Differential neural mechanisms for movement adaptations following neuromuscular training in young female athletes with a history of sports-related concussion.

Sports-related concussion (SRC) in adolescent athletes is associated with an increased risk of subsequent lower extremity injury. Neuromuscular training (NMT) has shown promise for reducing lower extremity injuries following SRC, however, neural adaptations in response to changes in lower extremity biomechanics following NMT in athletes with a history of SRC (HxSRC) remains poorly understood. Therefore, the purpose of this study was to identify changes in neural activity associated with lower extremity movement adaptations following a six-week NMT intervention in athletes with a HxSRC. Thirty-two right-hand/foot-dominant female adolescent athletes (16 with self-reported HxSRC, 16 age- and anthropometrically-matched controls) completed a bilateral leg press task with 3D motion analysis during functional magnetic resonance imaging (fMRI). Movement adaptations were defined as a change in frontal and sagittal plane range of motion (ROM) during the fMRI bilateral leg press task. Significant pre- to post-NMT reductions were observed in the non-dominant (left) mean frontal plane ROM. Whole-brain neural correlate analysis revealed that increased cerebellar activity was significantly associated with reduced mean left-knee frontal ROM for matched controls. Exploratory within group analyses identified neural correlates in the postcentral gyrus for the HxSRC group which was associated with reduced mean left-knee frontal plane ROM. These distinct longitudinal changes provide preliminary evidence of differential neural activity associated with NMT to support knee frontal plane control in athletes with and without a HxSRC.

Associations Between Brain Metabolites Measured With MR Spectroscopy and Head Impacts in High School American Football Athletes.

BACKGROUND: While changes in brain metabolites after injury have been reported, relationships between metabolite changes and head impacts are less characterized. PURPOSE: To investigate alterations in neurochemistry in high school athletes as a function of head impacts, concussion, and the use of a jugular vein compression (JVC) collar. STUDY TYPE: Prospective controlled trial. SUBJECTS: A total of 284 male American football players, divided into JVC collar and noncollar groups; 215 included in final analysis (age = 15.9 ± 1.0 years; 114 in collar group). FIELD STRENGTH/SEQUENCE: 3 Tesla/T1-weighted gradient echo, 1H point resolved spectroscopy, acquired between August and November 2018. ASSESSMENT: Head impacts were quantified using accelerometers. Concussion was diagnosed by medical professionals for each team. Pre- to postseason differences in total N-acetylaspartate (tNAA), total choline (tCho), myo-inositol (myoI), and glutamate + glutamine (Glx), in primary motor cortex (M1) and anterior cingulate cortex (ACC), relative to total creatine (tCr), were determined. STATISTICAL TESTS: Group-wise comparisons were performed using Wilcoxon signed-rank, Friedman's, and Mann-Whitney U tests. Relationships between ∆metabolite/tCr and mean g-force were analyzed using linear regressions accounting for concussion and JVC collar. Significance was set at P ≤ 0.05. RESULTS: In participants without concussion, a significant decrease in tCho/tCr (0.233 ± 1.40 × 10-3 to 0.227 ± 1.47 × 10-7) and increase in Glx/tCr (1.60 ± 8.75 × 10-3 to 1.63 ± 1.08 × 10-2) in ACC were observed pre- to postseason. The relationship between ∆tCho/tCr in M1 and ACC and mean g-force from >80 g to >140 g differed significantly between participants with and without concussion (M1 ß ranged from 3.9 × 10-3 to 2.1 × 10-3; ACC ß ranged from 2.7 × 10-3 to 2.1 × 10-3). Posthoc analyses revealed increased tCho/tCr in M1 was positively associated with mean g-force >100 g (ß = 3.6 × 10-3) and >110 g (ß = 2.9 × 10-3) in participants with concussion. Significant associations between ∆ myoI / tCr $$ \Delta \mathrm{myoI}/\mathrm{tCr} $$ in ACC and mean g-force >110 g (ß = -1.1 × 10-3) and >120 g (ß = -1.1 × 10-3) were observed in the collar group only. DATA CONCLUSION: Diagnosed concussion and the use of a JVC collar result in distinct neurochemical trends after repeated head impacts. LEVEL OF EVIDENCE: 2 TECHNICAL EFFICACY: Stage 3.

Does Neuromuscular Training Reduce the Risk of Lower-Extremity Musculoskeletal Injury in High School Female Athletes With a History of Sport-Related Concussion?

