Recent neuroimaging studies have suggested that repetitive subconcussive head impacts, even after only one sport season, may lead to pre- to post-season structural and functional alterations in male high school football athletes. However, data on female athletes are limited. In the current investigation, we aimed to (1) assess the longitudinal pre- to post-season changes in functional MRI (fMRI) of working memory and working memory performance, (2) quantify the association between the pre- to post-season change in fMRI of working memory and the exposure to head impact and working memory performance, and (3) assess whether wearing a neck collar designed to reduce intracranial slosh via mild compression of the jugular veins can ameliorate the changes in fMRI brain activation observed in the female high school athletes who did not wear collars after a full soccer season. A total of 48 female high school soccer athletes (age range: 14.00–17.97 years) were included in the study. These athletes were assigned to the non-collar group (n = 21) or to the collar group (n = 27). All athletes undewent MRI at both pre-season and post-season. In each session, a fMRI verbal N-Back task was used to engage working memory. A significant pre- to post-season increase in fMRI blood oxygen level dependent (BOLD) signal was demonstrated when performing the N-back working memory task in the non-collar group but not in the collar group, despite the comparable exposure to head impacts during the season between the two groups. The collar group demonstrated significantly smaller pre- to post-season change in fMRI BOLD signal than the non-collar group, suggesting a potential protective effect from the collar device. Significant correlations were also found between the pre- to post-season increase in fMRI brain activation and the decrease in task accuracy in the non-collar group, indicating an association between the compensatory mechanism in underlying neurophysiology and the alteration in the behavioral outcomes.
Get full access to this article
View all access options for this article.
References
1.
MooreR.D., LepineJ., and EllembergD. (2017). The independent influence of concussive and sub-concussive impacts on soccer players' neurophysiological and neuropsychological function. Int. J. Psychophysiol., 112, 22–30.
2.
BailesJ.E., PetragliaA.L., OmaluB. I., NaumanE., and TalavageT. (2013). Role of subconcussion in repetitive mild traumatic brain injury. J. Neurosurg., 119, 1235–1245.
3.
BazarianJ.J., ZhuT., ZhongJ., JanigroD., RozenE., RobertsA., JavienH., Merchant-BornaK., AbarB., and BlackmanE.G. (2014). Persistent, long-term cerebral white matter changes after sports-related repetitive head impacts. PLoS One, 8, e94734.
4.
DavenportE.M., WhitlowC.T., UrbanJ.E., EspelandM.A., JungY., RosenbaumD.A., GioiaG.A., PowersA.K., StitzelJ.D., and MaldjianJ.A. (2014). Abnormal white matter integrity related to head impact exposure in a season of high school varsity football. J. Neurotrauma, 31, 1617–1624.
5.
BahramiN., SharmaD., RosenthalS., DavenportE.M., UrbanJ.E., WagnerB., JungY., VaughanC.G., GioiaG.A., StitzelJ.D., WhitlowC.T., and MaldjianJ.A. (2016). Subconcussive head impact exposure and white matter tract changes over a single season of youth football. Radiology, 281, 919–926.
6.
MyerG.D., YuanW., Barber FossK.D., ThomasS., SmithD., LeachJ., KieferA.W., DicesareC., AdamsJ., GubanichP.J., KitchenK., SchneiderD.K., BraswellD., KruegerD., and AltayeM. (2016). Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br. J. Sports Med., 50, 1276–1285.
7.
YuanW., LeachJ., MaloneyT., AltayeM., SmithD., GubanichP., Barber-FossK., ThomasS., DiCesareC., KieferA., and MyerG.D. (2017). Neck collar with mild jugular vein compression ameliorates brain activation changes during a working memory task after a season of high school football. J Neurotrauma, 34, 2432–2444.
8.
SchmithorstV.J., WilkeM., DardzinskiB.J., and HollandS.K. (2002). Correlation of white matter diffusivity and anisotropy with age during childhood and adolescence: a cross-sectional diffusion-tensor MR imaging study. Radiology, 222, 212–218.
9.
