Skip to main content
Log in

Functional neuroimaging of acute oculomotor deficits in concussed athletes

Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

In the pursuit to better understand the neural underpinnings of oculomotor deficits following concussion we performed a battery of oculomotor tests while performing simultaneous functional magnetic resonance imaging (fMRI). Based on the increasing evidence that concussion can disrupt multiple brain functional networks, including the oculomotor control networks, a series of classic saccadic and smooth pursuit tasks were implemented. Nine concussed athletes were tested within seven days of injury along with nine age and sex matched healthy normal volunteers. Both behavioral and fMRI data revealed differential results between the concussed and normal volunteer groups. Concussed subjects displayed longer latency time in the saccadic tasks, worse position errors, and fewer numbers of self-paced saccades compared to normal volunteer subjects. Furthermore, the concussed group showed recruitment of additional brain regions and larger activation sites as evidenced by fMRI. As a potential diagnostic and management tool for concussion, oculomotor testing shows promise, and here we try to understand the reasons for this disrupted performance with the aide of advanced neuroimaging tools.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Bartels, A., Logothetis, N. K., & Moutoussis, K. (2008). fMRI and its interpretations: an illustration on directional selectivity in area V5/MT. Trends in Neurosciences, 31(9), 444–453. doi:10.1016/j.tins.2008.06.004.

    Article  CAS  PubMed  Google Scholar 

  • Bergman, K., & Bay, E. (2010). Mild traumatic brain injury/concussion: A review for ED Nurses. Journal of Emergency Nursing, 36(3), 221–230. doi:10.1016/j.jen.2009.07.001.

    Article  PubMed  Google Scholar 

  • Bodis-Wollner, I., Bucher, S. F., Seelos, K. C., Paulus, W., Reiser, M., & Oertel, W. H. (1997). Functional MRI mapping of occipital and frontal cortical activity during voluntary and imagined saccades. Neurology, 49(2), 416–420.

    Article  CAS  PubMed  Google Scholar 

  • Boxer, A. L., Garbutt, S., Seeley, W. W., Jafari, A., Heuer, H. W., Mirsky, J., & Miller, B. L. (2012). Saccade abnormalities in autopsy-confirmed frontotemporal lobar degeneration and Alzheimer disease. Archives of Neurology, 69(4), 509–517. doi:10.1001/archneurol.2011.1021.

    Article  PubMed Central  PubMed  Google Scholar 

  • Broglio, S. P. (2007). Neurocognitive performance of concussed athletes when symptom free. Journal of Athletic Training, 42(4), 504.

    PubMed Central  PubMed  Google Scholar 

  • Brown, M. R., Goltz, H. C., Vilis, T., Ford, K. A., & Everling, S. (2006). Inhibition and generation of saccades: rapid event-related fMRI of prosaccades, antisaccades, and nogo trials. NeuroImage, 33(2), 644–659. doi:10.1016/j.neuroimage.2006.07.002.

    Article  PubMed  Google Scholar 

  • Bryant, R. A., & Harvey, A. G. (1999). Postconcussive symptoms and posttraumatic stress disorder after mild traumatic brain injury. The Journal of Nervous and Mental Disease, 187(5), 302–305. doi:10.1097/00005053-199905000-00006.

    Article  CAS  PubMed  Google Scholar 

  • Capo-Aponte, J. E., Urosevich, T. G., Temme, L. A., Tarbett, A. K., & Sanghera, N. K. (2012). Visual dysfunctions and symptoms during the subacute stage of blast-induced mild traumatic brain injury. Military Medicine, 177(7), 804–813.

    Article  PubMed  Google Scholar 

  • Contreras, R., Kolster, R., Voss, H. U., Ghajar, J., Suh, M., & Bahar, S. (2008). Eye-target synchronization in mild traumatic brain-injured patients. Journal of Biological Physics, 34(3–4), 381–392. doi:10.1007/s10867-008-9092-1.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dieterich, M., Muller-Schunk, S., Stephan, T., Bense, S., Seelos, K., & Yousry, T. A. (2009). Functional magnetic resonance imaging activations of cortical eye fields during saccades, smooth pursuit, and optokinetic nystagmus. The Annals of the New York Academy of Sciences, 1164, 282–292. doi:10.1111/j.1749-6632.2008.03718.x.

