as sport. Being able to respond quickly and consistently to incoming stimuli, such as other players or sporting equipment (e.g. pucks/balls, goal posts), could reduce the risk of re-injury.

Post-concussion IIV changes have previously been explored in adults,^22–31 yet no studies were found that explore IIV following concussion in youth. Overall, results from adult studies are mixed; some studies show higher variability in participants following concussion,^22–26 while others report nonsignificant differences.^27–30 As expected, there are many differences between the studies; including study design and time of testing post-concussion, which may impact the ability to detect differences after injury.

The majority of existing post-concussion IIV studies utilized group comparisons of concussed versus matched-control participants.^{22,23,25,26,28,31} While efforts were made to match individuals, comparing different groups does not allow for a true comparison of differences in individual variability. Additionally, some studies included a considerable range of time between testing and injury. This range between testing time could impact the ability to detect injury-related change in a diagnosis such as concussion, which is characterized by a short-recovery time. For example, Rabinowitz and Arnett²⁹ found no changes in IIV post-concussion using a computerized battery designed for adults and additional paper and pencil tests. Athletes were to be tested within one-week post-concussion, but ranged from 0 to 210 days post-concussion. Previous research has demonstrated the majority of adult athletes exhibit cognitive recovery within 10–14 days following concussion.^9,32,33 The differences between athletes immediately post-concussion and those months later may have contributed to the absence of IIV differences. This is further supported by an early study that found significantly increased IIV on a four-choice RT test only at 48 h post-concussion, with no differences at later time points (six weeks and six months) between injury and control groups.²³

This study proposes a first step to address the gaps in the literature by comparing pre- and post-concussion processing speed via mean RT and IIV in youth aged 10–14 years during a WM task. The WM task includes a verbal and nonverbal version, and has previously been used in the concussion literature exploring RT in both adults³⁴ and youth.¹⁵ Both studies compared a post-concussion and control group and found no differences between mean RT in adults³⁴ or youth.¹⁵ Similar to the Rabinowitz and Arnett²⁹ study discussed above, neither study utilized a solely acute or chronic population, but ranged in time since injury from 1 to 14 months for adults³⁴ and 9 to 90 days for youth.¹⁵ In contrast, the current study utilizes a pre-/post-concussion design to explore change in mean RT and IIV in youth during the subacute post-concussion state. The objectives of this study are to describe and compare (1) mean RT and (2) IIV pre- and subacutely post-concussion in a youth population during a WM task. Despite no change in RT during the same task from youth with mild TBI in the study by Keightley et al.,¹⁵ mean RT is expected to be slower post-concussion based on previous findings of increased RT in youth following concussion^4,5,11 given the participants are tested during the subacute post-concussion state. IIV is expected to increase post-concussion based on previous findings in adults.^22–25

Methods

Participants

Participants in this study were part of a three-year longitudinal study exploring the effects of concussion in minor hockey players. The larger study included 187 athletes (aged 8–14 years, 125 males:62 females) with 27 youth sustaining a concussion during the three years of the study. Twenty-one of the 27 completed WM tasks prior to their concussion. Current guidelines suggest that spontaneous recovery from a concussive event occurs within four weeks in youth.^7,33 But given previous research that found typical spontaneous recovery from concussion in youth within 10 days,^5,9,21 only youth tested within 10 days following injury were included in the sample (18 of 21 athletes) to ensure youth were captured within the subacute post-concussion stage. The study sample consisted of 18 youth, aged 10–14 years old (15 males) with pre-/post-concussion data. Inclusion criteria required that participants provide informed, written consent (from the parent) and verbal and/written assent (from the youth), be a native speaker of English, and have normal or corrected-to-normal vision and hearing. Exclusion criteria included a psychological, neurological, or learning disability diagnosis (except for a previous history of concussion). For this study, concussion was defined using the Consensus in Sport Group definition: “a traumatic brain injury induced by biomechanical forces…typically results in the rapid-onset and short-lived impairment of neurological function….”³³ A diagnosis of concussion was confirmed by a physician following report of a concussive event from the parent/guardian of the participant. The physician was either the family physician, a physician at a walk-in clinic, or pediatrician confirming a medical diagnosis following clinical examination. The examination was not consistent between practitioners. Ethics approval was granted for the study from the University of Toronto Research Ethics Board and the Sunnybrook Health Sciences Center Research Ethics Board.

