Authors: Robert E. Mangine, Thomas G. Palmer, James A. Tersak, Michael Mark, Joseph F Clark, Marsha Eifert-Mangine, Audrey Hill-Lindsay, Brian M Grawe
Categories: Case Series, Brain Mapping, Mirror Neuron Network, Neural networks, Neurophysiological assessment, Neuroplasticity, Quantitative electroencephalography/qEEG
Source: International Journal of Sports Physical Therapy
Doi: 10.26603/001c.124935
Authors: Robert E. Mangine, Thomas G. Palmer, James A. Tersak, Michael Mark, Joseph F Clark, Marsha Eifert-Mangine, Audrey Hill-Lindsay, Brian M Grawe
Athletic performance can be measured with a variety of clinical and functional assessment techniques. There is a need to better understand the relationship between the brain’s electrical activity and the body’s physiological performance capabilities in real-time while performing physical tasks related to sport. Orthopedic functional assessments used to monitor the neuroplastic properties of the central nervous system lack objectivity and/or pertinent functionality specific to sport. The ability to assess brain wave activity with physiological metrics during functional exercises associated with sport has proven to be difficult and impractical in real-time sport settings. Quantitative electroencephalography or qEEG brain mapping is a unique, real-time comprehensive assessment of brain electrical activity performed in combination with physiometrics which offers insight to neurophysiological brain-to-body function. Brain neuroplasticity has been associated with differences in musculoskeletal performance among athletes, however comparative real-time normal data to benchmark performance capabilities is limited.
This prospective, descriptive case series evaluated performance of task-driven activities using an innovative neurophysiological assessment technique of qEEG monitored neurophysiological responses to establish a comparative benchmark of performance capabilities in healthy, uninjured Division-I athletes.
Twenty-eight healthy uninjured females (n=11) and males (n=17) NCAA Division-I athletes participated in real-time neurophysiological assessment using a Bluetooth, wireless 21-channel dry EEG headset while performing functional activities.
Uninjured athletes experienced standard and regulated fluctuations of brain wave activity in key performance indicators of attention, workload capacity and sensorimotor rhythm (SMR) asymmetries.
qEEG neurophysiological real-time assessment concurrent with functional activities in uninjured, Division-I athletes may provide a performance capability benchmark. Real-time neurophysiological data can be used to monitor athletes’ preparedness to participate in sport, rehabilitation progressions, assist in development of injury prevention programs, and return to play decisions. While this paper focuses on healthy, uninjured participants, results underscore the need to discen pre-injury benchmarks.
4
Injury to the musculoskeletal system perpetuates concurrent and responsive neuroplastic alteration to the central nervous system that impacts quality of function.^1,2^ Recent objective real-time quantitative electroencephalogram (qEEG) neurophysiological assessment techniques have been identified to monitor neural adaptive structural and functional changes of the brain that impact functional movement patterns in pre- and post-injury status.^1,3^ Measuring neural activity of the brain during functional tasks offers clinicians objective data to evaluate and monitor regulatory functional properties of the brain-to-body connection offering insight to assist in identification of disturbances in musculoskeletal function leading to less than optimal biomechanical utility.^4^ Disturbances in the neural excitability and neuroplastic properties of the brain impacts neurophysiological function of the Central Nervous System (CNS) leading to altered motor responses during functional activities.^1–4^ Targeting the neuroplastic properties of the brain and CNS have become a primary goal for sports medicine professionals and athletes during both training and injury rehabilitation progressions. The ability to objectively track and monitor neurological structural and functional changes in the brain’s state that affect musculoskeletal function may allow for the optimal management of training and rehabilitation protocols. qEEG has been suggested as a metric for monitoring brain states and brain function as they relate to functional motor performance.^1^
Similar to functional Magnetic Resonance Imaging (fMRI) of the brain, qEEG reflects changes in the state of the brain related to workload of the different brain regions.^5^ However, fMRI techniques are not practically applicable for the assessment of dynamic and functional movements.^1,3^ In addition, the static fMRI images provide limited time windows of brain activity which limits the conclusive alterations associated with musculoskeletal function.^5^ qEEG offers consistent objective assessments of brain state and the ability to adapt to the changing environment.^6^
Assessing qEEG brain activity while performing functional movement in healthy uninjured athletes will provide normal objective performance indicators of neurophysiological function. Such baselines can serve as real-time performance properties that assume the brain state is adequately in sequence with the peripheral neurological properties.^5,6^ Such performance benchmarks can be used as comparative norms to help establish standards for athlete readiness to participate in sport. Therefore, this prospective investigation evaluated neurophysiological responses to performance of task-driven activities using an innovative neurophysiological assessment technique of qEEG monitored neurophysiological responses to establish a comparative benchmark of performance capabilities in healthy, uninjured Division-I athletes. Such baseline data may be used to measure neurophysiological changes as related to degradation and/or improvement of brain state over time.
Twenty-eight uninjured NCAA Division-I athletes qualified and consented to participate in this IRB approved prospective case series designed study. Athletes were excluded from participation if they presented with a current injury, a current history of an attention deficit, anxiety, or history of injury that resulted in disqualification from play in the prior six months. The twenty-eight athletes (10 females and 18 males) participated in a variety of competitive sports including both contact and non-contact.
Quantitative electroencephalography (qEEG) is a modern clinical digital assessment used to measure electrical patterns at the surface of scalp which reflect a continuous measure of cortical activity and are referred to as “brainwaves” and assess the central nervous system processing efficiency, power spectra, amplitude, and connectivity. qEEG was used to investigate real-time brain electrical patterns and neurophysiological function as it relates efficiency, power spectra, amplitude, and brain connectivity during functional movement tasks associated with sport. qEEG data were collected during a single testing session of baseline measures where each participant performed a uniform series of cognitive, motor imagery, reaction time and physical functional motor tasks (Figure 1). Baseline data were established by monitoring qEEG brain wave activity during periods where participants sat with eyes closed and eyes open. Once the qEEG baseline was established, participants performed a variety of tasks, including a cognitive test, overt imagery and a corresponding covert activity, functional movement exercises (balance, single limb, and agility tasks) and a reaction time test. Motor imagery was performed before and after five functional movement tasks as previously published.^1,7^ Functional movement tasks emphasized balance, gait, mobility and lower extremity symmetry.^8–10^

