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Experimental Brain Research

, Volume 237, Issue 5, pp 1267–1278 | Cite as

Quadriceps muscle function following anterior cruciate ligament reconstruction: systemic differences in neural and morphological characteristics

  • Adam S. LepleyEmail author
  • Dustin R. Grooms
  • Julie P. Burland
  • Steven M. Davi
  • Jeffrey M. Kinsella-Shaw
  • Lindsey K. Lepley
Research Article

Abstract

Quadriceps muscle dysfunction is common following anterior cruciate ligament reconstruction (ACLR). Data considering the diversity of neural changes, in-concert with morphological adaptations of the quadriceps muscle, are lacking. We investigated bilateral differences in neural and morphological characteristics of the quadriceps muscle in ACLR participants (n = 11, month post-surgery: 69.4 ± 22.4) compared to controls matched by sex, age, height, weight, limb dominance, and activity level. Spinal reflex excitability was assessed using Hoffmann reflexes (H:M); corticospinal excitability was quantified via active motor thresholds (AMT) and motor-evoked potentials (MEP) using transcranial magnetic stimulation. Cortical activation was assessed using a knee flexion/extension task with functional magnetic resonance imaging (fMRI). Muscle volume was quantified using structural MRI. Muscle strength and patient-reported outcomes were also collected. 2 × 2 RM ANOVAs were used to evaluate group differences. Smaller quadriceps muscle volume (total volume, rectus femoris, vastus medialis, and intermedius) and lower strength were detected compared to contralateral and control limbs. Individuals with ACLR reported higher levels of pain and fear and lower levels of knee function compared to controls. No differences were observed for H:M. ACLR individuals demonstrated higher AMT bilaterally and smaller MEPs in the injured limb, compared to the controls. ACLR participants demonstrated greater activation in frontal lobe areas responsible for motor and pain processing compared to controls, which were associated with self-reported pain. Our results suggest that individuals with ACLR demonstrate systemic neural differences compared to controls, which are observed concurrently with smaller quadriceps muscle volume, quadriceps muscle weakness, and self-reported dysfunction.

Keywords

Functional magnetic resonance imaging Transcranial magnetic stimulation Muscle atrophy Cortical activation Quadriceps weakness 

Notes

Acknowledgements

The authors would like to acknowledge Elisa Medeiros (MRI services manager, University of Connecticut’s Brain Imaging Research Center) for their assistance and support in MRI data collection and design. This research was supported by a Faculty Seed Grant from the University of Connecticut’s Brain Imaging Research Center (BIRC).

