Repetitive subconcussive head impacts and changes in sensory processing for balance control

Repetitive subconcussive head impacts (RHI) may be associated with current and future detrimental neurological effects. However, the effects of RHI on sensory processing for balance control is unknown and may have significant clinical implications if athletes are still participating in sport despite impairments.  Question Are there changes in sensory processing for balance control during standing and walking following RHI?  Thirty healthy, adult, amateur soccer players (15 males, 15 females, 21.8±2.8 years, 69.9±11.5 kg, 171.4±8.2 cm) volunteered for the standing balance assessment (i.e., experiment 1). A distinct cohort of twenty healthy, adult, amateur soccer players (10 males, 10 females, 22.3±4.5 years, 70.0±10.5 kg, 170.5±9.8 cm) volunteered for the walking balance assessment (i.e., experiment 2). We used a repeated measures design across three time points (pre-heading, 0-hours post-heading, 24-hours post-heading). Participants were randomly assigned to an experimental (i.e., performed 10 soccer headers in 10 minutes) or a control group (i.e., did not perform any soccer heading between sessions). In experiment 1, participants stood in a virtual reality cave while experiencing simultaneous perturbations to their visual, vestibular, and proprioceptive systems. In experiment 2, participants walked blindfolded along a foam walkway and experienced a vestibular perturbation on the second heel strike of the right foot. Changes in sensory processing were assessed using repeated measures ANOVAs.  There were no changes in sensory reweighting during experiment 1 and no changes in balance responses to the vestibular stimulus in experiment 2.  Although the cumulative effects of RHI may result in later-life cognitive, behavioral, and mood impairments, a single episode of repeated soccer headers does not appear to be associated with acute impairments in sensory processing for balance control.

Related papers:

title: Chronic Traumatic Encephalopathy in Athletes: Progressive Tauopathy After Repetitive Head Injury
abstract: Since the 1920s, it has been known that the repetitive brain trauma associated with boxing may produce a progressive neurological deterioration, originally termed dementia pugilistica, and more recently, chronic traumatic encephalopathy (CTE). We review 48 cases of neuropathologically verified CTE recorded in the literature and document the detailed findings of CTE in 3 professionalathletes, 1 football player and 2 boxers. Clinically, CTE is associated with memory disturbances, behavioral and personality changes, parkinsonism, and speech and gait abnormalities. Neuropathologically, CTE is characterized by atrophy of the cerebral hemispheres, medial temporal lobe, thalamus, mammillary bodies, and brainstem, with ventricular dilatation and a fenestrated cavum septum pellucidum. Microscopically, there are extensive tau-immunoreactive neurofibrillary tangles, astrocytic tangles, and spindle-shaped and threadlike neurites throughout the brain. The neurofibrillary degeneration of CTE is distinguished from other tauopathies by preferential involvement of the superficial cortical layers, irregular patchy distribution in the frontal and temporal cortices, propensity for sulcal depths, prominent perivascular, periventricular, and subpial distribution, and marked accumulation of tau-immunoreactive astrocytes. Deposition of &bgr;-amyloid, most commonly as diffuse plaques, occurs in fewer than half the cases. Chronic traumatic encephalopathy is a neuropathologically distinct slowly progressive tauopathy with a clear environmental etiology.

title: Head impact exposure in collegiate football players.
abstract: In American football, impacts to the helmet and the resulting head accelerations are the primary cause of concussion injury and potentially chronic brain injury. The purpose of this study was to quantify exposures to impacts to the head (frequency, location and magnitude) for individual collegiate football players and to investigate differences in head impact exposure by player position. A total of 314 players were enrolled at three institutions and 286,636 head impacts were recorded over three seasons. The 95th percentile peak linear and rotational acceleration and HITsp (a composite severity measure) were 62.7g, 4378rad/s(2) and 32.6, respectively. These exposure measures as well as the frequency of impacts varied significantly by player position and by helmet impact location. Running backs (RB) and quarter backs (QB) received the greatest magnitude head impacts, while defensive line (DL), offensive line (OL) and line backers (LB) received the most frequent head impacts (more than twice as many than any other position). Impacts to the top of the helmet had the lowest peak rotational acceleration (2387rad/s(2)), but the greatest peak linear acceleration (72.4g), and were the least frequent of all locations (13.7%) among all positions. OL and QB had the highest (49.2%) and the lowest (23.7%) frequency, respectively, of front impacts. QB received the greatest magnitude (70.8g and 5428rad/s(2)) and the most frequent (44% and 38.9%) impacts to the back of the helmet. This study quantified head impact exposure in collegiate football, providing data that is critical to advancing the understanding of the biomechanics of concussive injuries and sub-concussive head impacts.

title: Reducing purposeful headers from goal kicks and punts may reduce cumulative exposure to head acceleration
abstract: The purpose of this study was to measure peak linear and rotational head acceleration in women’s collegiate soccer and explore the variations in acceleration across different strategic scenarios. Game videos from 14 games were used to identify the strategic scenario in which the athlete headed the ball. Strategic scenarios included: bounce, secondary header, punt, throw-in, goal kick, corner kick, and kick. Peak linear and rotational accelerations were measured using the Smart Impact Monitor (Triax Technologies Inc., Norwalk, CT). Goal kick (38.8 ± 19.4 g, p = 0.001, ß = 8.9; 9.3 ± 3.9 krad/s2, p = 0.004, ß = 1.9) and punt (36.0 ± 15.1 g, p = 0.055, ß = 6.3; 10.1 ± 4.8 krad/s2, p = 0.002, ß = 2.5) impacts resulted in higher linear and rotational head accelerations than the base variable, kick (30.0 ± 19.5 g; 7.5 ± 4.1 krad/s2). This suggests that limiting headers from goal kicks and punts in younger athletes who are still learning proper heading technique may limit cumulative linear and rotational accelerations.