CONTEXT: There is a well-established increased risk of lower-extremity (LE) musculoskeletal (MSK) injury following a sport-related concussion (SRC). Neuromuscular training programs improve biomechanics associated with LE MSK injury and reduce LE MSK injury incidence, but their relative effectiveness in athletes with history of SRC is unknown. The purpose of this study was to evaluate LE MSK injury incidence in female adolescent athletes with history of SRC following a neuromuscular training intervention. DESIGN: Prospective case-control. METHODS: Seventy-seven adolescent female athletes aged 12-18 years who participated in soccer, volleyball, or basketball were recruited from a single institutional sports medicine research and performance center to complete a 6-week neuromuscular training program prior to competitive athletic season. Group (Control, History of SRC) comparisons of athlete exposure and relative LE MSK injury risk and rates during the competitive athletic season were assessed. RESULTS: Ten injuries were recorded by 9 athletes. Female athletes who reported history of SRC had increased injury risk (Risk Ratio 3.9, 95% CI, 1.1-13.8, P = .01) and increased injury rate (rate ratio 4.1, 95% CI, 1.1-15.8, P = .03) compared with female athletes without history of SRC. CONCLUSIONS: Female adolescent athletes with history of SRC showed a greater risk of LE MSK injury compared with athletes with no history of SRC. Future work is still needed to understand the underlying mechanisms associated with future LE MSK injury following SRC and interventions that ameliorate elevated injury risk.

Automated quantitative assessment of bone contusions and overlying articular cartilage following anterior cruciate ligament injury.

Quantitative methods to characterize bone contusions and associated cartilage injury remain limited. We combined standardized voxelwise normalization and 3D mapping to automate bone contusion segmentation post-anterior cruciate ligament (ACL) injury and evaluate anomalies in articular cartilage overlying bone contusions. Forty-five patients (54% female, 26.4 ± 11.8 days post-injury) with an ACL tear underwent 3T magnetic resonance imaging of their involved and uninvolved knees. A novel method for voxelwise normalization and 3D anatomical mapping was used to automate segmentation, labeling, and localization of bone contusions in the involved knee. The same mapping system was used to identify the associated articular cartilage overlying bone lesions. Mean regional T1ρ was extracted from articular cartilage regions in both the involved and uninvolved knees for quantitative paired analysis against ipsilateral cartilage within the same compartment outside of the localized bone contusion. At least one bone contusion lesion was detected in the involved knee within the femur and/or tibia following ACL injury in 42 participants. Elevated T1ρ (p = 0.033) signal were documented within the articular cartilage overlying the bone contusions resulting from ACL injury. In contrast, the same cartilaginous regions deprojected onto the uninvolved knees showed no ipsilateral differences (p = 0.795). Automated bone contusion segmentation using standardized voxelwise normalization and 3D mapping deprojection identified altered cartilage overlying bone contusions in the setting of knee ACL injury.

High magnitude exposure to repetitive head impacts alters female adolescent brain activity for lower extremity motor control.

Contact and collision sport participation among adolescent athletes has raised concerns about the potential negative effects of cumulative repetitive head impacts (RHIs) on brain function. Impairments from RHIs and sports-related concussions (SRC) may propagate into lingering neuromuscular control. However, the neural mechanisms that link RHIs to altered motor control processes remain unknown. The purpose of this study was to isolate changes in neural activity for a lower extremity motor control task associated with the frequency and magnitude of RHI exposure. A cohort of fifteen high school female soccer players participated in a prospective longitudinal study and underwent pre- and post-season functional magnetic resonance imaging (fMRI). During fMRI, athletes completed simultaneous bilateral ankle, knee, and hip flexion/extension movements against resistance (bilateral leg press) to characterize neural activity associated with lower extremity motor control. RHI data were binned into continuous categories between 20 g - 120 g (defined by progressively greater intervals), with the number of impacts independently modeled within the fMRI analyses. Results revealed that differential exposure to high magnitude RHIs (≥90 g - < 110 g and ≥ 110 g) was associated with acute changes in neural activity for the bilateral leg press (broadly inclusive of motor, visual, and cognitive regions; all p < 0.05 & z > 3.1). Greater exposure to high magnitude RHIs may impair lower extremity motor control through maladaptive neural mechanisms. Future work is warranted to extend these mechanistic findings and examine the linkages between RHI exposure and neural activity as it relates to subsequent neuromuscular control deficits.

The Evolution of Neuroimaging Technologies to Evaluate Neural Activity Related to Knee Pain and Injury Risk.