References

  1. Ardern CL, Webster KE, Taylor NF, Feller JA (2011) Return to sport following anterior cruciate ligament reconstruction surgery: a systematic review and meta-analysis of the state of play. Br J Sports Med 45:596–606.  https://doi.org/10.1136/bjsm.2010.076364 CrossRefGoogle Scholar
  2. Baumeister J, Reinecke K, Weiss M (2008) Changed cortical activity after anterior cruciate ligament reconstruction in a joint position paradigm: an EEG study. Scand J Med Sci Sports 18:473–484.  https://doi.org/10.1111/j.1600-0838.2007.00702.x CrossRefGoogle Scholar
  3. Baumeister J, Reinecke K, Schubert M, Weiss M (2011) Altered electrocortical brain activity after ACL reconstruction during force control. J Orthop Res 29:1383–1389.  https://doi.org/10.1002/jor.21380 CrossRefGoogle Scholar
  4. Beckmann CF, Jenkinson M, Smith SM (2003) General multilevel linear modeling for group analysis in. FMRI Neuroimage 20:1052–1063.  https://doi.org/10.1016/S1053-8119(03)00435-X CrossRefGoogle Scholar
  5. Chmielewski TL, Jones D, Day T, Tillman SM, Lentz TA, George SZ (2008) The association of pain and fear of movement/reinjury with function during anterior cruciate ligament reconstruction rehabilitation. J Orthop Sports Phys Therapy 38:746–753.  https://doi.org/10.2519/jospt.2008.2887 CrossRefGoogle Scholar
  6. Del Percio C et al (2009) “Neural efficiency” of athletes’ brain for upright standing: a high-resolution EEG study. Brain Res Bull 79:193–200.  https://doi.org/10.1016/j.brainresbull.2009.02.001 CrossRefGoogle Scholar
  7. Dunst B et al (2014) Neural efficiency as a function of task demands. Intelligence 42:22–30.  https://doi.org/10.1016/j.intell.2013.09.005 CrossRefGoogle Scholar
  8. Flanigan DC, Everhart JS, Pedroza A, Smith T, Kaeding CC (2013) Fear of reinjury (kinesiophobia) and persistent knee symptoms are common factors for lack of return to sport after anterior cruciate ligament reconstruction. Arthrosc J Arthrosc Relat Surg 29:1322–1329.  https://doi.org/10.1016/j.arthro.2013.05.015 CrossRefGoogle Scholar
  9. Gao YJ, Ren WH, Zhang YQ, Zhao ZQ (2004) Contributions of the anterior cingulate cortex and amygdala to pain- and fear-conditioned place avoidance in rats. Pain 110:343–353.  https://doi.org/10.1016/j.pain.2004.04.030 CrossRefGoogle Scholar
  10. Griffin LY et al (2006) Understanding and preventing noncontact anterior cruciate ligament injuries—a review of the Hunt Valley II Meeting, January 2005. Am J Sport Med 34:1512–1532.  https://doi.org/10.1177/0363546506286866 CrossRefGoogle Scholar
  11. Grooms DR, Page SJ, Onate JA (2015) Brain activation for knee movement measured days before second anterior cruciate ligament injury: neuroimaging in musculoskeletal medicine. J Athl Train 50:1005–1010.  https://doi.org/10.4085/1062-6050-50.10.02 CrossRefGoogle Scholar
  12. Grooms DR, Page SJ, Nichols-Larsen DS, Chaudhari AM, White SE, Onate JA (2017) Neuroplasticity associated with anterior cruciate ligament reconstruction. J Orthop Sports Phys Ther 47:180–189.  https://doi.org/10.2519/jospt.2017.7003 CrossRefGoogle Scholar
  13. Groppa S et al (2012) A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 123:858–882.  https://doi.org/10.1016/j.clinph.2012.01.010 CrossRefGoogle Scholar
  14. Gumucio JP, Sugg KB, Sibilsky Enselman ER, Konja AC, Eckhardt LR, Bedi A, Mendias CL (2018) Anterior cruciate ligament tear induces a sustained loss of muscle fiber force production. Muscle Nerve.  https://doi.org/10.1002/mus.26075 Google Scholar