title: Linear Acceleration in Direct Head Contact Across Impact Type, Player Position, and Playing Scenario in Collegiate Women's Soccer Players.
abstract: Heading, an integral component of soccer, exposes athletes to a large number of head impacts over a career. The literature has begun to indicate that cumulative exposure may lead to long-term functional and psychological deficits. Quantifying an athlete's exposure over a season is a first step in understanding cumulative exposure.


To measure the frequency and magnitude of direct head impacts in collegiate women's soccer players across impact type, player position, and game or practice scenario.


National Collegiate Athletic Association Division I institution.


Twenty-three collegiate women's soccer athletes.



  Athletes wore Smart Impact Monitor accelerometers during all games and practices. Impacts were classified during visual, on-field monitoring of athletic events. All direct head impacts that exceeded the 10 g threshold were included in the final data analysis. The dependent variable was linear acceleration, and the fixed effects were (1) type of impact: clear, pass, shot, unintentional deflection, or head-to-head contact; (2) field position: goalkeeper, defense, forward, or midfielder; (3) playing scenario: game or practice.


Shots (32.94 g ± 12.91 g, n = 38; P = .02) and clears (31.09 g ± 13.43 g, n = 101; P = .008) resulted in higher mean linear accelerations than passes (26.11 g ± 15.48 g, n = 451). Head-to-head impacts (51.26 g ± 36.61 g, n = 13; P < .001) and unintentional deflections (37.40 g ± 34.41 g, n = 24; P = .002) resulted in higher mean linear accelerations than purposeful headers (ie, shots, clears, and passes). No differences were seen in linear acceleration across player position or playing scenario.


Nonheader impacts, including head-to-head impacts and unintentional deflections, resulted in higher mean linear accelerations than purposeful headers, including shots, clears, and passes, but occurred infrequently on the field. Therefore, these unanticipated impacts may not add substantially to an athlete's cumulative exposure, which is a function of both frequency and magnitude of impact.

title: Potential Long-Term Consequences of Concussive and Subconcussive Injury.
abstract: Repeated concussive and subconcussive trauma is associated with the later development of chronic traumatic encephalopathy (CTE), a neurodegenerative disease associated with clinical symptoms in multiple domains and a unique pattern of pathologic changes. CTE has been linked to boxing and American football; CTE has also been identified in soccer, ice hockey, baseball, rugby, and military service. To date, most large studies of CTE have come from enriched cohorts associated with brain bank donations for traumatic brain injury, although several recent studies re-examining neurodegenerative disease brain banks suggest that CTE is more common than is currently appreciated.

title: Subconcussive head impacts in sport: A systematic review of the evidence.
abstract: To identify and evaluate the evidence that examines subconcussive impacts in sport-specific settings, and address two objectives: a) to determine how 'subconcussion' is characterized in the current literature, and b) to identify directions for future research.



Systematic review.



CINAHL, EMBASE, MedLine, PsycINFO, SportDiscus, and Web of Science were searched for articles that sought to assess subconcussive impacts or outcomes related to non-concussive head impact exposure. Eligible articles were reviewed and evaluated with three quality assessment tools by rotating pairs of reviewers.



A total of 1966 articles were screened. Fifty-six studies met the inclusion criteria. Studies were classified into three main categories based on primary focus: neurobiological, neuropsychological, and impact exposure metrics. The neurobiological studies suggested that in male athletes, functional and microstructural deterioration was associated with repetitive head impacts. There was insufficient to weak evidence for the relationship between repetitive hits to the head and deterioration in neurocognitive performance. Studies of impact exposure metrics examined various indices, including linear acceleration, rotational acceleration, and location and frequency of hits. Insufficient evidence was presented to determine a minimal injury threshold for repetitive hits to the head. Across all categories of studies there was a lack of consistency and clarity in defining and measuring variables related to the concept of 'subconcussion'.



Evidence reviewed predominantly from studies of male athletes in contact and collision sports identifies that repetitive hits to the head are associated with microstructural and functional changes in the brain. Whether these changes represent injury is unclear. We determined the term 'subconcussion' to be inconsistently used, poorly defined, and misleading. Future research is needed to characterize the phenomenon in question.

title: The neurobiological effects of repetitive head impacts in collision sports
abstract: It is now recognized that repetitive head impacts (RHI) in sport have the potential for long-term neurological impairments. In order to identify targets for intervention and/or pharmacological treatment, it is necessary to characterize the neurobiological mechanisms associated with RHI. This review aims to summarize animal and human studies that specifically address Blood Brain Barrier (BBB) dysfunction, abnormal neuro-metabolic and neuro-inflammatory processes as well as Tau aggregation associated with RHI in collision sports. Additionally, we examine the influence of physical activity and genetics on outcomes of RHI, discuss methodological considerations, and provide suggestions for future directions of this burgeoning area of research.