    Article  PubMed  Google Scholar 

  • Drew, A. S., Langan, J., Halterman, C., Osternig, L. R., Chou, L. S., & van Donkelaar, P. (2007). Attentional disengagement dysfunction following mTBI assessed with the gap saccade task. Neuroscience Letters, 417(1), 61–65. doi:10.1016/j.neulet.2007.02.038.

    Article  CAS  PubMed  Google Scholar 

  • Ford, K. A., Goltz, H. C., Brown, M. R., & Everling, S. (2005). Neural processes associated with antisaccade task performance investigated with event-related FMRI. Journal of Neurophysiology, 94(1), 429–440. doi:10.1152/jn.00471.2004.

    Article  PubMed  Google Scholar 

  • Guskiewicz, K. M., Bruce, S. L., Cantu, R. C., Ferrara, M. S., Kelly, J. P., McCrea, M., & McLeod, T. C. V. (2004). National Athletic Trainers' Association position statement: Management of sport-related concussion. Journal of Athletic Training, 39(3), 280–297.

    PubMed Central  PubMed  Google Scholar 

  • Heitger, M. H., Anderson, T. J., & Jones, R. D. (2002). Saccade sequences as markers for cerebral dysfunction following mild closed head injury. Attention, 140, 433–448. doi:10.1016/S0079-6123(02)40067-2.

    CAS  Google Scholar 

  • Heitger, M. H., Anderson, T. J., Jones, R. D., Dalrymple-Alford, J. C., Frampton, C. M., & Ardagh, M. W. (2004). Eye movement and visuomotor arm movement deficits following mild closed head injury. Brain, 127, 575–590. doi:10.1093/Brain/Awh066.

    Article  PubMed  Google Scholar 

  • Heitger, M. H., Macaskill, M. R., Jones, R. D., & Anderson, T. J. (2005). The impact of mild closed head injury on involuntary saccadic adaptation: evidence for the preservation of implicit motor learning. Brain Injury, 19(2), 109–117.

    Article  PubMed  Google Scholar 

  • Heitger, M. H., Jones, R. D., Dalrymple-Alford, J. C., Frampton, C. M., Ardagh, M. W., & Anderson, T. J. (2006). Motor deficits and recovery during the first year following mild closed head injury. Brain Injury, 20(8), 807–824. doi:10.1080/02699050600676354.

    Article  PubMed  Google Scholar 

  • Heitger, M. H., Jones, R. D., Macleod, A. D., Snell, D. L., Frampton, C. M., & Anderson, T. J. (2009). Impaired eye movements in post-concussion syndrome indicate suboptimal brain function beyond the influence of depression, malingering or intellectual ability. Brain, 132(Pt 10), 2850–2870. doi:10.1093/brain/awp181.

    Article  PubMed  Google Scholar 

  • Hellerstein, L. F., Freed, S., & Maples, W. C. (1995). Vision profile of patients with mild brain injury. Journal of the American Optometric Association, 66(10), 634–639.

    CAS  PubMed  Google Scholar 

  • Kaufman, L. D., Pratt, J., Levine, B., & Black, S. E. (2010). Antisaccades: a probe into the dorsolateral prefrontal cortex in Alzheimer′s disease. A critical review. Journal of Alzheimer's Disease, 19(3), 781–793. doi:10.3233/JAD-2010-1275.

    PubMed  Google Scholar 

  • Kraus, M. F., Little, D. M., Donnell, A. J., Reilly, J. L., Simonian, N., & Sweeney, J. A. (2007). Oculomotor function in chronic traumatic brain injury. Cognitive and Behavioral Neurology, 20(3), 170–178. doi:10.1097/WNN.0b013e318142badb.