  15. Harkey M, McLeod M, Terada M, Gribble P, Pietrosimone B (2015) Quadratic association between corticomotor and spinal-reflexive excitability and self-reported disability in participants with chronic ankle instability. J Sport Rehabil  https://doi.org/10.1123/jsr.2014-0282 Google Scholar
  16. Heroux ME, Tremblay F (2006) Corticomotor excitability associated with unilateral knee dysfunction secondary to anterior cruciate ligament injury. Knee Surg Sport Tr A 14:823–833  https://doi.org/10.1007/S00167-006-0063-4 CrossRefGoogle Scholar
  17. Heun R, Jessen F, Klose U, Erb M, Granath DO, Grodd W (2000) Response-related fMRI analysis during encoding and retrieval revealed differences in cerebral activation by retrieval success. Psychiatry Res 99:137–150CrossRefGoogle Scholar
  18. Hiemstra LA, Webber S, MacDonald PB, Kriellaars DJ (2007) Contralateral limb strength deficits after anterior cruciate ligament reconstruction using a hamstring tendon graft. Clin Biomech 22:543–550.  https://doi.org/10.1016/j.clinbiomech.2007.01.009 CrossRefGoogle Scholar
  19. Higgins LD, Taylor MK, Park D, Ghodadra N, Marchant M, Pietrobon R, Cook C (2007) Reliability and validity of the International Knee Documentation Committee (IKDC) subjective knee form. Joint Bone Spine 74:594–599.  https://doi.org/10.1016/j.jbspin.2007.01.036 CrossRefGoogle Scholar
  20. Hoffman M, Koceja DM (2000) Hoffmann reflex profiles and strength ratios in postoperative anterior cruciate ligament reconstruction patients. Int J Neurosci 104:17–27CrossRefGoogle Scholar
  21. Hoffstaedter F et al (2014) The role of anterior midcingulate cortex in cognitive motor control: evidence from functional connectivity analyses. Hum Brain Mapp 35:2741–2753.  https://doi.org/10.1002/hbm.22363 CrossRefGoogle Scholar
  22. Hopkins J, Ingersoll CD (2000) Arthrogenic muscle inhibition: a limiting factor in joint rehabilitation. J Sport Rehabil 9:135–159CrossRefGoogle Scholar
  23. Hopkins JT, Ingersoll CD, Edwards JE, Cordova ML (2000) Changes in soleus motoneuron pool excitability after artificial knee joint effusion. Arch Phys Med Rehabil 81:1199–1203.  https://doi.org/10.1053/apmr.2000.6298 CrossRefGoogle Scholar
  24. Hopkins J, Ingersoll C, Krause B, Edwards J, Cordova M (2001a) Effect of knee joint effusion on quadriceps and soleus motoneuron pool excitability. Med Sci Sports Exerc 33:123–126CrossRefGoogle Scholar
  25. Hopkins JT, Ingersoll CD, Krause BA, Edwards JE, Cordova ML (2001b) Effect of knee joint effusion on quadriceps and soleus motoneuron pool excitability. Med Sci Sport Exer 33:123–126CrossRefGoogle Scholar
  26. Hoxie SC, Dobbs RE, Dahm DL, Trousdale RT (2008) Total knee arthroplasty after anterior cruciate ligament reconstruction. J Arthroplasty 23:1005–1008.  https://doi.org/10.1016/J.Arth.2007.08.017 CrossRefGoogle Scholar
  27. Ingersoll CD, Grindstaff TL, Pietrosimone BG, Hart JM (2008) Neuromuscular consequences of anterior cruciate ligament injury. Clin Sports Med 27:383–404.  https://doi.org/10.1016/j.csm.2008.03.004 CrossRefGoogle Scholar
  28. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841CrossRefGoogle Scholar
  29. Kapreli E et al (2009) Anterior cruciate ligament deficiency causes brain plasticity: a functional MRI study. Am J Sports Med 37:2419–2426.  https://doi.org/10.1177/0363546509343201 CrossRefGoogle Scholar
  30. Kittelson AJ, Thomas AC, Kluger BM, Stevens-Lapsley JE (2014) Corticospinal and intracortical excitability of the quadriceps in patients with knee osteoarthritis. Exp Brain Res 232:3991–3999.  https://doi.org/10.1007/s00221-014-4079-6 CrossRefGoogle Scholar