PURPOSE OF REVIEW: In this review, we present recent findings and advancements in the use of neuroimaging to evaluate neural activity relative to ACL injury risk and patellofemoral pain. In particular, we describe prior work using fMRI and EEG that demonstrate the value of these techniques as well as the necessity of continued development in this area. Our goal is to support future work by providing guidance for the successful application of neuroimaging techniques that most effectively expose pain and injury mechanisms. RECENT FINDINGS: Recent studies that utilized both fMRI and EEG indicate that athletes who are at risk for future ACL injury exhibit divergent brain activity both during active lower extremity movement and at rest. Such activity patterns are likely due to alterations to cognitive, visual, and attentional processes that manifest as coordination deficits during naturalistic movement that may result in higher risk of injury. Similarly, in individuals with PFP altered brain activity in a number of key regions is related to subjective pain judgements as well as measures of fear of movement. Although these findings may begin to allow objective pain assessment and identification, continued refinement is needed. One key limitation across both ACL and PFP related work is the restriction of movement during fMRI and EEG data collection, which drastically limits ecological validity. Given the lack of sufficient research using EEG and fMRI within a naturalistic setting, our recommendation is that researchers target the use of mobile, source localized EEG as a primary methodology for exposing neural mechanisms of ACL injury risk and PFP. Our contention is that this method provides an optimal balance of spatial and temporal resolution with ecological validity via naturalistic movement.

Visuo-vestibular and cognitive connections of the vestibular neuromatrix are conserved across age and injury populations.

BACKGROUND AND PURPOSE: Given the prevalence of vestibular dysfunction in pediatric concussion, there is a need to better understand pathophysiological disruptions within vestibular and associated cognitive, affective, and sensory-integrative networks. Although current research leverages established intrinsic connectivity networks, these are nonspecific for vestibular function, suggesting that a pathologically guided approach is warranted. The purpose of this study was to evaluate the generalizability of the previously identified "vestibular neuromatrix" in adults with and without postconcussive vestibular dysfunction to young athletes aged 14-17. METHODS: This retrospective study leveraged resting-state functional MRI data from two sites. Site A included adults with diagnosed postconcussive vestibular impairment and healthy adult controls and Site B consisted of young athletes with preseason, postconcussion, and postseason time points (prospective longitudinal data). Adjacency matrices were generated from preprocessed resting-state data from each sample and assessed for overlap and network structure in MATLAB. RESULTS: Analyses indicated the presence of a conserved "core" network of vestibular regions as well as areas subserving visual, spatial, and attentional processing. Other vestibular connections were also conserved across samples but were not linked to the "core" subnetwork by regions of interest included in this study. CONCLUSIONS: Our results suggest that connections between central vestibular, visuospatial, and known intrinsic connectivity networks are conserved across adult and pediatric participants with and without concussion, evincing the significance of this expanded, vestibular-associated network. Our findings thus support this network as a workable model for investigation in future studies of dysfunction in young athlete populations.

The effects of sports-related concussion history on female adolescent brain activity and connectivity for bilateral lower extremity knee motor control.

Sports-related concussions (SRCs) are associated with neuromuscular control deficits in athletes following return to play. However, the connection between SRC and potentially disrupted neural regulation of lower extremity motor control has not been investigated. The purpose of this study was to investigate brain activity and connectivity during a functional magnetic resonance imaging (fMRI) lower extremity motor control task (bilateral leg press) in female adolescent athletes with a history of SRC. Nineteen female adolescent athletes with a history of SRC and nineteen uninjured (without a history of SRC) age- and sport-matched control athletes participated in this study. Athletes with a history of SRC exhibited less neural activity in the left inferior parietal lobule/supramarginal gyrus (IPL) during the bilateral leg press compared to matched controls. Based upon signal change detected in the brain activity analysis, a 6 mm region of interest (seed) was defined to perform secondary connectivity analyses using psychophysiological interaction (PPI) analyses. During the motor control task, the left IPL (seed) was significantly connected to the right posterior cingulate gyrus/precuneus cortex and right IPL for athletes with a history of SRC. The left IPL was significantly connected to the left primary motor cortex (M1) and primary somatosensory cortex (S1), right inferior temporal gyrus, and right S1 for matched controls. Altered neural activity in brain regions important for sensorimotor integration and motor attention, combined with unique connectivity to regions responsible for attentional, cognitive, and proprioceptive processing, indicate compensatory neural mechanisms may underlie the lingering neuromuscular control deficits associated with SRC.

The Effects of Attention-Deficit/Hyperactivity Disorder Symptoms on the Association between Head Impacts and Post-Season Neurocognitive and Behavioral Outcomes.