    Article  PubMed  Google Scholar 

  • Langlois, J. A., Rutland-Brown, W., & Wald, M. M. (2006). The epidemiology and impact of traumatic brain injury - A brief overview. The Journal of Head Trauma Rehabilitation, 21(5), 375–378.

    Article  PubMed  Google Scholar 

  • Lencer, R., & Trillenberg, P. (2008). Neurophysiology and neuroanatomy of smooth pursuit in humans. Brain and Cognition, 68(3), 219–228. doi:10.1016/j.bandc.2008.08.013.

    Article  PubMed  Google Scholar 

  • Lincoln, A. E., Caswell, S. V., Almquist, J. L., Dunn, R. E., Norris, J. B., & Hinton, R. Y. (2011). Trends in Concussion Incidence in High School Sports A Prospective 11-Year Study. The American Journal of Sports Medicine, 39(5), 958–963. doi:10.1177/0363546510392326.

    Article  PubMed  Google Scholar 

  • McCrory, P., Meeuwisse, W., Johnston, K., Dvorak, J., Aubry, M., Molloy, M., & Cantu, R. (2009). Consensus Statement on Concussion in Sport: the 3rd International Conference on Concussion in Sport held in Zurich, November 2008. British Journal of Sports Medicine, 43(Suppl 1), i76–i84. doi:10.1136/bjsm.2009.058248.

    Article  PubMed  Google Scholar 

  • McCrory, P., Meeuwisse, W. H., Aubry, M., Cantu, R. C., Dvorak, J., Echemendia, R. J., & Turner, M. (2013). Consensus Statement on Concussion in Sport: The 4th International Conference on Concussion in Sport, Zurich, November 2012. Journal of Athletic Training, 48(4), 554–575. doi:10.4085/1062-6050-48.4.05.

    Article  PubMed Central  PubMed  Google Scholar 

  • McDowell, J. E., Dyckman, K. A., Austin, B. P., & Clementz, B. A. (2008). Neurophysiology and neuroanatomy of reflexive and volitional saccades: evidence from studies of humans. Brain and Cognition, 68(3), 255–270. doi:10.1016/j.bandc.2008.08.016.

    Article  PubMed Central  PubMed  Google Scholar 

  • Muri, R. M., & Nyffeler, T. (2008). Neurophysiology and neuroanatomy of reflexive and volitional saccades as revealed by lesion studies with neurological patients and transcranial magnetic stimulation (TMS). Brain and Cognition, 68(3), 284–292. doi:10.1016/j.bandc.2008.08.018.

    Article  PubMed  Google Scholar 

  • Nitschke, M. F., Binkofski, F., Buccino, G., Posse, S., Erdmann, C., Kompf, D., & Heide, W. (2004). Activation of cerebellar hemispheres in spatial memorization of saccadic eye movements: An fMRI study. Human Brain Mapping, 22(2), 155–164. doi:10.1002/Hbm.20025.

    Article  PubMed  Google Scholar 

  • Ozyurt, J., Rutschmann, R. M., & Greenlee, M. W. (2006). Cortical activation during memory-guided saccades. Neuroreport, 17(10), 1005–1009.

    Article  PubMed  Google Scholar 

  • Pierrot-Deseilligny, C., Rivaud, S., Gaymard, B., & Agid, Y. (1991). Cortical control of memory-guided saccades in man. Experimental Brain Research, 83(3), 607–617.

    Article  CAS  PubMed  Google Scholar 

  • Pierrot-Deseilligny, C., Israel, I., Berthoz, A., Rivaud, S., & Gaymard, B. (1993). Role of the different frontal lobe areas in the control of the horizontal component of memory-guided saccades in man. Experimental Brain Research, 95(1), 166–171.

    Article  CAS  PubMed  Google Scholar 

  • Raz, E., Jensen, J. H., Ge, Y., Babb, J. S., Miles, L., Reaume, J., & Inglese, M. (2011). Brain Iron Quantification in Mild Traumatic Brain Injury: A Magnetic Field Correlation Study. American Journal of Neuroradiology, 32(10), 1851–1856. doi:10.3174/Ajnr.A2637.