  31. Konishi Y, Ikeda K, Nishino A, Sunaga M, Aihara Y, Fukubayashi T (2007) Relationship between quadriceps femoris muscle volume and muscle torque after anterior cruciate ligament repair. Scand J Med Sci Sports 17:656–661.  https://doi.org/10.1111/j.1600-0838.2006.00619.x CrossRefGoogle Scholar
  32. Krishnan C, Williams GN (2011) Factors explaining chronic knee extensor strength deficits after ACL reconstruction. J Orthop Res 29:633–640.  https://doi.org/10.1002/Jor.21316 CrossRefGoogle Scholar
  33. Kuenze C, Blemker SS, Hart JM (2016) Quadriceps function relates to muscle size following ACL reconstruction. J Orthop Res.  https://doi.org/10.1002/jor.23166 Google Scholar
  34. Lepley AS, Ericksen HM, Sohn DH, Pietrosimone BG (2014) Contributions of neural excitability and voluntary activation to quadriceps muscle strength following anterior cruciate ligament reconstruction. Knee 21:736–742.  https://doi.org/10.1016/j.knee.2014.02.008 CrossRefGoogle Scholar
  35. Lepley AS, Bahhur NO, Murray AM, Pietrosimone BG (2015a) Quadriceps corticomotor excitability following an experimental knee joint effusion. Knee Surg Sports Traumatol Arthrosc 23:1010–1017.  https://doi.org/10.1007/s00167-013-2816-1 CrossRefGoogle Scholar
  36. Lepley AS, Gribble PA, Thomas AC, Tevald MA, Sohn DH, Pietrosimone BG (2015b) Quadriceps neural alterations in anterior cruciate ligament reconstructed patients: a 6-month longitudinal investigation. Scand J Med Sci Sports.  https://doi.org/10.1111/sms.12435 Google Scholar
  37. Lindstrom M, Strandberg S, Wredmark T, Fellander-Tsai L, Henriksson M (2013) Functional and muscle morphometric effects of ACL reconstruction. A prospective CT study with 1 year follow-up. Scand J Med Sci Sports 23:431–442.  https://doi.org/10.1111/j.1600-0838.2011.01417.x CrossRefGoogle Scholar
  38. Livingston SC, Ingersoll CD (2008) Intra-rater reliability of a transcranial magnetic stimulation technique to obtain motor evoked potentials. Int J Neurosci 118:239–256CrossRefGoogle Scholar
  39. Lohmander LS, Ostenberg A, Englund M, Roos H (2004) High prevalence of knee osteoarthritis, pain, and functional limitations in female soccer players twelve years after anterior cruciate ligament injury. Arthritis Rheum 50:3145–3152.  https://doi.org/10.1002/art.20589 CrossRefGoogle Scholar
  40. Lohse KR, Wadden K, Boyd LA, Hodges NJ (2014) Motor skill acquisition across short and long time scales: a meta-analysis of neuroimaging data. Neuropsychologia 59:130–141.  https://doi.org/10.1016/j.neuropsychologia.2014.05.001 CrossRefGoogle Scholar
  41. Luc-Harkey BA et al (2017) Greater intracortical inhibition associates with lower quadriceps voluntary activation in individuals with ACL reconstruction. Exp Brain Res 235:1129–1137.  https://doi.org/10.1007/s00221-017-4877-8 CrossRefGoogle Scholar
  42. Maden-Wilkinson TM, Degens H, Jones DA, McPhee JS (2013) Comparison of MRI and DXA to measure muscle size and age-related atrophy in thigh muscles. J Musculoskelet Neuronal Interact 13:320–328Google Scholar
  43. Mather RC 3rd et al (2013) Societal and economic impact of anterior cruciate ligament tears. J Bone Jt Surg Am 95:1751–1759.  https://doi.org/10.2106/JBJS.L.01705 CrossRefGoogle Scholar
  44. Mirkov DM, Knezevic OM, Maffiuletti NA, Kadija M, Nedeljkovic A, Jaric S (2017) Contralateral limb deficit after ACL-reconstruction: an analysis of early and late phase of rate of force development. J Sports Sci 35:435–440.  https://doi.org/10.1080/02640414.2016.1168933 CrossRefGoogle Scholar
  45. Molnar-Szakacs I, Iacoboni M, Koski L, Mazziotta JC (2005) Functional segregation within pars opercularis of the inferior frontal gyrus: evidence from fMRI studies of imitation and action observation. Cereb Cortex 15:986–994.  https://doi.org/10.1093/cercor/bhh199 CrossRefGoogle Scholar
