Skip to main content

Brain activation during neurocognitive testing using functional near-infrared spectroscopy in patients following concussion compared to healthy controls

Abstract

There is no accepted clinical imaging modality for concussion, and current imaging modalities including fMRI, DTI, and PET are expensive and inaccessible to most clinics/patients. Functional near-infrared spectroscopy (fNIRS) is a non-invasive, portable, and low-cost imaging modality that can measure brain activity. The purpose of this study was to compare brain activity as measured by fNIRS in concussed and age-matched controls during the performance of cognitive tasks from a computerized neurocognitive test battery. Participants included nine currently symptomatic patients aged 18–45 years with a recent (15–45 days) sport-related concussion and five age-matched healthy controls. The participants completed a computerized neurocognitive test battery while wearing the fNIRS unit. Our results demonstrated reduced brain activation in the concussed subject group during word memory, (spatial) design memory, digit-symbol substitution (symbol match), and working memory (X’s and O’s) tasks. Behavioral performance (percent-correct and reaction time respectively) was lower for concussed participants on the word memory, design memory, and symbol match tasks than controls. The results of this preliminary study suggest that fNIRS could be a useful, portable assessment tool to assess reduced brain activation and augment current approaches to assessment and management of patients following concussion.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Abdelnour, F., & Huppert, T. J. (2010). Group analysis for functional optical brain imaging using a random effects model. Biomedical Optics Express, 2, 1–25.

    Google Scholar 

  • Abdelnour, A. F., & Huppert, T. (2009). Real-time imaging of human brain function by near-infrared spectroscopy using an adaptive general linear model. NeuroImage, 46, 133–143.

    PubMed Central  PubMed  Article  Google Scholar 

  • Abdelnour, A. F., & Huppert, T. J. (2011). A random-effects model for group-level analysis of diffuse optical brain imaging. Biomedical Optics Express, 2, 1–25.

    PubMed Central  Article  Google Scholar 

  • Abdelnour, F., Genovese, C., & Huppert, T. (2010). Hierarchical Bayesian regularization of reconstructions for diffuse optical tomography using multiple priors. Biomedical Optics Express, 1, 1084–1103.

    PubMed Central  PubMed  Article  Google Scholar 

  • Adelson, P. D., Nemoto, E., Colak, A., & Painter, M. (1998). The use of near infrared spectroscopy (NIRS) in children after traumatic brain injury: a preliminary report. Acta Neurochirurgica Supplement, 71, 250–254.

    CAS  PubMed  Google Scholar 

  • Alsalaheen, B. A., Mucha, A., Morris, L. O., Whitney, S. L., Furman, J. M., Camiolo-Reddy, C. E., et al. (2010). Vestibular rehabilitation for dizziness and balance disorders after concussion. Journal of Neurologic Physical Therapy, 34, 87–93.

    PubMed  Article  Google Scholar 

  • Broshek, D. K., Kaushik, T., Freeman, J. R., Erlanger, D., Webbe, F., & Barth, J. T. (2005). Sex differences in outcome following sports-related concussion. Journal of Neurosurgery, 102, 856-863.

    Google Scholar 

  • Chen, J. K., Johnston, K. M., Frey, S., Petrides, M., Worsley, K., & Ptito, A. (2004). Functional abnormalities in symptomatic concussed athletes: an fMRI study. NeuroImage, 22, 68–82.

    PubMed  Article  Google Scholar 

  • Chen, J. K., Johnston, K. M., Petrides, M., & Ptito, A. (2008). Neural substrates of symptoms of depression following concussion in male athletes with persisting postconcussion symptoms. Arch General Psychology, 65, 81–89.

    Article  Google Scholar 

  • Collie, A., Darby, D., & Maruff, P. (2001). Computerised cognitive assessment of athletes with sports related head injury. British Journal of Sports Medicine, 35, 297–302.

    Google Scholar 

  • Cope, M., Delpy, D. T., Reynolds, E. O., Wray, S., Wyatt, J., & van der Zee, P. (1988). Methods of quantitating cerebral near infrared spectroscopy data. Advances in Experimental Medicine and Biology, 222, 183–189.

    CAS  PubMed  Article  Google Scholar 

  • Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.

    CAS  PubMed  Article  Google Scholar 

  • Custo, A., Wells, W. M., 3rd, Barnett, A. H., Hillman, E. M., & Boas, D. A. (2006). Effective scattering coefficient of the cerebral spinal fluid in adult head models for diffuse optical imaging. Applied Optics, 45, 4747–4755.

    PubMed  Article  Google Scholar 

  • Dehghani, H., Eames, M. E., Yalavarthy, P. K., Davis, S. C., Srinivasan, S., Carpenter, C. M., et al. (2008). Near infrared optical tomography using NIRFAST: algorithm for numerical model and image reconstruction. Communications in Numerical Methods in Engineering, 25, 711–732.

    PubMed Central  PubMed  Article  Google Scholar 

  • Dick, R. W. (2009). Is there a gender difference in concussion incidence and outcomes? British Journal of Sports Medicine, 43, 46–50.