Cognitive tasks, including a Stroop Test, Positive Imagery Exercise, and Anticipation Challenge were designed to stimulate and measure cognitive functions. The Covert Imagery Task and companion Overt Motor Task were designed to stimulate and measure Mirror Neuron Network (MNN) activation. MNN is a critical component of the brain’s social cognitive function in action recognition, imitation, learning, and understanding the intentions and observations behind others’ actions. These neurons are excited during incidences when an individual performs or observes a motor skill which stimulates exclusive motor functions. Nine physical tasks an unloaded squat; single leg step down (right and left); single leg balance (right and left); sidestep right, sidestep left; and single leg squat (right and left), as well as a scored Reaction Test, were designed to stimulate Mirror Neuron Network activity while measuring regional connectivity and hemispherical asymmetry. These tasks also enabled measurement of attention levels and workload capabilities.^11,12^
Investigators utilized a CGX9 (Cognionics Company, San Diego CA) Quick-20r v2, 21-channel dry EEG head set to collect continuous electrical brain activity while simultaneously completing the the functional movements. Chi, et al.^7^ found this system to be a reliable and valid method to measure evoked response potentials as repeatable signals were seen when a standardized test protocol approach is used as compared to traditional wet, wired EEG systems. The dependent variables of cognitive function, attention, workload capability, and Sensorimotor Rhythm (SMR) asymmetries were monitored.^1,12^ Each measure accounted for acute real-time neurophysiological compensation and accommodations to physical and cognitive tasks.^13,14^ Additional physiological measures were conducted as secondary dependent variables to examine participants’ physical performance during each Neurophysiological Assessment Task. These measures heart rate to examine stress, anxiety and ability to relax^15^; heart rate variability to examine the ability regulate emotion, attention and breathing^16^; respiration rate to examine stress, concentration and ability to minimize distraction^17^; trapezius muscle tension to examine asymmetry and injury predisposition^18^; galvanic skin response to examine fatigue, emotional arousal and anticipation^19^; and peripheral temperature to examine the participant’s ability to regulate stress response.^20^ Physiometric data was collected with the CGX AIM^TM^ (CGX, a Cognionics Company, San Diego CA) physiological device.
The CLR Advantage^TM^ (CLR Neurosthenics® Manhattan Beach, CA) Neurophysiological Assessment Platform and the CGXAIM were utilized to simultaneously collect, process and analyze neurophysiological data from the brain and physiological monitoring through electrical data from the body. The CGX devices were then used to stream continuous biometric data via wireless connection to CLR Advantage. This configuration allowed participants to perform various physical tasks without restriction. After confirming the quality and consistency of CGX signal data, CLR Advantage was used to guide participants through the series of preprogrammed neurophysiologic assessment tasks. As investigators selected each task from a remote assessment screen (Figure 2, Step 1), CLR Advantage would display corresponding visual cues and instructions for participants to follow on a separate screen (Figure2, Step 2). Upon completion of each assessment, CLR Advantage would utilize Intheon Neuroscale^TM^ to generate analytic reports for each participant (Figure2, Step 3). CLR Advantage was also used to collect preassessment profile and medical history data from each participant.^1^