title: Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion.
abstract: Head trauma and concussion in football players have recently received considerable media attention. Postmortem evidence suggests that accrual of damage to the brain may occur with repeated blows to the head, even when the individual blows fail to produce clinical symptoms. There is an urgent need for improved detection and characterization of head trauma to reduce future injury risk and promote development of new therapies. In this study we examined neurological performance and health in the presence of head collision events in high school football players, using longitudinal measures of collision events (the HIT(™) System), neurocognitive testing (ImPACT(™)), and functional magnetic resonance imaging MRI (fMRI). Longitudinal assessment (including baseline) was conducted in 11 young men (ages 15-19 years) participating on the varsity and junior varsity football teams at a single high school. We expected and observed subjects in two previously described categories: (1) no clinically-diagnosed concussion and no changes in neurological behavior, and (2) clinically-diagnosed concussion with changes in neurological behavior. Additionally, we observed players in a previously undiscovered third category, who exhibited no clinically-observed symptoms associated with concussion, but who demonstrated measurable neurocognitive (primarily visual working memory) and neurophysiological (altered activation in the dorsolateral prefrontal cortex [DLPFC]) impairments. This new category was associated with significantly higher numbers of head collision events to the top-front of the head, directly above the DLPFC. The discovery of this new category suggests that more players are suffering neurological injury than are currently being detected using traditional concussion-assessment tools. These individuals are unlikely to undergo clinical evaluation, and thus may continue to participate in football-related activities, even when changes in brain physiology (and potential brain damage) are present, which will increase the risk of future neurological injury.

title: Biomechanical correlates of symptomatic and asymptomatic neurophysiological impairment in high school football.
abstract: Concussion is a growing public health issue in the United States, and chronic traumatic encephalopathy (CTE) is the chief long-term concern linked to repeated concussions. Recently, attention has shifted toward subconcussive blows and the role they may play in the development of CTE. We recruited a cohort of high school football players for two seasons of observation. Acceleration sensors were placed in the helmets, and all contact activity was monitored. Pre-season computer-based neuropsychological tests and functional magnetic resonance imaging (fMRI) tests were also obtained in order to assess cognitive and neurophysiological health. In-season follow-up scans were then obtained both from individuals who had sustained a clinically-diagnosed concussion and those who had not. These changes were then related through stepwise regression to history of blows recorded throughout the football season up to the date of the scan. In addition to those subjects who had sustained a concussion, a substantial portion of our cohort who did not sustain concussions showed significant neurophysiological changes. Stepwise regression indicated significant relationships between the number of blows sustained by a subject and the ensuing neurophysiological change. Our findings reinforce the hypothesis that the effects of repetitive blows to the head are cumulative and that repeated exposure to subconcussive blows is connected to pathologically altered neurophysiology.

title: Soccer heading is associated with white matter microstructural and cognitive abnormalities.
abstract: To investigate the association of soccer heading with subclinical evidence of traumatic brain injury.



With institutional review board approval and compliance with HIPAA guidelines, 37 amateur soccer players (mean age, 30.9 years; 78% [29] men, 22% [eight] women) gave written informed consent and completed a questionnaire to quantify heading in the prior 12 months and lifetime concussions. Diffusion-tensor magnetic resonance (MR) imaging at 3.0 T was performed (32 directions; b value, 800 sec/mm(2); 2 × 2 × 2-mm voxels). Cognitive function was measured by using a computerized battery of tests. Voxelwise linear regression (heading vs fractional anisotropy [FA]) was applied to identify significant regional associations. FA at each location and cognition were tested for a nonlinear relationship to heading by using an inverse logit model that incorporated demographic covariates and history of concussion.



Participants had headed 32-5400 times (median, 432 times) over the previous year. Heading was associated with lower FA at three locations in temporo-occipital white matter with a threshold that varied according to location (885-1550 headings per year) (P < .00001). Lower levels of FA were also associated with poorer memory scores (P < .00001), with a threshold of 1800 headings per year. Lifetime concussion history and demographic features were not significantly associated with either FA or cognitive performance.



Heading is associated with abnormal white matter microstructure and with poorer neurocognitive performance. This relationship is not explained by a history of concussion.

title: Heading Frequency Is More Strongly Related to Cognitive Performance Than Unintentional Head Impacts in Amateur Soccer Players
abstract: Compared to heading, unintentional head impacts (e.g., elbow to head, head to head, head to goalpost) in soccer are more strongly related to risk of moderate to very severe Central Nervous System (CNS) symptoms. But, most head impacts associated with CNS symptoms that occur in soccer are mild and are more strongly related to heading. We tested for a differential relation of heading and unintentional head impacts with neuropsychological (NP) test performance.  Active adult amateur soccer players were recruited in New York City and the surrounding areas for this repeated measures longitudinal study of individuals who were enrolled if they had 5+ years of soccer play and were active playing soccer 6+ months/year. All participants completed a baseline validated questionnaire (“HeadCount-2w”), reporting 2-week recall of soccer activity, heading and unintentional head impacts. In addition, participants also completed NP tests of verbal learning, verbal memory, psychomotor speed, attention, and working memory. Most participants also completed one or more identical follow-up protocols (i.e., HeadCount-2w and NP tests) at 3- to 6-month intervals over a 2-year period. Repeated measures General Estimating Equations (GEE) linear models were used to determine if variation in NP tests at each visit was related to variation in either heading or unintentional head impacts in the 2-week period before testing. Results 308 players (78% male) completed 741 HeadCount-2w. Mean (median) heading/2-weeks was 50 (17) for men and 26 (7) for women. Heading was significantly associated with poorer performance on psychomotor speed (p < 0.001) and attention (p = 0.02) tasks and was borderline significant with poorer performance on the working memory (p = 0.06) task. Unintentional head impacts were not significantly associated with any NP test. Results did not differ after excluding 22 HeadCount-2w with reported concussive or borderline concussive symptoms.  Poorer NP test performance was consistently related to frequent heading during soccer practice and competition in the 2 weeks before testing. In contrast, unintentional head impacts incurred during soccer were not related to cognitive performance.