Procedure

Recruitment was completed through a general information letter distributed to team personnel from local hockey leagues. Participants completed the verbal and nonverbal WM task yearly as close as possible to the onset of the hockey season. The WM task was re-tested acutely post-concussion, and within 72 h of concussion when possible. Trained lab personnel administered all testing in a distraction-free environment on a laptop computer with an external mouse. The experiment was run using Visual Basic 2.0^©. Participants were given task instructions and provided practice time for both the verbal and nonverbal task before testing until 80% accuracy was achieved. Athletes were monitored for symptoms using the Post-Concussion Symptom Scale – Revised (PCS-R) daily for seven days and then weekly until symptoms reduced to baseline, or when PCS-R was less than or equal to seven (see PCS-R subsection). The PCS-R was also completed before the WM task if testing fell outside of the regular PCS-R administration schedule. The first few PCS-R scores were completed over the telephone with the participant and lab personnel until they understood how to use the measure. Any remaining PCS-R scores were submitted by email to lab personnel.

WM task

The WM task used was an experimental task developed by Petrides et al.^35,36 and has previously been used with adults and youth post-concussion.^15,34 There were two task types, one verbal and one nonverbal. The verbal task used six-letter abstract words. The nonverbal task used abstract color images. During either the verbal or nonverbal WM task, four different abstract stimuli were presented, followed by a delay. After the delay, a single stimulus was shown, and participants made a response using the external mouse. The participant responded if the final stimulus was or was not shown in the four stimuli presented before the delay. Only five possible stimuli existed and were randomly repeated throughout the task. Each of the four stimuli prior to delay was 1 s in duration. The delay between the four stimuli and the single response stimulus was 1.5 s. Each task included 24 WM trials. For further task description and images of task stimuli, see Keightley et al.¹⁵

PCS-R

The PCS-R^37,38 was used to monitor self-reported symptoms following concussion in youth and is used here to further describe the sample used in this study . The PCS-R contains 21 symptoms commonly experienced following concussion including physical, cognitive, emotional, and sleep-related items. At time of testing, participants self-rated their experience of each symptom using a scale from 0 to 6. A score of 0 indicates that the participant is not currently experiencing that symptom. Many of the 21 symptoms described in the PCS-R can be experienced in everyday life (such as fatigue or headache) and thus a score of greater than 0 can occur without a concussion.³⁷ An overall score of greater than or equal to 8 on the PCS-R is indicative of persistent or ongoing symptoms following concussion. The PCS-R has demonstrated high internal consistency reliability for both high school and collegiate athletes, with no found differences between age groups.³⁷

Processing speed measures

The following measures were used to describe processing speed: (1) mean RT (ms) and (2) coefficient of variation (CV). RT and CV were calculated using correct trials. The CV was calculated by $\frac{standard deviation of reaction times}{mean reaction time}$ . The CV was selected to measure IIV in this study because it provides a more robust measure of variance than intraindividual standard deviation.³⁹

Data analysis

Participant and injury characteristics were described. A Shapiro–Wilk test of normality was completed, and verbal CV variables scores lacked a normal distribution (p < 0.05). A change score was calculated for processing speed measures by subtracting the post-concussion score from pre-concussion score. Descriptive statistics (mean, standard deviation, and range) were calculated for pre- and post-concussion variables and change scores (geometric mean and standard deviation were reported for CV values, see below). Pre- and post-concussion mean RT scores were compared using t-tests. CV variables were transformed using a log transformation, which passed normality testing (p > 0.05). Pre- and post-concussion comparisons of CV scores were completed using a t-test of the log-transformed values. With two comparisons made for primary and secondary objectives, a Bonferroni correction for multiple comparisons was applied and the alpha level was adjusted to 0.025. Cohen’s d was calculated following t-test using (t/√n). Effect size was determined using Cohen’s table of effect size indicating d ≤ 0.20 is trivial, ≥0.20 is small, ≥0.50 is medium, and >0.80 is a large effect size.⁴⁰ Spearman’s rank correlations were also calculated for processing change scores (RT and CV) with (1) age at post-concussion and (2) elapsed time between pre- and post-concussion time points to explore relationships that could impact t-test findings. Additionally, Spearman’s rank correlations were completed to determine the relationship between age at pre-concussion and pre-concussion processing scores to compare trends expected in typical development compared to change scores seen in pre-/post-concussion analyses described above. All analyses were performed using SPSS version 22.0^©. A statistician was consulted to ensure the best approach to data analysis was used to examine the study objectives.

Results

Demographic and injury characteristics

Participants ranged from 10 to 14 years of age at pre- and post-concussion, and 15 of 18 were male (83%). Average time from concussion to post-concussion testing was 3.2 ± 2.0 days and ranged from one to nine days. Time between pre- and post-concussion averaged 109.9 ± 101 days and ranged from 4 to 365 days. PCS-R scores averaged 3.6 ± 3.1 at pre-concussion and 17.4 ± 22.8 at post-concussion. All participants played on a representative or recreational minor hockey team at varying levels of play (house league-AAA). All athletes were injured during sport play; 17 were injured during sports including hockey, lacrosse, and soccer and one was injured during gym class. Three participants reported a history of one concussion prior to the current injury but reported not being symptomatic prior to the current injury. The timeframe reported for the previous concussion was limited, often only including the year of injury (ranging 1–3 years before the concussions reported in the current study). The dataset was analyzed without participants who had a history of concussion to examine the impact on overall findings. All findings were unchanged, so all data points were included in the analyses. Overall demographic and injury details are reported in Table 1.