  46. Morse CI, Degens H, Jones DA (2007) The validity of estimating quadriceps volume from single MRI cross-sections in young men. Eur J Appl Physiol 100:267–274.  https://doi.org/10.1007/s00421-007-0429-4 CrossRefGoogle Scholar
  47. Needle AR, Lepley AS, Grooms DR (2017) Central nervous system adaptation after ligamentous injury: a summary of theories, evidence, and clinical interpretation. Sports Med 47:1271–1288.  https://doi.org/10.1007/s40279-016-0666-y CrossRefGoogle Scholar
  48. Neuman P, Englund M, Kostogiannis I, Friden T, Roos H, Dahlberg LE (2008) Prevalence of tibiofemoral osteoarthritis 15 years after nonoperative treatment of anterior cruciate ligament injury: a prospective cohort study. Am J Sports Med 36:1717–1725.  https://doi.org/10.1177/0363546508316770 CrossRefGoogle Scholar
  49. Noehren B, Andersen A, Hardy P, Johnson DL, Ireland ML, Thompson KL, Damon B (2016) Cellular and morphological alterations in the vastus lateralis muscle as the result of ACL injury and reconstruction. J Bone Jt Surg Am 98:1541–1547.  https://doi.org/10.2106/JBJS.16.00035 CrossRefGoogle Scholar
  50. Norte GE, Pietrosimone BG, Hart JM, Hertel J, Ingersoll CD (2010) Relationship between transcranial magnetic stimulation and percutaneous electrical stimulation in determining the quadriceps central activation ratio. Am J Phys Med Rehabil 89:986–996CrossRefGoogle Scholar
  51. Norte GE, Hertel JN, Saliba SA, Diduch DR, Hart JM (2018a) Quadriceps and patient-reported function in ACL-Reconstructed patients: a principal component analysis. J Sport Rehabil:1–9  https://doi.org/10.1123/jsr.2017-0080
  52. Norte GE, Knaus KR, Kuenze C, Handsfield GG, Meyer CH, Blemker SS, Hart JM (2018b) MRI-based assessment of lower-extremity muscle volumes in patients before and after ACL reconstruction. J Sport Rehabil 27:201–212.  https://doi.org/10.1123/jsr.2016-0141 CrossRefGoogle Scholar
  53. Palmieri RM, Ingersoll CD (2005) Intersession reliability of a protocol to assess reflex activation history in the vastus medialis. Int J Neurosci 115:735–740.  https://doi.org/10.1080/00207450590523404 CrossRefGoogle Scholar
  54. Palmieri RM et al (2004a) Arthrogenic muscle response to a simulated ankle joint effusion. Br J Sports Med 38:26–30.  https://doi.org/10.1136/Bjsm.2002.001677 CrossRefGoogle Scholar
  55. Palmieri RM, Tom JA, Edwards JE, Weltman A, Saliba EN, Mistry DJ, Ingersoll CD (2004b) Arthrogenic muscle response induced by an experimental knee joint effusion is mediated by pre- and post-synaptic spinal mechanisms. J Electromyogr Kines 14:631–640.  https://doi.org/10.1016/J.Jelekin.2004.06.002 CrossRefGoogle Scholar
  56. Palmieri-Smith RM, Kreinbrink J, Ashton-Miller JA, Wojtys EM (2007) Quadriceps inhibition induced by an experimental knee joint effusion affects knee joint mechanics during a single-legged drop landing. Am J Sport Med 35:1269–1275.  https://doi.org/10.1177/0363546506296417 CrossRefGoogle Scholar
  57. Palmieri-Smith RM, Thomas AC, Wojtys EM (2008) Maximizing quadriceps strength after ACL reconstruction. Clin Sport Med 27:405–424.  https://doi.org/10.1016/J.Csm.2008.02.001 CrossRefGoogle Scholar
  58. Paterno MV, Schmitt LC, Ford KR, Rauh MJ, Myer GD, Huang B, Hewett TE (2010) Biomechanical measures during landing and postural stability predict second anterior cruciate ligament injury after anterior cruciate ligament reconstruction and return to sport. Am J Sports Med 38:1968–1978.  https://doi.org/10.1177/0363546510376053 CrossRefGoogle Scholar