title: Acute changes in postural control after soccer heading.
abstract: This study intended to determine if an acute bout of soccer heading alters postural control and pronounced self-reported symptoms of cerebral concussion. Collegiate soccer players were randomly assigned to one of 2 groups. Each participant completed a baseline postural control assessment prior to heading. Participants either simulated (control group; CG) or performed (experimental group; EG) 10 headers at 11.2 m/s in 10 min. The postural assessment was repeated post heading at hrs 1, 24, and 48. The postural control parameter assessed was the root mean square (RMS) of the center of mass (COM). COM RMS were calculated for the anterior-posterior (AP) and medial-lateral (ML) time series. Compared to the CG, for the AP and ML time series COM RMS values were significantly higher in the EG at hr 24 (p <0.05). An acute bout of heading results in quantifiable alterations in postural control that are detectable 24 h post heading and dissipate within an additional 24 h. The significant findings may be due to the dynamic postural control assessment that incorporated robust discordant environmental conditions.

title: An in-vivo model of functional head impact testing in non-helmeted athletes
abstract: Development of a functional in-vivo head impact testing model would enhance the ability to elucidate mechanisms underlying individual responses to head impact in sports where a helmet is not worn. The objective of this paper is to describe a novel in-vivo method of assessing human head linear impact acceleration during the functional activity of soccer heading, using a repeated-measures design in a university research laboratory. 17 college-aged soccer players (age, 20.93 years (standard deviation (SD), 1.17 years); height, 170.39cm (SD, 10.15cm); mass, 71.50kg (SD, 9.89kg); head—neck mass, 5.90kg (SD, 0.83kg)) participated in this study. All participants read and signed a university Institutional-Review-Board-approved informed consent before participating. The resultant linear head acceleration (in units of g) was measured for each participant during soccer heading. The head impact model consisted of controlled soccer headers and a triaxial accelerometer affixed to a custom-fitted mouthpiece. A force-sensitive resistor on the forehead assessed impact quality. Standard soccer balls were projected from a JUGS soccer machine travelling at 11.10m/s (25mile/h) and covering a distance of 11m (35ft). The subjects performed standing or simulated headers while aiming at a target positioned 5m in front of them. The intra-class correlation coefficient (ICC2,1) was 0.845 for resultant accelerations. In this paper, the development and testing of a novel in-vivo functional human head impact testing model are described. Results suggest that this methodology has potential for assessing resultant peak linear head impact accelerations during the functional activity of soccer heading and in other non-helmet-wearing sports.

title: Effect of soccer heading ball speed on S100B, sideline concussion assessments and head impact kinematics
abstract: To examine the effect of soccer heading ball speed on S-100B serum concentration, concussion sideline assessments and linear head impact acceleration.  Sixteen division I soccer players participated in this pre-test post-test design study. Athletes performed five standing headers over a 10 minute period at 30 (n = 5), 40 (n = 5) or 50 (n = 6) miles per hour (mph) (randomized). S-100B serum concentration (ng mL−1) and sideline concussion assessments were measured prior to and post-heading. Peak resultant linear head acceleration (gravitational units; g) was measured during soccer heading.  No statistically significant interaction effects were identified between ball velocity groups over time on S100B (effect sizes ranged from 0.03–0.23) or concussion assessments tests. There was a non-significant increase (p = 0.06) in head impact acceleration from the 30 (30.6; SD = 6.2 g) to 50 mph (50.7; SD = 7.7 g) ball speed.  In this controlled setting, an acute bout of soccer heading across various ball velocities did not affect S100B or concussion assessment test scores. These findings are preliminary, as the small sample size in each group may have played a role in the lack of significant findings.

title: Head and neck size and neck strength predict linear and rotational acceleration during purposeful soccer heading
abstract: There is increasing societal concern about the long-term effects of repeated impacts from soccer heading, but there is little information about ways to reduce head impact severity. The purpose of this study was to identify factors that contribute to head acceleration during soccer heading. One-hundred soccer players completed 12 controlled soccer headers. Peak linear (PLA) and rotational (PRA) accelerations were measured using a triaxial accelerometer and gyroscope. Head acceleration contributing factors were grouped into 3 categories: size (head mass, neck girth), strength (sternocleidomastoid, upper trapezius) and technique [kinematics (trunk, head-to-trunk range-of-motion), sternocleidomastoid and upper trapezius activity]. Multiple regression analyses indicated size variables explained 22.1% of the variance in PLA and 23.3% of the variance in PRA; strength variables explained 13.3% of the variance in PLA and 17.2% of the variance in PRA; technique variables did not significantly predict PLA or PRA. These findings suggest that head and neck size and neck strength predict PLA and PRA. Anthropometric and neck strength measurements should be considered when determining an athlete’s readiness to begin soccer heading.