The EEG and physiologic data screen were designed to capture the most relevant and incisive athletic performance metrics. With 21 channels of continuously streaming EEG, investigators were able to collect data to determine participants’ neural network connectivity, activation, asymmetry and frequency bands levels during each neurophysiological assessment task. The data collected supported sufficient Power Spectral Density (PSD) levels to measure performance across multiple networks and regions of interest a) Default Mode Network (medial prefrontal cortex, posterior cingulate cortex, Hippocampus, precuneus, inferior parietal lobe, parietal regions and temporal lobe); b) Salience Network (anterior insula and dorsal anterior cingulate cortex); c) Mirror Neuron Network (inferior frontal cortex and in the inferior parietal cortex, d) Attention (dorsal frontoparietal); e) Sensorimotor Cortex (primary somatosensory cortical area and the primary motor cortical area); and, f) Occipital Lobe (visual processing center ). PSD levels also provided sufficient data to calculate performance within EEG frequency bands, Including: g) Delta (0.5 to 4Hz); h) Theta (4 to 7Hz); i) Alpha (8 to 12Hz); j) SMR(12 to 15Hz); and k) Beta1-3 (12 to 30Hz
Power spectral analysis (PSA) is a common and well-established method for analyzing EEG signals.^19^ PSA uses a power spectrum to quantify the amplitude of each frequency component in the EEG waveform. PSA estimates the power of a signal at different frequencies.
Spectral analysis comparison between power and frequency bands was measured at the change between Eyes Open (EO) and Eyes Closed (EC). The Welsh^20^ method was used for spectral density estimation and used for estimating the power spectral density analysis and then used 1/frequency (F) normalization to convert to decibels. The raw EEG compared EO versus EC during resting states and analytics based on measurements per channel, across all channels, right and left hand as well as different brain regions, frequency bands, frequency band ratios and Regions of Interest (ROI). Figure 3 represents a sample Power Spectral Density (PSD) assessment of a male participant.