SzeszkoP.R., VogelJ., AshtariM., MalhotraA.K., BatesJ., KaneJ.M., BilderR.M., FrevertT., and LimK. (2003). Sex differences in frontal lobe white matter microstructure: a DTI study. Neuroreport, 14, 2469–2473.
10.
Barnea-GoralyN., MenonV., EckertM., TammL., BammerR., KarchemskiyA., DantC.C., and ReissA.L. (2005). White matter development during childhood and adolescence: a cross-sectional diffusion tensor imaging study. Cereb. Cortex, 15, 1848–1854.
11.
McAllisterT.W., SaykinA.J., FlashmanL.A., SparlingM.B., JohnsonS.C., GuerinS.J., MamourianA.C., WeaverJ.B., and YanofskyN. (1999). Brain activation during working memory 1 month after mild traumatic brain injury: a functional MRI study. Neurology, 53, 1300–1308.
12.
McAllisterT.W., SparlingM.B., FlashmanL.A., GuerinS.J., MamourianA.C., and SaykinA.J. (2001). Differential working memory load effects after mild traumatic brain injury. Neuroimage, 14, 1004–1012.
13.
LevinH.S., HantenG., ZhangL., SwankP.R., Ewing-CobbsL., DennisM., BarnesM.A., MaxJ., SchacharR., ChapmanS.B., and HunterJ.V. (2004). Changes in working memory after traumatic brain injury in children. Neuropsychology, 18, 240–247.
14.
NewsomeM.R., ScheibelR.S., SteinbergJ.L., TroyanskayaM., SharmaR.G., RauchR.A., LiX., and LevinH.S. (2007). Working memory brain activation following severe traumatic brain injury. Cortex, 43, 95–111.
15.
NewsomeM.R., ScheibelR.S., HunterJ.V., WangZ.J., ChuZ., LiX., and LevinH.S. (2007b). Brain activation during working memory after traumatic brain injury in children. Neurocase, 13, 16–24.
16.
Sánchez-CarriónR., GómezP.V., JunquéC., Fernández-EspejoD., FalconC., BargallóN., Roig-RoviraT., Enseñat-CantallopsA., and BernabeuM. (2008a). Frontal hypoactivation on functional magnetic resonance imaging in working memory after severe diffuse traumatic brain injury. J. Neurotrauma, 25, 479–494.
17.
Sanchez-CarrionR., Fernandez-EspejoD., JunqueC., FalconC., BargalloN., RoigT., BernabeuM., TormosJ.M., and VendrellP. (2008b). A longitudinal fMRI study of working memory in severe TBI patients with diffuse axonal injury. Neuroimage, 43, 421–429.
18.
NaunheimR.S., StandevenJ., RichterC., and LewisL.M. (2000). Comparison of impact data in hockey, football, and soccer. J. Trauma, 48, 938–941.
19.
KirkendallD.T., JordanS.E., and GarrettW. E. (2001). Heading and head injuries in soccer. Sports Med. 31, 369–386.
20.
SpiottaA.M., BartschA.J., and BenzelE. C. (2012). Heading in soccer: dangerous play?. Neurosurgery, 70, 1–11.
21.
NaunheimR.S., RydenA., StandevenJ., GeninG., LewisL., ThompsonP., and BaylyP. (2003). Does soccer headgear attenuate the impact when heading a soccer ball?. Acad. Emerg. Med., 10, 85–90.
22.
WithnallC., ShewchenkoN., WonnacottM., and DvorakJ. (2005). Effectiveness of headgear in football. Br. J. Sports Med., 39, Suppl. 1, i40–i48.
23.
NiedfeldtM.W. (2011). Head injuries, heading, and the use of headgear in soccer. Curr. Sports Med. Rep., 10, 324–329.
24.
BensonB.W., McIntoshA.S., MaddocksD., HerringS.A., RafteryM., and DvorakJ. (2013). What are the most effective risk-reduction strategies in sport concussion?. Br. J. Sports. Med., 47, 321–326.
25.