title: Sex and age differences in head acceleration during purposeful soccer heading
abstract: Differences in head–neck segment mass, purposeful heading technique, and cervical strength and stiffness may contribute to differences in head accelerations across sex and age. The purpose of this study was to compare head acceleration across sex and age (youth [12–14 years old], high school and collegiate) during purposeful soccer heading. One-hundred soccer players (42 male, 58 female, 17.1 ± 3.5 years, 168.5 ± 20.3 cm, 61.5 ± 13.7 kg) completed 12 controlled soccer headers at an initial ball velocity of 11.2 m/s. Linear and rotational accelerations were measured using a triaxial accelerometer and gyroscope and were transformed to the head centre-of-mass. A MANOVA revealed a significant multivariate main effect for sex (Pillai’s Trace = .165, F(2,91) = 11.868, p < .001), but not for age (Pillai’s Trace = .033, F(4,182) = 0.646, p = .630). Peak linear and rotational accelerations were higher in females (40.9 ± 13.3 g; 3279 ± 1065 rad/s2) than males (27.6 ± 8.5 g, 2219 ± 823 rad/s2). These data suggest that under controlled soccer heading conditions, females may be exposed to higher head accelerations than males.

title: Vestibular Dysfunction after Subconcussive Head Impact.
abstract: Current thinking views mild head impact (i.e., subconcussion) as an underrecognized phenomenon that has the ability to cause significant current and future detrimental neurological effects. Repeated mild impacts to the head, however, often display no observable behavioral deficits based on standard clinical tests, which may lack sensitivity. The current study investigates the effects of subconcussive impacts from soccer heading with innovative measures of vestibular function and walking stability in a pre- 0-2 h, post- 24 h post-heading repeated measures design. The heading group (n = 10) executed 10 headers with soccer balls projected at a velocity of 25 mph (11.2 m/sec) over 10 min. Subjects were evaluated 24 h before, immediately after, and 24 h after soccer heading with: the modified Balance Error Scoring System (mBESS); a walking stability task with visual feedback of trunk movement; and galvanic vestibular stimulation (GVS) while standing with eyes closed on foam. A control group (n = 10) followed the same protocol with no heading. The results showed significant decrease in trunk angle, leg angle gain, and center of mass gain relative to GVS for the heading group compared with controls. Medial-lateral trunk orientation displacement and velocity during treadmill walking increased immediately after mild head impact for the heading group compared with controls. Controls showed an improvement in mBESS scores over time, indicating a learning effect, which was not observed with the heading group. These results suggest that mild head impact leads to a transient dysfunction in vestibular processing, which deters walking stability during task performance.

title: Vestibular and balance issues following sport-related concussion
abstract: To review relevant literature regarding the effect of concussion on vestibular function, impairments, assessments and management strategies.  Dizziness and balance impairments are common following sport-related concussion. Recommendations regarding the management of sport-related concussion suggest including tests of balance within the multifactorial assessment paradigm for concussive injuries.  The literature was searched for guidelines and original studies related to vestibular impairments following concussion, oculomotor and balance assessments and treatment or rehabilitation of vestibular impairments. The databases searched included Medline, CINAHL, Sport Discus and the Cochrane Database of Systematic Reviews through October 2013.  Dizziness following concussion occurs in ∼67–77% of cases and has been implicated as a risk factor for a prolonged recovery. Balance impairments also occur after concussion and last 3–10 days post-injury. Assessments of balance can be done using both clinical and instrumented measures with success. Vestibular rehabilitation has been shown to improve outcomes in patients with vestibular impairments, with one study demonstrating success in decreasing symptoms and increasing function following concussion.  Best practices suggest that the assessment of vestibular function through cranial nerve, oculomotor and balance assessments are an important aspect of concussion management. Future studies should evaluate the effectiveness of vestibular rehabilitation for improving patient outcomes.

title: Dynamic Reweighting of Three Modalities for Sensor Fusion
abstract: We simultaneously perturbed visual, vestibular and proprioceptive modalities to understand how sensory feedback is re-weighted so that overall feedback remains suited to stabilizing upright stance. Ten healthy young subjects received an 80 Hz vibratory stimulus to their bilateral Achilles tendons (stimulus turns on-off at 0.28 Hz), a ±1 mA binaural monopolar galvanic vestibular stimulus at 0.36 Hz, and a visual stimulus at 0.2 Hz during standing. The visual stimulus was presented at different amplitudes (0.2, 0.8 deg rotation about ankle axis) to measure: the change in gain (weighting) to vision, an intramodal effect; and a change in gain to vibration and galvanic vestibular stimulation, both intermodal effects. The results showed a clear intramodal visual effect, indicating a de-emphasis on vision when the amplitude of visual stimulus increased. At the same time, an intermodal visual-proprioceptive reweighting effect was observed with the addition of vibration, which is thought to change proprioceptive inputs at the ankles, forcing the nervous system to rely more on vision and vestibular modalities. Similar intermodal effects for visual-vestibular reweighting were observed, suggesting that vestibular information is not a “fixed” reference, but is dynamically adjusted in the sensor fusion process. This is the first time, to our knowledge, that the interplay between the three primary modalities for postural control has been clearly delineated, illustrating a central process that fuses these modalities for accurate estimates of self-motion.