Upon completion of each participant assessment session, collected data was further processed to calculate individual performance metrics, data aggregation, exponential smoothing (by task) and generation of sub-cohort (uninjured, male/female) analytics. The CLR Advantage Neurophysiological Assessment Platform was utilized to analyze participants’ Individual Performance Reports (IPRs) then compare those results to that of the study sub-cohort (uninjured male and female athletes). IPRs may be used to identify neurophysiological deficiencies and provide clinically valuable information to the rehabilitation specialists, coach, or athlete themselves about how the reacts and accommodates based on the demands of their sport and/or position. Four reports generated

The mean age of participants was 19.37 ± 1 years (females 19.8 years; males 19.1 years); height = 176.75cm ± 8.05 cm (females 167cm; males 186cm); weight = 79.38 ± 14.36 kg females 67kg; males 84kg). (Figure 7)

Analysis of the qEEG data of the male and female athletes in this case series demonstrated asymmetries during motor strategies during the step down left, single leg squat and the unloaded squat. Females performed better in the single leg squat and unloaded squat while males performed better on the step-down landing left task. These findings were also supported by the SMR Cortex plots. These cortex plots illustrate characteristics for both male and female, regions of interest, frequency bands of the EEG and network activation during assessment of motor tasks that emphasize balance, gait, mobility and lower extremity symmetry. (Figure 8)

The Attention metric indicates the ability to maintain goal-directed behavior in the face of distractions. The metric composites were measured during the performance of the functional movement tasks, covert and overt imagery, and cognitive tasks. The attention metric is calculated utilizing frequency band ratios of frontal theta and beta/alpha. Attention increased consistently for both females and males until the single leg balance task as represented in Figure 9.

Brain workload is related to the brain region(s) of interest engaged through electrical connections during the performance of tasks being performed. The workload metric indicates how the brain responds to the activities being engaged. Results from previous studies have shown that there is a significant difference between men and women in terms of brain workload capability.^24^ Figure 10 indicates the brain workload metric by task for both females and males. Females’ cognitive workload capability was higher than males beginning at the initial baseline task. Monitoring brain workload in tandem with other key components, such as, attention and focus provide insight as to the effect certain tasks may tax the brain state.

Resting state utilized a spectral analysis comparison between power and frequency bands measuring the delta between EO and EC. The EEG cortex plots illustrate characteristics of various networks for both males and females, and activity in both left and right hemispheres during select functional movement tasks. The EEG cortex plots demonstrate longitudinal EEG for the initial brain map baseline, cognitive tasks, motor tasks and mental imagery. Females exhibited more symmetrical pre- and post- motor task. (Figure 11)