BensonB.W., HamiltonG.M., MeeuwisseW.H., McCroryP., and DvorakJ. (2009). Is protective equipment useful in preventing concussion? A systematic review of the literature. Br. J. Sports. Med., 43, Suppl. 1, i56–i67.
26.
MyerG.D., YuanW., Barber FossK.D., SmithD., AltayeM., RechesA., LeachJ., KieferA.W., KhouryJ. C., WeissM., ThomasS., DicesareC., AdamsJ., GubanichP. J., GevaA., ClarkJ.F., MeehanW.P.3rd, MihalikJ.P., and KruegerD. (2016). The effects of external jugular compression applied during head impact exposure on longitudinal changes in brain neuroanatomical and neurophysiological biomarkers: a preliminary investigation. Front. Neurol., 7, 74.
27.
ReynoldsB.B., PatrieJ., HenryE.J., GoodkinH.P., BroshekD.K., WintermarkM., and DruzgalT.J. (2016). Practice type effects on head impact in collegiate football. J. Neurosurg., 124, 501–510.
SmithD.W., BailesJ.E., FisherJ.A., RoblesJ., TurnerR.C., and MillsJ.D. (2012). Internal jugular vein compression mitigates traumatic axonal injury in a rat model by reducing the intracranial slosh effect. Neurosurgery, 70, 740–746.
30.
FristonK.J., WilliamsS., HowardR., FrackowiakR.S., and TurnerR. (1996). Movement-related effects in fMRI time-series. Magn. Reson. Med., 35, 346–355.
31.
SmithS.M., and NicholsT. E. (2009). Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage, 44, 83–98.
32.
American Association of Neurological Surgeons. (2017). Sports-related head injury. http://www.aans.org/en/Patients/Neurosurgical-Conditions-and-Treatments/Sports-related-Head-Injury. (April22, 2017)
33.
TrebleA., HasanK.M., IftikharA., StuebingK.K., KramerL.A., Cox, JrC.S., SwankP.R., and Ewing-CobbsL. (2013). Working memory and corpus callosum microstructural integrity after pediatric traumatic brain injury: a diffusion tensor tractography study. J. Neurotrauma, 30, 1609–1619.
KontosA.P., BraithwaiteR., ChrismanS.P., McAllister-DeitrickJ., SymingtonL., ReevesV.L., and CollinsM.W. (2016). Meta-analytical review of the effects of football heading. Br. J. Sports. Med., 51, 1118–1124.
36.
BroglioS.P., EcknerJ.T., MartiniD., SosnoffJ.J., KutcherJ.S., and RandolphC. (2011). Cumulative head impact burden in high school football. J. Neurotrauma, 28, 2069–2078.
37.
UrbanJ.E., DavenportE.M., GolmanA.J., MaldjianJ.A., WhitlowC.T., PowersA.K., and StitzelJ.D. (2013). Head impact exposure in youth football: high school ages 14 to 18 years and cumulative impact analysis. Ann. Biomed. Eng., 41, 2474–2487.
38.
CortesN., LincolnA.E., MyerG.D., HepburnL., HigginsM., PutukianM., and CaswellS.V. (2017). Video analysis verification of head impact events measured by wearable sensors. Am. J. Sports. Med., 45, 2379–2387.
39.
PressJ.N., and RowsonS. (2017). Quantifying head impact exposure in collegiate women's soccer. Clin. J. Sport Med., 27, 104–110.
40.
WallisG., StokesM., CousijnH., WoolrichM., and NobreA.C. (2015). Frontoparietal and cingulo-opercular networks play dissociable roles in control of working memory. J. Cogn. Neurosci., 27, 2019–2034.
41.
WildeE.A., NewsomeM.R., BiglerE.D., PertabJ., MerkleyT.L., HantenG., ScheibelR.S., LiX., ChuZ., YallampalliR., HunterJ.V., and LevinH.S. (2011). Brain imaging correlates of verbal working memory in children following traumatic brain injury. Int. J. Psychophysiol., 82, 86–96.
42.
GordonE.M., StollstorffM., and VaidyaC.J. (2012). Using spatial multiple regression to identify intrinsic connectivity networks involved in working memory performance. Hum. Brain Mapp., 33, 1536–1552.