Table 1.

Descriptive findings including demographic and injury characteristics.

	Age pre-concussion mean (SD) range	Age post-concussion mean (SD) range	Pre-to-post interval^a mean (SD) range	PCS-R post-concussion mean (SD) range	No. of participants
	Age pre-concussion mean (SD) range	Age post-concussion mean (SD) range	Pre-to-post interval^a mean (SD) range	PCS-R post-concussion mean (SD) range	n	One previous concussion	Reported injury during sport play
All participants	11.4 (0.9) 10.2–13.7	11.7 (1.1) 10.3–14.7	109.9 (101.0)	17.4 (22.8) 0–89	18	3	17^b

SD: standard deviation.

^aPre-to-post-concussion interval measured in days.

^bParticipant injured outside of sport play was injured during gym class (a sport environment).

Change in RT following concussion

Descriptive (mean, standard deviation, and range), t-score, p-value, confidence intervals, and associated effect sizes for average RT during the WM task can be found in Table 2. A positive change score indicates a lower score (faster RT) post-concussion and a negative change score indicates a higher score (slower RT) post-concussion. Following Bonferroni correction, no findings were statistically significant (p > 0.025).

Table 2.

Pre- and post-concussion descriptive and t-test findings for reaction time during verbal and nonworking memory tasks.

	Pre-concussion^a	Post-concussion	Change^b	t-test^c
	Mean (SD)	Mean (SD)	Mean (SD)	t-statistic	p-value	Cohen’s d	Effect size
	Range	Range	(95% CI)
Verbal	1257 (206)	1374 (220)	−117 (224)	−2.21	0.041	−0.45	Small
	772–1675	896–1687	(−228, −5)
Nonverbal	1230 (175)	1284 (262)	−54 (290)	−0.789	0.441	−0.17	Small
	937–1536	672–1890	(−198, 90)

SD: standard deviation.

^aReaction time reported in milliseconds. No significant findings (corrected p > 0.025).

^bChange score represents pre-concussion − post-concussion RT score.

^ct-statistc 17 degrees of freedom.

Change in IIV following concussion

Descriptive (mean, standard deviation, and range), t-score, p-value, confidence intervals, and associated effect sizes for the CV during the WM task can be found in Table 3. A positive change score indicates a lower score (less variability) post-concussion and a negative change score indicates a higher score (more variability) post-concussion. Following Bonferroni correction, findings showed an increase in nonverbal WM CV following concussion (t (17) = −2.56, p = 0.020).

Table 3.

Pre- and post-concussion descriptive and t-test findings for coefficient of variation.

	Pre-concussion	Post-concussion		t-test^a
	Mean (SD)^b	Mean (SD)	% Change	t	p	d	Effect size
	Range	Range	(95% CI)
Verbal	0.257 (0.10) 0.16–0.57	0.271 (0.13) 0.15–0.73	5.45% increase	−0.28	0.787	−0.176	Trivial
Nonverbal	0.237 (0.07) 0.12–0.43	0.292 (0.09) 0.18–0.48	23.2% increase	−2.56	0.020^c	−0.299	Small

^at-statistic 17 degrees of freedom.

^bGeometric mean, standard deviation (SD), and range reported.

^cSignificant finding (corrected p < 0.025).

Correlations between change in processing speed post-concussion with age and interval between pre- and post-concussion

Spearman’s rank correlation and p-value were calculated for relationships between change in RT and CV processing and (1) age at post-concussion (r ranged from −0.07 to −0.28) and (2) time interval between pre- and post-concussion (number of days) (r ranged from −0.08 to −0.30). No significant findings were found (p > 0.006).

Correlations between pre-concussion age and processing speed

Spearman’s rank correlation, effect size, and p-value are reported in Table 4 for relationships between pre-concussion age and processing variables (mean RT and CV). Two significant findings are reported (p < 0.025) suggesting verbal WM average RT and nonverbal WM CV decrease (faster and less variable) with increasing age in this age group when no concussive event is involved.

Table 4.

Correlation findings between pre-concussion age and pre-concussion processing speed.

	Spearman’s r	p-value
Pre-test RT (ms)
Verbal	−0.55	0.018^a
Nonverbal	−0.28	0.257
Pre-test coefficient of variation
Verbal	−0.03	0.919
Nonverbal	−0.55	0.019^a

^aSignificant findings (corrected p < 0.025).