OBJECTIVE: Having attention-deficit/hyperactivity disorder (ADHD) is a risk factor for concussion that impacts concussion diagnosis and recovery. The relationship between ADHD and repetitive subconcussive head impacts on neurocognitive and behavioral outcomes is less well known. This study evaluated the role of ADHD as a moderator of the association between repetitive head impacts on neurocognitive test performance and behavioral concussion symptoms over the course of an athletic season. METHOD: Study participants included 284 male athletes aged 13-18 years who participated in high school football. Parents completed the Strengths and Weaknesses of ADHD Symptoms and Normal Behavior (SWAN) ratings about their teen athlete before the season began. Head impacts were measured using an accelerometer worn during all practices and games. Athletes and parents completed behavioral ratings of concussion symptoms and the Attention Network Task (ANT), Digital Trail Making Task (dTMT), and Cued Task Switching Task at pre- and post-season. RESULTS: Mixed model analyses indicated that neither head impacts nor ADHD symptoms were associated with post-season athlete- or parent-reported concussion symptom ratings or neurocognitive task performance. Moreover, no relationships between head impact exposure and neurocognitive or behavioral outcomes emerged when severity of pre-season ADHD symptoms was included as a moderator. CONCLUSION: Athletes' pre-season ADHD symptoms do not appear to influence behavioral or neurocognitive outcomes following a single season of competitive football competition. Results are interpreted in light of several study limitations (e.g., single season, assessment of constructs) that may have impacted this study's pattern of largely null results.

Visual-Spatial Attentional Performance Identifies Lower Extremity Injury Risk in Adolescent Athletes.

OBJECTIVE: Strategies to identify lower extremity musculoskeletal (LEMSK) injury risk have been informed by prospectively identified biomechanical and neuromuscular risk factors. Emergent evidence suggests that cognitive and oculomotor performance may also contribute to LEMSK injury. The purpose of this study was to determine whether prospective cognitive and oculomotor measures identify adolescent athletes who sustain an in-season LEMSK injury. DESIGN: Prospective longitudinal study. SETTINGS: Controlled laboratory and athletic event settings. PARTICIPANTS: Four hundred eighty-eight adolescent male football and female soccer athletes aged 13 to 18 years. ASSESSMENT OF RISK FACTORS: Preseason baseline cognitive and oculomotor performance: Attention Network Task (ANT), cued task switching, King-Devick test, and near point of convergence. MAIN OUTCOME MEASURE: Incidence of LEMSK sprains and strains during a single competitive season. RESULTS: Attention Network Task-orienting network reaction time (RT) was the only cognitive or oculomotor measure significantly associated with LEMSK injury [B = 1.015, 95% confidence interval (CI): 1.01-1.024, P < 0.01]. Every 10 milliseconds increase in orienting network RT was associated with a 15% increased risk for LEMSK injury. Athletes demonstrating an orienting network RT ≥ 32.8 milliseconds had a higher risk for LEMSK injury relative to athletes below the cut-point (relative risk, 2.62; 95% CI, 1.52-4.52; odds ratio, 3.00; 95% CI, 1.63-5.52). CONCLUSIONS: Deficits in visual-spatial components of attention were associated with 2.62 times greater risk for LEMSK injury in adolescent athletes. The present results add evidence to suggest that visual-spatial attentional processing contributes to LEMSK injury and may supplement previously established LEMSK injury risk assessments.

Characterization of Motor-Evoked Responses Obtained with Transcutaneous Electrical Spinal Stimulation from the Lower-Limb Muscles after Stroke.

An increasing number of studies suggests that a novel neuromodulation technique targeting the spinal circuitry enhances gait rehabilitation, but research on its application to stroke survivors is limited. Therefore, we investigated the characteristics of spinal motor-evoked responses (sMERs) from lower-limb muscles obtained by transcutaneous spinal cord stimulation (tSCS) after stroke compared to age-matched and younger controls without stroke. Thirty participants (ten stroke survivors, ten age-matched controls, and ten younger controls) completed the study. By using tSCS applied between the L1 and L2 vertebral levels, we compared sMER characteristics (resting motor threshold (RMT), slope of the recruitment curve, and latency) of the tibialis anterior (TA) and medial gastrocnemius (MG) muscles among groups. A single pulse of stimulation was delivered in 5 mA increments, increasing from 5 mA to 250 mA or until the subjects reached their maximum tolerance. The stroke group had an increased RMT (27-51%) compared to both age-matched (TA: p = 0.032; MG: p = 0.005) and younger controls (TA: p < 0.001; MG: p<0.001). For the TA muscle, the paretic side demonstrated a 13% increased latency compared to the non-paretic side in the stroke group (p = 0.010). Age-matched controls also exhibited an increased RMT compared to younger controls (TA: p = 0.002; MG: p = 0.007), suggesting that altered sMER characteristics present in stroke survivors may result from both stroke and normal aging. This observation may provide implications for altered spinal motor output after stroke and demonstrates the feasibility of using sMER characteristics as an assessment after stroke.