title: Vestibular Contributions during Human Locomotor Tasks
abstract: This review explores vestibular contributions during dynamic tasks with the goal of identifying the underlying roles of vestibular information in task progression and balance control. Vestibular contributions to upper and lower body control during locomotor tasks were found.

title: Effects of galvanic vestibular stimulation during human walking
abstract: 1 To identify vestibular influences on human walking, galvanic vestibular stimulation was applied to normal adult subjects as they walked to a previously seen target. A transmastoidal step stimulus commenced as subjects started walking. With the eyes shut, the galvanic stimulus caused large turns towards the side with the anodal current. 2 Ability to perceive the trajectory of gait without visual cues was measured by guiding blindfolded subjects from one arbitrary point to another, either walking or seated in a wheelchair. On reaching a destination position and removing the blindfold, subjects pointed to indicate the starting position. Subjects made considerable errors in estimating the trajectory, but were equally accurate whether in the wheelchair or walking. 3 To determine the effects of vestibular stimulation on the perception of trajectory, the galvanic stimulus was applied to blindfolded subjects as they were guided from one point to another in the wheelchair. The vestibular stimulus produced an illusory shift in the trajectory travelled. This shift was towards the side with the cathode, i.e. in the opposite direction to the turn produced by the stimulus during walking. 4 We conclude that galvanic vestibular stimulation during walking causes subjects to turn from their planned trajectory. In part, this altered course may compensate for an altered perception of trajectory produced by the stimulus. However, altered perception of the vertical or the base of support, or direct vestibulo‐fugal influences on the leg muscles could contribute to the changes in gait.

title: Probing the human vestibular system with galvanic stimulation.
abstract: Galvanic vestibular stimulation (GVS) is a simple, safe, and specific way to elicit vestibular reflexes. Yet, despite a long history, it has only recently found popularity as a research tool and is rarely used clinically. The obstacle to advancing and exploiting GVS is that we cannot interpret the evoked responses with certainty because we do not understand how the stimulus acts as an input to the system. This paper examines the electrophysiology and anatomy of the vestibular organs and the effects of GVS on human balance control and develops a model that explains the observed balance responses. These responses are large and highly organized over all body segments and adapt to postural and balance requirements. To achieve this, neurons in the vestibular nuclei receive convergent signals from all vestibular receptors and somatosensory and cortical inputs. GVS sway responses are affected by other sources of information about balance but can appear as the sum of otolithic and semicircular canal responses. Electrophysiological studies showing similar activation of primary afferents from the otolith organs and canals and their convergence in the vestibular nuclei support this. On the basis of the morphology of the cristae and the alignment of the semicircular canals in the skull, rotational vectors calculated for every mode of GVS agree with the observed sway. However, vector summation of signals from all utricular afferents does not explain the observed sway. Thus we propose the hypothesis that the otolithic component of the balance response originates from only the pars medialis of the utricular macula.

title: Complementary mechanisms for upright balance during walking
abstract: Lateral balance is a critical factor in keeping the human body upright during walking. Two important mechanisms for balance control are the stepping strategy, in which the foot placement is changed in the direction of a sensed fall to modulate how the gravitational force acts on the body, and the lateral ankle strategy, in which the body mass is actively accelerated by an ankle torque. Currently, there is minimal evidence about how these two strategies complement one another to achieve upright balance during locomotion. We use Galvanic vestibular stimulation (GVS) to induce the sensation of a fall at heel-off during gait initiation. We found that young healthy adults respond to the illusory fall using both the lateral ankle strategy and the stepping strategy. The stance foot center of pressure (CoP) is shifted in the direction of the perceived fall by ≈2.5 mm, starting ≈247 ms after stimulus onset. The foot placement of the following step is shifted by ≈15 mm in the same direction. The temporal delay between these two mechanisms suggests that they independently contribute to upright balance during locomotion, potentially in a serially coordinated manner. Modeling results indicate that without the lateral ankle strategy, a much larger step width is required to maintain upright balance, suggesting that the small but early CoP shift induced by the lateral ankle strategy is critical for upright stability during locomotion. The relative importance of each mechanism and how neurological disorders may affect their implementation remain an open question.

title: No acute changes in postural control after soccer heading
abstract: Soccer heading has been proposed as a potential cause of cerebral dysfunction.  To examine the acute effects of two types of soccer heading on postural control.  Collegiate soccer players were randomly assigned to one of four groups: control, linear heading, simulated rotational heading, or rotational heading. Each subject completed a baseline postural stability assessment on day 1. On day 2 the same assessment was completed for the control subjects. The simulated rotational heading group completed a simulated heading drill before postural stability testing. The linear and rotational heading groups performed a heading drill with 20 balls at 88.71 km/h (55 mph), before postural stability testing. Separate one between (group), three within (surface, eyes, and day), mixed model, repeated measures analyses of variance were conducted on values for total sway and mean centre of pressure.  The mixed model analysis of variance of results showed no significant differences (p>0.05) for the interactions of interest for either variable. Results suggest no acute changes in measures of postural control in soccer players completing either a linear or rotational soccer heading drill of 20 balls at a fixed speed.  Non-significant interactions between surface, eyes, day, and group indicate that sensory interaction of the balance mechanism components are not be compromised by the heading drill. This research supports previous studies suggesting that there are no acute risks associated with routine soccer heading. A direct comparison between these findings and those suggesting long term chronic deficits, however, cannot be made. Other studies that report chronic cerebral deficits in soccer players may have resulted from factors other than soccer heading and warrant further examination.