    Article  CAS  PubMed  Google Scholar 

  • Schraa-Tam, C. K., van Broekhoven, P., van der Geest, J. N., Frens, M. A., Smits, M., & van der Lugt, A. (2009). Cortical and cerebellar activation induced by reflexive and voluntary saccades. Experimental Brain Research, 192(2), 175–187. doi:10.1007/s00221-008-1569-4.

    Article  PubMed  Google Scholar 

  • Sedney, C. L., Orphanos, J., & Bailes, J. E. (2011). When to Consider Retiring an Athlete After Sports-Related Concussion. Clinics in Sports Medicine, 30(1), 189–200. doi:10.1016/j.csm.2010.08.005.

    Article  PubMed  Google Scholar 

  • Slobounov, S. M., Zhang, K., Pennell, D., Ray, W., Johnson, B., & Sebastianelli, W. (2010). Functional abnormalities in normally appearing athletes following mild traumatic brain injury: a functional MRI study. Experimental Brain Research, 202(2), 341–354. doi:10.1007/s00221-009-2141-6.

    Article  PubMed Central  PubMed  Google Scholar 

  • Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47(10), 2015–2028. doi:10.1016/j.neuropsychologia.2009.03.004.

    Article  PubMed Central  PubMed  Google Scholar 

  • Suh, M., Kolster, R., Sarkar, R., McCandliss, B., & Ghajar, J. (2006). Deficits in predictive smooth pursuit after mild traumatic brain injury. Neuroscience Letters, 401(1–2), 108–113. doi:10.1016/j.neulet.2006.02.074.

    Article  CAS  PubMed  Google Scholar 

  • Sweeney, J. A., Luna, B., Keedy, S. K., McDowell, J. E., & Clementz, B. A. (2007). fMRI studies of eye movement control: investigating the interaction of cognitive and sensorimotor brain systems. NeuroImage, 36(Suppl 2), T54–T60. doi:10.1016/j.neuroimage.2007.03.018.

    Article  PubMed Central  PubMed  Google Scholar 

  • Theriault, M., De Beaumont, L., Tremblay, S., Lassonde, M., & Jolicoeur, P. (2011). Cumulative effects of concussions in athletes revealed by electrophysiological abnormalities on visual working memory. Journal of Clinical and Experimental Neuropsychology, 33(1), 30–41. doi:10.1080/13803391003772873.

    Article  PubMed  Google Scholar 

  • Toepper, M., Markowitsch, H. J., Gebhardt, H., Beblo, T., Thomas, C., Gallhofer, B., & Sammer, G. (2010). Hippocampal involvement in working memory encoding of changing locations: an fMRI study. Brain Research, 1354, 91–99. doi:10.1016/j.brainres.2010.07.065.

    Article  CAS  PubMed  Google Scholar 

  • Van der Stappen, A., Wuyts, F. L., & Van de Heyning, P. H. (2000). Computerized electronystagmography: normative data revisited. Acta Oto-Laryngologica, 120(6), 724–730.

    Article  Google Scholar 

  • Wade, N. J. (2010). Pioneers of eye-movement research. Perception, 39(8), 1150–1150.

    Google Scholar 

  • Witt, S. T., Lovejoy, D. W., Pearlson, G. D., & Stevens, M. C. (2010). Decreased prefrontal cortex activity in mild traumatic brain injury during performance of an auditory oddball task. Brain Imaging and Behavior, 4(3–4), 232–247. doi:10.1007/s11682-010-9102-3.

    Article  PubMed  Google Scholar 

Download references

Conflict of interest

Brian Johnson, Kai Zhang, Mark Hallett, and Seymon Slobounov declare that they have no conflicts of interest.

Informed consent

All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients for being included in the study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Semyon Slobounov.

Additional information

Brian Johnson and Kai Zhang contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Johnson, B., Zhang, K., Hallett, M. et al. Functional neuroimaging of acute oculomotor deficits in concussed athletes. Brain Imaging and Behavior 9, 564–573 (2015). https://doi.org/10.1007/s11682-014-9316-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-014-9316-x

Keywords

Navigation