43.
RepovšG., and BarchD.M. (2012). Working memory related brain network connectivity in individuals with schizophrenia and their siblings. Front. Hum. Neurosci., 6, 137.
44.
PerlsteinW.M., ColeM.A., DemeryJ.A., SeignourelP.J., DixitN.K., LarsonM.J., and BriggsR.W. (2004). Parametric manipulation of working memory load in traumatic brain injury: behavioral and neural correlates. J. Int. Neuropsychol. Soc., 10, 724–741.
45.
NewsomeM.R., ScheibelR.S., SeignourelP.J., SteinbergJ.L., TroyanskayaM., LiX., and LevinH.S. (2009). Effects of methylphenidate on working memory in traumatic brain injury: a preliminary FMRI investigation. Brain Imaging Behav. 3, 298–305.
46.
SmitsM., DippelD.W., HoustonG.C., WielopolskiP.A., KoudstaalP.J., HuninkM.G., and van der LugtA. (2009). Postconcussion syndrome after minor head injury: brain activation of working memory and attention. Hum. Brain Mapp., 30, 2789–2803.
47.
KasaharaM., MenonD.K., SalmondC.H., OuttrimJ.G., TavaresJ.V., CarpenterT.A., PickardJ.D., SahakianB.J., and StamatakisE.A. (2011). Traumatic brain injury alters the functional brain network mediating working memory. Brain Inj. 25, 1170–1187.
48.
WylieG.R., FreemanK., ThomasA., ShpanerM., OKeefeM., WattsR., and NaylorM.R. (2015). Cognitive improvement after mild traumatic brain injury measured with functional neuroimaging during the acute period. PLoS One, 10, e0126110.
49.
ChenJ.K., JohnstonK.M., PetridesM., and PtitoA. (2008). Neural substrates of symptoms of depression following concussion in male athletes with persisting postconcussion symptoms. Arch. Gen. Psychiatry, 65, 81–89.
50.
ChenJ.K., JohnstonK.M., PetridesM., and PtitoA. (2008b). Recovery from mild head injury in sports: evidence from serial functional magnetic resonance imaging studies in male athletes. Clin. J. Sport Med., 18, 241–247.
51.
LovellM.R., PardiniJ.E., WellingJ., CollinsM.W., BakalJ., LazarN., RoushR., EddyW.F., and BeckerJ.T. (2007). Functional brain abnormalities are related to clinical recovery and time to return-to-play in athletes. Neurosurgery, 61, 352–359.
52.
PardiniJ.E., PardiniD.A., BeckerJ.T., DunfeeK.L., EddyW.F., LovellM.R., and WellingJ.S. (2010). Postconcussive symptoms are associated with compensatory cortical recruitment during a working memory task. Neurosurgery, 67, 1020–1028.
53.
DettwilerA., MurugavelM., PutukianM., CubonV., FurtadoJ., and OshersonD. (2014). Persistent differences in patterns of brain activation after sports-related concussion: a longitudinal functional magnetic resonance imaging study. J. Neurotrauma, 31, 180–188.
54.
WestfallD.R., WestJ.D., BaileyJ.N., ArnoldT.W., KerseyP.A., SaykinA.J., and McDonaldB.C. (2015). Increased brain activation during working memory processing after pediatric mild traumatic brain injury (mTBI). J. Pediatr. Rehabil. Med., 8, 297–308.
55.
TalavageT.M., NaumanE.A., BreedloveE.L., YorukU., DyeA.E., MorigakiK.E., FeuerH., and LeverenzL.J. (2014). Functionally-detected cognitive impairment in high school football players without clinically-diagnosed concussion. J. Neurotrauma, 31, 327–338.
56.
ShenkT.E., RobinsonM.E., SvaldiD.O., AbbasK., BreedloveK.M., LeverenzL.J., NaumanE.A., and TalavageT.M. (2015). FMRI of visual working memory in high school football players. Dev. Neuropsychol., 40, 63–68.