title: Effect of an acute bout of soccer heading on postural control and self-reported concussion symptoms.
abstract: Our purpose was to determine if an acute bout of heading soccer balls adversely affected postural control and self-reported symptoms of cerebral concussion. Thirty-one college-aged soccer players were randomly placed into either a kicking group or a heading group. Subjects either kicked or headed 18 soccer balls over the course of 40 minutes. Subjects had their postural control assessed while standing on a force plate and completed a concussion symptoms checklist on three separate occasions: prior to, immediately following, and 24 hours after kicking or heading. There were no significant differences between the heading and kicking groups on the postural control measures prior to, immediately following, and 24 hours after kicking/heading. The heading group did, however, report significantly more concussion symptoms than the kicking group immediately after heading, but not 24 hours after heading. The number of previous concussions sustained by subjects did not influence the effects of heading. An acute bout of soccer heading appears to cause an increase in self-reported symptoms of cerebral concussion lasting less than 24 hours but no quantifiable deficits in postural control. Further research is needed to investigate the cumulative effects of soccer heading on postural control and other objective measures of brain function.

title: Postural Control Deficits After Repetitive Soccer Heading.
abstract: To determine the acute effects of repetitive soccer heading on postural control.



Prospective study; participants were divided into 2 groups: a soccer heading group and a control group.



Biomechanics laboratory.



One hundred sixty participants, including youth (age = 13.0 ± 0.8 years), high school (age = 17.2 ± 1.0 years), and collegiate (age = 20.2 ± 1.3 years) male and female soccer players, participated in this study.



Participants in the soccer heading group performed 12 soccer headers (initial velocity = 11.2 m/s). Postural control testing was performed both before (PRE) and immediately after (POST) the purposeful soccer headers. Control participants performed postural control testing PRE and POST a 15-minute wait period. During postural control testing, participants were asked to stand on the MobileMat (Tekscan Inc, Boston, Massachusetts) for two 2-minute intervals with their hands on their hips and their feet together with one eyes-open and one eyes-closed trial.



Using the center-of-pressure data, 95% area, sway velocity, and ApEn were calculated. Multilevel linear models were used to analyze the effects of age, sex, group, condition, and concussion history simultaneously.



Participants in the soccer heading group had significantly higher sway velocity POST than participants in the control group after controlling for age, sex, concussion history, condition, and PRE (t = -3.002; P = 0.003; 95% confidence interval, -0.482 to -0.100). There were no significant differences from PRE to POST for 95% area, M/L ApEn, and A/P ApEn.



Repetitive soccer heading does not affect most postural control measures, even among youth athletes. However, sway velocity increased after heading relative to control participants independent of age, sex, and concussion history.

title: Repetitive Head Impacts in Football Do Not Impair Dynamic Postural Control
abstract: The purpose of this study was to assess the effect of repetitive head impacts experienced by football players compared to noncontact athletes on dynamic postural control during both single-task (ST) and dual-task (DT) conditions.  Thirty-four football players wearing accelerometer instrumented helmets and 13 cheerleaders performed a dynamic postural control battery, consisting of ST and DT gait initiation, gait, and gait termination, both prior to and following the football season. A 2 (group) × 2 (time) repeated measures ANOVA compared performance across 32 dynamic postural outcomes. A linear regression was performed on postural control change scores with common head impact kinematics serving as the independent variables.  The football players experienced a mean of 538.1 ± 409.1 head impacts in the season with a mean linear acceleration of 27.8g ± 3.2g. There were no significant interactions for any of the ST or DT dynamic postural control tasks. There was a significant relationship between head impact kinematics and the lateral center of pressure displacement during the anticipatory postural adjustment phase (r2 = 0.26, P = 0.010) and transitional phase (r2 = 0.511, P = 0.042) during ST gait initiation. For both measures, the number of impacts exceeding 98g was the only significant predictor of decreased center of pressure displacement.  A single competitive football season did not adversely affect dynamic postural control when comparing football players to cheerleaders who do not experience repetitive head impacts. Furthermore, there were limited relationships with head impact kinematics suggesting that a single season of football does not adversely affect most outcome measures of instrumented dynamic postural control. These findings are consistent with most studies which fail to identify clinical differences related to repetitive head impacts.

title: Effects of Repetitive Head Impacts on a Concussion Assessment Battery.
abstract: The purpose of this study was to determine the relationship between repetitive head impacts (RHI) and clinical concussion assessments across a season among collegiate football (FB) and women's soccer (WSOC) players.



Fifteen male FB and 23 WSOC players participated in this study. Participants were included if they were medically cleared for unrestricted athletic participation. Participants were tested in a university athletic training room on two occasions: preseason (PRE) and postseason (POST). The outcome measures consisted of tandem gait (TG), Standardized Assessment of Concussion, Balance Error Scoring System, King-Devick (KD), clinical reaction time, and Immediate Post-Concussion Assessment and Cognitive Testing. Repetitive head impact during the season was quantified using the Head Impact Telemetry System (Simbex, NH) for FB and the Smart Impact Monitor (SIM; Triax Technologies, Norwalk, CT) for WSOC. Independent variables included total number of impacts, average magnitude of peak linear acceleration, cumulative linear exposure, and number of impacts ≥98g.