The primary objective of this case series was to utilize neurophysiologic assessment data, including brain hemisphere asymmetry, attention levels, and brain workload analytics to quantify performance outcomes in healthy, uninjured athletes during functional movements.^1,12^ The results demonstrate variances in functional tasks between uninjured Division-I athletes (males and female) in key performance indicators of cognitive function, attention, brain workload capability and SMR asymmetry were observed. Musculoskeletal biomechanical asymmetries or disfunction have been previously reported to be associated with variations in muscle and brain symmetry between left and right hemispheres.^25^ The reported data affords a visual representation of neurophysiological performance observed during with qEEG monitoring during performance of task driven assessments. This provides researchers and clinicians alike with a possible mechanism to explore neural behaviors, brain symmetries, and brain state regulation associated with normal movements.
Current applications in rehabilitation have increasingly embraced the concept of neural-oriented rehabilitation methods to facilitate neuroplastic adaptation. The brain has multiple cell types that divide and grow, thus developing new connections throughout a lifespan.^26^ Plasticity is a hallmark of the adaptability of the brain to remodel, adapt, and repair the central nervous system as a result of purposeful interventions using environmental modifications and brain exercises to stimulate neurofeedback improvements.^27,28^ In a similar fashion, neurological assessments provide insight into the functioning properties of the neural brain-to-body connection.
Sports medicine professionals are familiar with the concept that skeletal muscle cells do not divide with conditioning, but brain cells can divide and precipitate plasticity.^26^ It is incumbent upon the rehabilitation specialist to be cognizant of the role of the brain’s adaptability and changes that are seen in the pre- and post-injury periods. Dysregulation and rebuilding of neural networks during functional development and during the rehabilitation process are the hallmarks of neuroplasticity. Mangine et al.^1^ used high fidelity real-time qEEG and physiometric monitoring software to demonstrate simultaneous linear improvements in neurophysiological and musculoskeletal performance in a case report of an athlete after anterior cruciate ligament reconstruction and rehabilitation during a return to play progression. Although in a single subject, these findings suggest changes in the brain’s neuroplastic properties impact musculoskeletal function.^1^ Thus, clinicians should seek to objectively evaluate brain state during functional training and/or rehabilitation progressions.
Division I athletes possess elite levels of human performance capabilities in strength, agility, balance, reaction time and focus.^24^ Until recently, measuring these capabilities was largely limited to sport statistics, kinematic observation (time trials, jumping distance, etc.)^24^ and various strength assessments (bench press, leg press, etc.).^29^ Over time, the proliferation of sports related injuries has warranted investigations into the role the of the brain-to-body connection^30^ in athletic performance, including both psychological factors^31,32^ and neurological function.^33^
There is a need for methods to support assessment of facets of neuroplasticity as part of functional rehabilitation and the development of athletic skills. The current case series provides information gained from neurophysiologic assessment that demonstrates a foundation utilizing analytics from task-driven exercises to evaluate and benchmark athletic performance capabilities and may assist optimize rehabilitation outcomes within the sports medicine field.
Embracing rehabilitation interventions designed to optimize brain and body performance seems ideal for monitoring athlete preparedness in both clinical rehabilitation and sports performance. Recent findings^1^ have reported dysregulation in qEEG brain mapping occurs following anterior-cruciate injury and/or reconstruction. Mangine et al.^1^ demonstrated a functional correction in brain state regulation to be related to improved neurophysiological outcomes, such as, reaction time and task completion during a rehabilitative return to play process following an anterior cruciate ligament repair in a single subject. A dysregulated brain state appears to disrupt neuroprocessing necessary to maintain biomechanical and functional stability associated with sport performance and injury prevention mechanics.^7,33^ Future studies could utilize neurophysiological baseline data and progressive assessment information to aid in decision making concerning management and rehabilitation of the injured athlete**.**
This case series is a first requisite step in building a body of evidence connecting physical activities and brain functional responses among healthy athletes. Using a combination of qEEG, physiometrics, psychometric, and kinematic applications to monitor change in neurophysiological performance post musculoskeletal injury seems warranted but requires more specialized targeted programs for behaviors associated with brain process for motor control, skill development, and biomechanical sport functions. Future studies should investigate the use of neurophysiological assessments to help determine brain regulatory status and functional readiness to return to athletic participation. Additionally, advanced understanding of brain activity to coordinate neuromuscular function during sports participation may assist sports medicine professionals in examining strategies to mitigate injuries.
The neurophysiologic assessments were performed on healthy non-fatigued, uninjured Division 1 athletes using musculoskeletal movements associated with sport and rehabilitation. Fatigue factors have been shown to have a relationship with functional performance^34^ and were not accounted for in this case series. qEEG data were not collected during actual sport participation, so maximal strength and maximal speed likely not reached by each participant. The task driven activities were limited to controlled movements requiring the brain and body functioning together supporting clean analytics by limiting extraneous EEG “noise” during data collection. Notwithstanding, outcome measures from the current study are unique in combining qEEG, physiometric, and physical movements**.**
The data collected in this case series supports the potential use of the combination of qEEG and physiometric data as a novel neurophysiological real-time measurement to serve as a clinical assessment for establishing comparative baseline normative data for athlete performance. In addition to the unique utility of qEEG and neurophysiologic as an assessment for baseline data, qEEG assessment could provide meaningful data to support clinical decision making and clinical intervention choices. Performing qEEG assessments in tandem with functional movements may allow clinicians to gain insight into the athlete’s potential readiness for participation and safe return to play, related to brain health and neurophysiological function. The authors hope that this work will be to empower sports medical professionals to consider quantitative information concerning the brain’s role in motor function as it relates to motor performance and rehabilitation in athletic or functionally active populations.