57.
RobinsonM.E., ShenkT.E., BreedloveE.L., LeverenzL.J., NaumanE.A., and TalavageT.M. (2015). The role of location of subconcussive head impacts in FMRI brain activation change. Dev. Neuropsychol., 40, 74–79.
58.
NaumanE.A., BreedloveK.M., BreedloveE.L., TalavageT.M., RobinsonM.E., and LeverenzL.J. (2015). Post-season neurophysiological deficits assessed by impact and fmri in athletes competing in American football. Dev. Neuropsychol., 40, 85–91.
59.
MaruishiM., MiyataniM., NakaoT., and MuranakaH. (2007). Compensatory cortical activation during performance of an attention task by patients with diffuse axonal injury: a functional magnetic resonance imaging study. J. Neurol. Neurosurg. Psychiatry, 78, 168–173.
LejbakL., CrossleyM., and VrbancicM. (2011). A male advantage for spatial and object but not verbal working memory using the n-back task. Brain Cogn. 76, 191–196.
62.
MillerD.I., and HalpernD.F. (2014). The new science of cognitive sex differences. Trends Cogn. Sci., 18, 37–45.
63.
IngalhalikarM., SmithA., ParkerD., SatterthwaiteT.D., ElliottM.A., RuparelK., HakonarsonH., GurR.E., GurR.C., and VermaR. (2014). Sex differences in the structural connectome of the human brain. Proc. Natl. Acad. Sci. U. S. A., 111, 823–828.
64.
OwenA.M., McMillanK.M., LairdA.R., and BullmoreE. (2005). N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp. 25, 46–59.
65.
CallicottJ.H., MattayV.S., BertolinoA., FinnK., CoppolaR., FrankJ.A., GoldbergT.E., and WeinbergerD.R. (1999). Physiological characteristics of capacity constraints in working memory as revealed by functional MRI. Cereb. Cortex, 9, 20–26.
66.
VeltmanD.J., RomboutsS.A., and DolanR.J. (2003). Maintenance versus manipulation in verbal working memory revisited: an fMRI study. Neuroimage, 18, 247–256.
67.
LiptonM.L., KimN., ZimmermanM.E., KimM., StewartW.F., BranchC.A., and LiptonR.B. (2013). Soccer heading is associated with white matter microstructural and cognitive abnormalities. Radiology, 268, 850–857.
68.
BerzK., DivineJ., FossK.B., HeyR., FordK.R., and MyerG.D. (2013). Sex-specific differences in the severity of symptoms and recovery rate following sports-related concussion in young athletes. Phys. Sportsmed., 41, 58–63.
69.
CovassinT., MoranR., and ElbinR.J. (2016). Sex differences in reported concussion injury rates and time loss from participation: an update of the National Collegiate Athletic Association Injury Surveillance Program from 2004–2005 through 2008–2009. J. Athl. Train., 51, 189–194.
70.
KhodaeeM., CurrieD.W., AsifI.M., and ComstockR.D. (2016). Nine-year study of US high school soccer injuries: data from a national sports injury surveillance programme. Br. J. Sports Med., 51, 185–193.
71.
SandelN.K., SchatzP., GoldbergK.B., and LazarM. (2016). Sex-based differences in cognitive deficits and symptom reporting among acutely concussed adolescent lacrosse and soccer players. Am. J. Sports Med., 45, 937–944.
72.
JanssenI., HeymsfieldS.B., WangZ., and RossR. (2000). Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J. Appl. Physiol., 89, 81–88.
73.
TierneyR.T., SitlerM.R., SwanikC.B., SwanikK.A., HigginsM., and TorgJ. (2005). Gender differences in head-neck segment dynamic stabilization during head acceleration. Med. Sci. Sports. Exerc., 37, 272–279.
74.
CollinsC.L., FletcherE.N., FieldsS.K., KluchuroskyL., RohrkemperM.K., ComstockR.D.,n and CantuR.C. (2014). Neck strength: a protective factor reducing risk for concussion in high school sports. J. Prim. Prev., 35, 309–319.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