Results from direct-entry multiple regression analyses suggest significant associations between RHI and both visual memory (R = 0.670, F = 6.487, P = 0.002) and TG (R = 0.636, F = 3.841, P = 0.029) for WSOC and between RHI and KD (R = 0.756, F = 5.579, P = 0.013) for FB, whereby those with greater exposure performed worse. No other regression analyses within or across groups were significant.



These data suggest that RHI do not represent clinically meaningful changes on a multifaceted and multimodal concussion assessment battery. However, there may be subtle visual/vestibular impairments as observed by the associations between RHI and visual memory/TG among WSOC, RHI, and KD among FB.

title: Usefulness of some current balance tests for identifying individuals with disequilibrium due to vestibular impairments.
abstract: The goal of this study was to determine which of several clinical balance tests best identifies patients with vestibular disorders. We compared the scores of normals and patients on the Berg Balance Scale (Berg), Dynamic Gait Index (DGI), Timed Up and Go (TUG), Computerized Dynamic Posturography Sensory Organization Test (SOT), and a new obstacle avoidance test: the Functional Mobility Test (FMT). The study was performed in an out-patient balance laboratory at a tertiary care center. Subjects were 40 normal adults, and 40 adults with vestibular impairments. The main outcome measures were the sensitivity of tests to patients and specificity to normals. When adjusted for age the Berg, TUG, DGI and FMT had moderate sensitivity and specificity. SOT had moderately high sensitivity and specificity. SOT and FMT, combined, had high sensitivity and moderate specificity. Therefore, the kinds of tests of standing and walking balance that clinicians may use to screen patients for falling are not as good for screening for vestibular disorders as SOT. SOT combined with FMT is better. When screening patients for vestibular disorders, when objective diagnostic tests of the vestibular system, itself, are unavailable, tests of both standing and walking balance, together, give the most information about community-dwelling patients. These tests may also indicate the presence of sub-clinical balance problems in community-dwelling, asymptomatic adults.

title: Failure on the Foam Eyes Closed Test of Standing Balance Associated With Reduced Semicircular Canal Function in Healthy Older Adults
abstract: Standing on foam with eyes closed (FOEC) has been characterized as a measure of vestibular function; however, the relative contribution of vestibular function and proprioceptive function to the FOEC test has not been well described. In this study, the authors investigate the relationship between peripheral sensory systems (vestibular and proprioception) and performance on the FOEC test in a cohort of healthy adults.  A total of 563 community-dwelling healthy adults (mean age, 72.7 [SD, 12.6] years; range, 27 to 93 years) participating in the Baltimore Longitudinal Study of Aging were tested. Proprioceptive threshold (PROP) was evaluated with passive motion detection at the right ankle. Vestibulo-ocular reflex (VOR) gain was measured using video head impulses. Otolith function was measured with cervical and ocular vestibular-evoked myogenic potentials. Participants stood on FOEC for 40 sec while wearing BalanSens (BioSensics, LLC, Watertown, MA) to quantify center of mass sway area. A mixed-model multiple logistic regression was used to examine the odds of passing the FOEC test based on PROP, VOR, cervical vestibular-evoked myogenic potential, and ocular vestibular-evoked myogenic potential function in a multisensory model while controlling for age and gender.  The odds of passing the FOEC test decreased by 15% (p < 0.001) for each year of increasing age and by 8% with every 0.1 reduction in VOR gain (p = 0.025). Neither PROP nor otolith function was significantly associated with passing the FOEC test.  Failure to maintain balance during FOEC may serve as a proxy for rotational vestibular contributions to postural control. Semicircular canals are more sensitive to low-frequency motion than otoliths that may explain these relationships because standing sway is dominated by lower frequencies. Lower VOR gain and increased age independently decreased the odds of passing the test.

title: Adaptations of walking pattern on a compliant surface to regulate dynamic stability
abstract: Dynamic stability can be threatened by various travel surface changes that humans encounter on a daily basis. The central nervous system (CNS) must acquire appropriate information about upcoming surface changes and provide necessary proactive and reactive changes to maintain stability. The purpose of this study was to examine stability control by characterizing adaptations in step patterns, center of mass (COM) trajectory, and lower limb muscle activity when stepping onto and walking on a compliant surface. Eight young adults walked under two conditions: baseline ground walking and while walking on a large foam mat (compliant surface). Optotrak system was used to collect 3D-full body kinematics and electromyography was collected for the rectus femoris, biceps femoris, tibialis anterior, medial gastrocnemius, and soleus bilaterally. Vertical COM decreased on the compliant surface while medio-lateral COM was not affected. This lowering of the vertical COM peak would provide a more stable posture when walking on the surface. Toe trajectory during the swing phase was elevated to avoid tripping on the deformable compliant surface. Step width and length increased on the compliant surface which would increase base of support and provide better control of COM. Increases in gastrocnemius and soleus activity during push-off accounted for increases in step length seen on the compliant surface. Dynamic stability margin in the anterior–posterior direction demonstrated a constant overcompensation and subsequent correction in COM control. These proactive and reactive changes in motor patterns show how the CNS actively coordinates all body segments while traveling on a compliant surface in order to maximize stability.