    Google Scholar 

  • Erlanger, D., Feldman, D., Kutner, K., Kaushik, T., Kroger, H., Fes- ta, J., et al. (2003). Development and validation of a Web-based neuropsychological test protocol for sports-related return-to-play decision-making. Archives of Clinical Neuropsychology, 18, 293–316.

    Google Scholar 

  • Friston, K. (2007). Statistical parametric mapping: the analysis of functional brain images. London: Academic.

    Google Scholar 

  • Frommer, L. J., Gurka, K. K., Cross, K. M., Ingersoll, C. D., & Comstock, S. A. (2011). Sex differences in concussion symptoms of high school athletes. Journal of Athletic Training, 46, 76–84.

    Google Scholar 

  • Giza, C. C., & Hovda, D. A. (2001). The Neurometabolic Cascade of Concussion. Journal of Athletic Training, 36, 228–235.

    PubMed Central  PubMed  Google Scholar 

  • Haitsma, I. K., & Maas, A. I. (2007). Monitoring cerebral oxygenation in traumatic brain injury. Progress in Brain Research, 161, 207–216.

    PubMed  Article  Google Scholar 

  • Holmes, C. J., Hoge, R., Collins, L., Woods, R., Toga, A. W., & Evans, A. C. (1998). Enhancement of MR images using registration for signal averaging. Journal of Computer Assisted Tomography, 22, 324–333.

    CAS  PubMed  Article  Google Scholar 

  • Huppert, T. J., Diamond, S. G., & Boas, D. A. (2008). Direct estimation of evoked hemoglobin changes by multimodality fusion imaging. Journal of Biomedical Optics, 13, 054031.

    PubMed Central  PubMed  Article  Google Scholar 

  • Huppert, T. J., Diamond, S. G., Franceschini, M. A., & Boas, D. A. (2009). HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain. Applied Optics, 48, D280–D298.

    PubMed Central  PubMed  Article  Google Scholar 

  • Jantzen, K. J., Anderson, B., Steinberg, F. L., & Kelso, J. A. (2004). A prospective functional MR imaging study of mild traumatic brain injury in college football players. AJNR American Journal of Neuroradiology, 25, 738–745.

    PubMed  Google Scholar 

  • Jobsis, F. F. (1977). Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science, 198, 1264–1267.

    CAS  PubMed  Article  Google Scholar 

  • Johnson, B., Zhang, K., Gay, M., Horovits, S., Hallett, M., Sebastianelli, W., et al. (2012). Alteration of brain default network in subacute phase of injury in concussed individuals: resting state fMRI study. Neuroimage, 59, 511–518.

    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, 375–378.

    PubMed  Article  Google Scholar 

  • Len, T. K., Neary, J. P., Asmundson, G. J., Goodman, D. G., Bjornson, B., & Bhambhani, Y. N. (2011). Cerebrovascular reactivity impairment after sport-induced concussion. Medicine and Science in Sports and Exercise, 43, 2241–2248.

    PubMed  Article  Google Scholar 

  • León-Carrion, J., Damas-López, J., Martín-Rodríguez, J. F., Domínguez-Roldán, J. M., Murillo-Cabezas, F., Barroso, Y. et al. (2008). The hemodynamics of cognitive control: the level of concentration of oxygenated hemoglobin in the superior prefrontal cortex varies as a function of performance in a modified Stroop task. Behavioral Brain Research, 193, 248–256.

    Google Scholar 

  • Lovell, M. R., & Fazio, V. (2008). Concussion management in the child and adolescent athlete. Current Sports Medicine Reports, 7, 12–15.

    PubMed  Article  Google Scholar 

  • Lovell, M. R., Pardini, J. E., Welling, J., Collins, M. W., Bakal, J., Lazar, N., et al. (2007). Functional brain abnormalities are related to clinical recovery and time to return-to-play in athletes. Neurosurgery, 61, 352–359. discussion 359-360.

    PubMed  Article  Google Scholar 

  • Mattout, J., Phillips, C., Penny, W. D., Rugg, M. D., & Friston, K. J. (2006). MEG source localization under multiple constraints: an extended Bayesian framework. NeuroImage, 30, 753–767.

    PubMed  Article  Google Scholar 

  • Maugans, T. A., Farley, C., Altaye, M., Leach, J., & Cecil, K. M. (2012). Pediatric sports-related concussion produces cerebral blood flow alterations. Pediatrics, 129, 28–37.

    PubMed Central  PubMed  Article  Google Scholar 

  • Mayer, A. R., Mannell, M. V., Ling, J., Elgie, R., Gasparovic, C., Phillips, J. P., et al. (2009). Auditory orienting and inhibition of return in mild traumatic brain injury: a FMRI study. Human Brain Mapping, 30, 4152–4166.

    PubMed Central  PubMed  Article  Google Scholar 

  • McAllister, T. W., Sparling, M. B., Flashman, L. A., Guerin, S. J., Mamourian, A. C., & Saykin, A. J. (2001). Differential working memory load effects after mild traumatic brain injury. NeuroImage, 14, 1004–1012.