  59. Paterno MV, Rauh MJ, Schmitt LC, Ford KR, Hewett TE (2012) Incidence of contralateral and ipsilateral anterior cruciate ligament (ACL) injury after primary ACL reconstruction and return to sport. Clin J Sport Med 22:116–121.  https://doi.org/10.1097/JSM.0b013e318246ef9e CrossRefGoogle Scholar
  60. Pietrosimone BG, Gribble PA (2012) Chronic ankle instability and corticomotor excitability of the fibularis longus muscle. J Athl Train 47:621–626.  https://doi.org/10.4085/1062-6050-47.6.11 CrossRefGoogle Scholar
  61. Pietrosimone BG, McLeod MM, Lepley AS (2012) A theoretical framework for understanding neuromuscular response to lower extremity joint injury. Sports Health 4:31–35.  https://doi.org/10.1177/1941738111428251 CrossRefGoogle Scholar
  62. Pietrosimone BG, Lepley AS, Ericksen HM, Gribble PA, Levine J (2013) Quadriceps strength and corticospinal excitability as predictors of disability after anterior cruciate ligament reconstruction. J Sport Rehabil 22:1–6CrossRefGoogle Scholar
  63. Pietrosimone BG, Lepley AS, Ericksen HM, Clements A, Sohn DH, Gribble PA (2015) Neural excitability alterations after anterior cruciate ligament reconstruction. J Athl Train 50:665–674.  https://doi.org/10.4085/1062-6050-50.1.11 CrossRefGoogle Scholar
  64. Pietrosimone B et al (2016) Quadriceps strength predicts self-reported function post-ACL reconstruction. Med Sci Sports Exerc 48:1671–1677.  https://doi.org/10.1249/MSS.0000000000000946 CrossRefGoogle Scholar
  65. Rae CL, Hughes LE, Anderson MC, Rowe JB (2015) The prefrontal cortex achieves inhibitory control by facilitating subcortical motor pathway connectivity. J Neurosci 35:786–794.  https://doi.org/10.1523/JNEUROSCI.3093-13.2015 CrossRefGoogle Scholar
  66. Rice DA, McNair PJ, Lewis GN, Dalbeth N (2014) Quadriceps arthrogenic muscle inhibition: the effects of experimental knee joint effusion on motor cortex excitability. Arthritis Res Ther 16:502.  https://doi.org/10.1186/s13075-014-0502-4 CrossRefGoogle Scholar
  67. Rio E, Kidgell D, Moseley GL, Cook J (2015) Elevated corticospinal excitability in patellar tendinopathy compared with other anterior knee pain or no pain Scandinavian. J Med Sci Sports.  https://doi.org/10.1111/sms.12538 Google Scholar
  68. Rosenthal MD, Moore JH, Stoneman PD, DeBerardino TM (2009) Neuromuscular excitability changes in the vastus medialis following anterior cruciate ligament reconstruction. Electromyogr Clin Neurophysiol 49:43–51Google Scholar
  69. Ruby P, Sirigu A, Decety J (2002) Distinct areas in parietal cortex involved in long-term and short-term action planning: a. PET investigation Cortex 38:321–339CrossRefGoogle Scholar
  70. Salavati M, Akhbari B, Mohammadi F, Mazaheri M, Khorrami M (2011) Knee injury and osteoarthritis outcome score (KOOS); reliability and validity in competitive athletes after anterior cruciate ligament reconstruction. Osteoarthritis Cartilage 19:406–410.  https://doi.org/10.1016/j.joca.2011.01.010 CrossRefGoogle Scholar
  71. Silva JMS, Alabarse PVG, Teixeira VON, Freitas EC, de Oliveira FH, Chakr R, Xavier RM (2018) Muscle wasting in osteoarthritis model induced by anterior cruciate ligament transection. PLoS One 13:e0196682.  https://doi.org/10.1371/journal.pone.0196682 CrossRefGoogle Scholar
  72. Smith SM (2002) Fast robust automated brain extraction. Hum Brain Mapp 17:143–155.  https://doi.org/10.1002/hbm.10062 CrossRefGoogle Scholar
  73. Smith SM et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219CrossRefGoogle Scholar