Discussion

The current study described and compared pre- and post-concussion processing speed in youth using mean RT and IIV. No changes in average RT were found between pre- and post-concussion for the verbal or nonverbal WM tasks. However, the nonverbal WM task showed a significant increase in the CV post-concussion. This suggests that while average RT is not significantly changed, the RTs during the nonverbal WM task are less consistent. Change in CV post-concussion supports our hypothesis that IIV increases following concussion in youth, but the difference in findings between tasks (verbal and nonverbal) were unexpected. We found no relationships between change in processing speed and age post-concussion and change in processing speed and number of days between injury and the post-concussion testing time. Additional findings showed a relationship between pre-concussion findings and pre-concussion age that suggests older youth are more likely to have lower IIV when no concussive event has occurred. This finding suggests that CV reduces with age, which is in opposition to the increase in CV found between pre- and post-concussion. This suggests that the reported changes between pre- and post-concussion are not developmental in nature or influenced by testing effects (testing interval). Further discussion of findings and limitations are included below.

RT findings were in opposition to our hypothesis, which expected overall RT to increase (or slow) following injury. Despite evidence of slowed RT between injury and control groups,^4,5,11 no difference in average RT is consistent with a previous group comparison study using the same task for youth experiencing a more prolonged recovery (9–90 days post-concussion)¹⁵ and another study exploring RT using a non-WM task post-concussion.³

Higher IIV in youth post-concussion was found for the nonverbal WM condition. We had hypothesized that higher IIV would be found for both WM tasks based on previous reports of higher CV acutely post-concussion in adults,²³ but did not find this. A previous study comparing WM performance with different stimuli across the lifespan found that performance with shapes (nonspatial visual) developed earlier than letters or numbers,⁴¹ and another study has shown that RT becomes faster within typical development, before reduction in IIV.⁴² Thus, if visual WM processing is more established in 10–14 year olds, average RT may not slow as youth may be more able to compensate for injury. Yet, the inconsistency within RTs may show greater fluctuations after concussion. A lack of change in verbal WM RT and CV was unexpected provided the above developmental literature which suggests competence with verbal stimuli is less established.⁴¹ More research is needed to directly compare average RT and IIV between different types of stimuli given the differences between tasks captured here.

Limitations

There were overall limitations in power to detect change due to a small sample and the multiple comparisons made. The sample size was 18 participants, which provided limited power to detect change. Especially given the variance seen between RT scores within the group, only the most robust differences⁴³ would be evident upon comparison and may be partly responsible for differences in findings between verbal and nonverbal tasks. Future studies should utilize a larger sample to increase power to detect statistical significance and be specifically designed to answer further research questions. The current work was limited as it included a subset of data from a larger study. Additionally, a control group with similar pre- to post-injury interval to compare to the pre-/post-injury findings of the concussion group would support the changes are due to injury-related sequelae. The WM tasks used were also limited by its experimental nature. Future studies would include tasks with tested validity and reliability to minimize test-related effects.

Conclusion

Overall findings include preliminary evidence of increased IIV in the absence of slowed RT following concussion in youth. Unlike originally hypothesized, findings of increased IIV were not found for bothtask types. This may suggest that differences exist in processing abilities between verbal and nonspatial visual stimuli at pre-concussion, which may impact post-concussion change.

Understanding the nature of processing speed consistency in youth post-concussion is important to understand real-world fluctuations in performance. Large fluctuations in RT could make for functional challenges at school such as test performance or processing information delivered in class, or during sports and other leisure activities. Despite the limitations, the lack of pre-/post-concussion findings in the literature makes this study novel. The uniqueness of this study, coupled with findings of increased IIV, provides rationale for further exploration of these changes in youth following concussion.

Footnotes

Acknowledgements

Many thanks to Nick Reed, Tali Dick, Sabrina Agnihotri, Sam Liu, and Amy Wilkinson for your help with data collection and to Marguerite Ennis for sharing her statistical insight.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the Ontario Neurotrauma Foundation (grant number 483615) and the Canadian Institutes of Health Research (grant number 484706).

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Exploring changes in processing speed and intraindividual variability in youth following sports-related concussion

Abstract

Background

Objective

Methods

Results

Conclusions

Keywords

Introduction

Methods

Participants

Procedure

WM task

PCS-R

Processing speed measures

Data analysis

Results

Demographic and injury characteristics

Change in RT following concussion

Change in IIV following concussion

Correlations between change in processing speed post-concussion with age and interval between pre- and post-concussion

Correlations between pre-concussion age and processing speed

Discussion

Limitations

Conclusion

Footnotes

Acknowledgements

Declaration of conflicting interests

Funding

References