    CAS  PubMed  Article  Google Scholar 

  • McAllister, T. W., Flashman, L. A., McDonald, B. C., & Saykin, A. J. (2006). Mechanisms of working memory dysfunction after mild and moderate TBI: evidence from functional MRI and neurogenetics. Journal of Neurotrauma, 23, 1450–1467.

    PubMed  Article  Google Scholar 

  • McCrory, P., Meeuqisse, W., Johnston, K., Dvorak J., Aubry, M., Molloy, M., et al. (2009). Consensus statement on concussion in sport 3rd international conference on concussion held in Zurich, November 2008. Clinical Journal of Sport Medicine, 19, 185–200.

    Google Scholar 

  • McCrory, P., Meeuwisse, W. H., Aubry, M., et al. (2013). Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012. British Journal of Sports Medicine, 47, 250–258.

    PubMed  Article  Google Scholar 

  • McGrath, N. (2010). Supporting the student-athlete’s return to the classroom after a sport-related concussion. Journal of Athletic Training, 45, 492–498.

    PubMed Central  PubMed  Article  Google Scholar 

  • Nakamura, T., Hillary, F. G., & Biswal, B. B. (2009). Resting network plasticity following brain injury. PLoS One, 4.

  • Obrig, H., & Villringer, A. (2003). Beyond the visible–imaging the human brain with light. Journal of Cerebral Blood Flow and Metabolism, 23, 1–18.

    PubMed  Article  Google Scholar 

  • Ptito, A., Chen, J. K., & Johnston, K. M. (2007). Contributions of functional magnetic resonance imaging (fMRI) to sport concussion evaluation. NeuroRehabilitation, 22, 217–227.

    PubMed  Google Scholar 

  • Sicard, K. M., & Duong, T. Q. (2005). Effects of hypoxia, hyperoxia, and hypercapnia on baseline and stimulus-evoked BOLD, CBF, and CMRO2 in spontaneously breathing animals. NeuroImage, 25, 850–858.

    PubMed Central  PubMed  Article  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, 341–354.

    PubMed Central  PubMed  Article  Google Scholar 

  • Slobounov, S. M., Gay, M., Zhang, K., Johnson, B., Pennell, D., Sebastianelli, W., et al. (2011). Alteration of brain functional network at rest and in response to YMCA physical stress test in concussed athletes: RsFMRI study. NeuroImage, 55, 1716–1727.

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Slobounov, S., Gay, M., Johnson, B., & Zhang, K. (2012). Concussion in athletics: ongoing clinical and brain imaging research controversies. Brain Imaging and Behavior, 6, 224–243.

    PubMed  Article  Google Scholar 

  • Soeda, A., Nakashima, T., Okumura, A., Kuwata, K., Shinoda, J., & Iwama, T. (2005). Cognitive impairment after traumatic brain injury: a functional magnetic resonance imaging study using the Stroop task. Neuroradiology, 47, 501–506.

    PubMed  Article  Google Scholar 

  • Stulemeijer, M., Vos, P. E., van der Werf, S., van Dijk, G., Rijpkema, M., & Fernandez, G. (2010). How mild traumatic brain injury may affect declarative memory performance in the post-acute stage. Journal of Neurotrauma, 27, 1585–1595.

    PubMed  Article  Google Scholar 

  • Van Kampen, D. A., Lovell, M. R., Pardini, J. E., Collins, M. W., & Fu, F. H. (2006). The “value added” of neurocognitive testing after sports-related concussion. The American Journal of Sports Medicine, 34, 1630–1635.

    PubMed  Article  Google Scholar 

  • Weatherall, A., Skowno, J., Lansdown, A., Lupton, T., & Garner, A. (2012). Feasibility of cerebral near-infrared spectroscopy monitoring in the pre-hospital environment. Acta Anaesthesiologica Scandinavica, 56, 172–177.

    CAS  PubMed  Article  Google Scholar 

  • Ye, J. C., Tak, S., Jang, K. E., Jung, J., & Jang, J. (2009). NIRS-SPM: statistical parametric mapping for near-infrared spectroscopy. NeuroImage, 44, 428–447.

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

Funding for this study was provided by the University of Pittsburgh Department of Radiology.

Informed consent statement

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.

Conflicts of interest statement

A. P. Kontos, T. J. Huppert, N. H. Beluk, R. J. Elbin, L. C. Henry, J. French, S. M. Dakan & M. W. Collins declare that they have no conflict of interest. Dr. Collins is a shareholder in ImPACT Applications, Inc. Dr. Collins involvement in the current manuscript involved interpretation of data. He did not have direct access to the raw data or participate in the analysis of the data

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. P. Kontos.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kontos, A.P., Huppert, T.J., Beluk, N.H. et al. Brain activation during neurocognitive testing using functional near-infrared spectroscopy in patients following concussion compared to healthy controls. Brain Imaging and Behavior 8, 621–634 (2014). https://doi.org/10.1007/s11682-014-9289-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-014-9289-9

Keywords

  • Concussion
  • Mild Traumatic Brain Injury
  • Neurocognitive Testing
  • Near Infrared Spectroscopy