  74. Strandberg S, Lindstrom M, Wretling ML, Aspelin P, Shalabi A (2013) Muscle morphometric effect of anterior cruciate ligament injury measured by computed tomography: aspects on using non-injured leg as control. BMC Musculoskelet Disord 14:150.  https://doi.org/10.1186/1471-2474-14-150 CrossRefGoogle Scholar
  75. Thomas AC, Wojtys EM, Brandon C, Palmieri-Smith RM (2016) Muscle atrophy contributes to quadriceps weakness after anterior cruciate ligament reconstruction. J Sci Med Sport 19:7–11.  https://doi.org/10.1016/j.jsams.2014.12.009 CrossRefGoogle Scholar
  76. Tourville TW, Jarrell KM, Naud S, Slauterbeck JR, Johnson RJ, Beynnon BD (2014) Relationship between isokinetic strength and tibiofemoral joint space width changes after anterior cruciate ligament reconstruction. Am J Sports Med 42:302–311.  https://doi.org/10.1177/0363546513510672 CrossRefGoogle Scholar
  77. Wenderoth N, Debaere F, Sunaert S, Swinnen SP (2005) The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour. Eur J Neurosci 22:235–246.  https://doi.org/10.1111/j.1460-9568.2005.04176.x CrossRefGoogle Scholar
  78. Wiggins AJ, Grandhi RK, Schneider DK, Stanfield D, Webster KE, Myer GD (2016) Risk of secondary injury in younger athletes after anterior cruciate ligament reconstruction: a systematic review and meta-analysis. Am J Sports Med.  https://doi.org/10.1177/0363546515621554 Google Scholar
  79. Williams GN, Buchanan TS, Barrance PJ, Axe MJ, Snyder-Mackler L (2005a) Quadriceps weakness, atrophy, and activation failure in predicted noncopers after anterior cruciate ligament injury. Am J Sports Med 33:402–407CrossRefGoogle Scholar
  80. Williams GN, Snyder-Mackler L, Barrance PJ, Buchanan TS (2005b) Quadriceps femoris muscle morphology and function after ACL injury: a differential response in copers versus non-copers. J Biomech 38:685–693.  https://doi.org/10.1016/j.jbiomech.2004.04.004 CrossRefGoogle Scholar
  81. Woodward TS, Ruff CC, Ngan ET (2006) Short- and long-term changes in anterior cingulate activation during resolution of task-set competition. Brain Res 1068:161–169.  https://doi.org/10.1016/j.brainres.2005.10.094 CrossRefGoogle Scholar
  82. Woolrich M (2008) Robust group analysis using outlier inference. Neuroimage 41:286–301.  https://doi.org/10.1016/j.neuroimage.2008.02.042 CrossRefGoogle Scholar
  83. Woolrich MW, Ripley BD, Brady M, Smith SM (2001a) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14:1370–1386.  https://doi.org/10.1006/nimg.2001.0931 CrossRefGoogle Scholar
  84. Woolrich MW, Ripley BD, Brady M, Smith SM (2001b) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14:1370–1386CrossRefGoogle Scholar
  85. Woolrich MW, Behrens TE, Beckmann CF, Jenkinson M, Smith SM (2004) Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21:1732–1747.  https://doi.org/10.1016/j.neuroimage.2003.12.023 CrossRefGoogle Scholar
  86. Worsley KJ (2001) Statistical analysis of activation images. Ch 14, in Functional MRI: An introduction to methods. Eds P. Jezzard, P.M. Matthews and S.M. Smith. OUPGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Adam S. Lepley
    • 1
    • 2
    Email author
  • Dustin R. Grooms
    • 3
    • 4
  • Julie P. Burland
    • 1
  • Steven M. Davi
    • 1
  • Jeffrey M. Kinsella-Shaw
    • 1
  • Lindsey K. Lepley
    • 1
    • 2
  1. 1.Department of KinesiologyUniversity of ConnecticutStorrsUSA
  2. 2.Department of Orthopaedic SurgeryUniversity of Connecticut Health CenterFarmingtonUSA
  3. 3.Ohio Musculoskeletal and Neurological InstituteOhio UniversityAthensUSA
  4. 4.Division of Athletic Training, School of Applied Health Sciences and WellnessOhio UniversityAthensUSA

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