Temporal decoupling of oxy- and deoxy-hemoglobin hemodynamic responses detected by functional near-infrared spectroscopy (fNIRS)
DOI:
https://doi.org/10.14738/jbemi.12.146Keywords:
Functional near-infrared spectroscopy, fNIRS, hemodynamics, motor control, neural activation, temporal couplingAbstract
This study provides experimental evidence that there is temporal decoupling between the hemodynamic responses of oxy- and deoxy-hemoglobin (Hb) as detected by functional near-infrared spectroscopy (fNIRS). Using 64 spatially distributed optrodes to record motor cortical activities during a free arm movement task (right-left and front-back movements), we detected that the temporal profile of oxy- and deoxy-Hb responses are desynchronized and decoupled (i.e., oxy- and deoxy-Hb levels do not rise and fall at the same time). We correlated four different measures of hemodynamic profiles with the arm movements, namely, oxy- (HbO2) and deoxy-hemoglobin (Hb) and their summation (HbO2 + Hb) and difference (HbO2 - Hb) signals. These measures correspond to the changes in oxygen delivery, oxygen extraction, total blood volume delivered, and total oxygenation with specific movement directions, respectively. They revealed different components of the hemodynamic response in a localized neuronal population in the motor cortex. The results suggested that, by using these four measures, oxygen delivery and oxygen extraction can be coupled in one movement direction, but decoupled in another movement direction for the same human subject executing the same movement task. Oxygen delivery and oxygen extraction do not always co-vary together temporally. Thus, using a single measure of oxygen delivery or extraction alone may not be sufficient to determine whether the cortical area is activated or deactivated. Rather, a combination of all four measures of hemodynamic signals that represent temporal coupling and decoupling of oxygen delivery and extraction is needed to differentiate the temporal profiles of neural activation and deactivation. It demonstrated that different hemodynamic measures can reveal temporally decoupled activation/deactivation patterns differentially during the right-left and front-back motor task. Therefore, relying on a single measure of deoxy-Hb may be insufficient to characterize the neural responses without the oxy-Hb measure. Orthogonal arm movement (right-left vs. front-back) directions can be differentiated based on the differential temporally coupled and decoupled hemodynamics.
References
Calderon-Arnulphi, M., A. Alaraj, and K. Slavin, Near infrared technology in neuroscience: past, present and future. Neurol Res, 2009. 31(6): p. 605 - 614.
Hoshi, Y., Towards the next generation of near-infrared spectroscopy. Philos Trans A Math Phys Eng Sci, 2011. 369(1955): p. 4425-39.
Pellicer, A. and C. Bravo Mdel, Near-infrared spectroscopy: a methodology-focused review. Semin Fetal Neonatal Med, 2011. 16(1): p. 42-9.
Cope, M., et al., Methods of quantitating cerebral near infrared spectroscopy data. Adv Exp Med Biol, 1988. 222: p. 183-9.
Montcel, B., R. Chabrier, and P. Poulet, Time-resolved absorption and hemoglobin concentration difference maps: a method to retrieve depth-related information on cerebral hemodynamics. Opt Express, 2006. 14(25): p. 12271-87.
Logothetis, N.K., et al., Neurophysiological investigation of the basis of the fMRI signal. Nature, 2001. 412(6843): p. 150-7.
Toronov, V., et al., Investigation of human brain hemodynamics by simultaneous near-infrared spectroscopy and functional magnetic resonance imaging. Med Phys, 2001. 28(4): p. 521-7.
Obata, T., et al., Discrepancies between BOLD and flow dynamics in primary and supplementary motor areas: application of the balloon model to the interpretation of BOLD transients. Neuroimage, 2004. 21(1): p. 144-53.
Huppert, T.J., et al., A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans. Neuroimage, 2006. 29(2): p. 368-82.
Schwartz, A.B., Direct cortical representation of drawing. Science, 1994. 265(5171): p. 540-2.
Kettner, R.E., A.B. Schwartz, and A.P. Georgopoulos, Primate motor cortex and free arm movements to visual targets in three-dimensional space. III. Positional gradients and population coding of movement direction from various movement origins. J Neurosci, 1988. 8(8): p. 2938-47.
Georgopoulos, A.P., R.E. Kettner, and A.B. Schwartz, Primate motor cortex and free arm movements to visual targets in three-dimensional space. II. Coding of the direction of movement by a neuronal population. J Neurosci, 1988. 8(8): p. 2928-37.
Georgopoulos, A.P., A.B. Schwartz, and R.E. Kettner, Neuronal population coding of movement direction. Science, 1986. 233(4771): p. 1416-9.
Lin, S., J. Si, and A.B. Schwartz, Self-organization of firing activities in monkey's motor cortex: trajectory computation from spike signals. Neural Comput, 1997. 9(3): p. 607-21.
Tam, N.D. and G. Zouridakis, Optical imaging of motor cortical activation using functional near-infrared spectroscopy. BMC Neuroscience, 2012. 13(Suppl 1): p. P27.
Tam, N.D. and G. Zouridakis, Optical imaging of motor cortical hemodynamic response to directional arm movements using near-infrared spectroscopy. American Journal of Biomedical Engineering, 2013. 3(2): p. 11-17.
Tam, N.D.Z., George, Decoding Movement Direction from Motor Cortex Recordings Using Near-Infrared Spectroscopy.. (in press). Infrared Spectroscopy: Theory, Developments and Applications2014, Hauppauge, NY: Nova Science Publishers, Inc.
Pouliot, P., et al., Nonlinear hemodynamic responses in human epilepsy: a multimodal analysis with fNIRS-EEG and fMRI-EEG. J Neurosci Methods, 2012. 204(2): p. 326-40.
Colier, W.N.J.M., et al., Detailed evidence of cerebral hemoglobin oxygenation changes in response to motor activation revealed by a continuous wave spectrophotometer with 10 Hz temporal resolution. Proc SPIE, 1997. 2979: p. 390–396.
Kuboyama, N., et al., The effect of maximal finger tapping on cerebral activation. J Physiol Anthropol Appl Human Sci, 2004. 23(4): p. 105-10.
Obrig, H., et al., Cerebral oxygenation changes in response to motor stimulation. J Appl Physiol, 1996. 81(3): p. 1174-83.
Obrig, H., et al., Length of resting period between stimulation cycles modulates hemodynamic response to a motor stimulus. Adv Exp Med Biol, 1997. 411: p. 471-80.
Hirth, C., et al., Simultaneous assessment of cerebral oxygenation and hemodynamics during a motor task. A combined near infrared and transcranial Doppler sonography study. Adv Exp Med Biol, 1997. 411: p. 461-9.
Leff, D.R., et al., Assessment of the cerebral cortex during motor task behaviours in adults: a systematic review of functional near infrared spectroscopy (fNIRS) studies. Neuroimage, 2011. 54(4): p. 2922-36.
Suzuki, M., et al., Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage, 2004. 23(3): p. 1020-6.
Wriessnegger, S.C., J. Kurzmann, and C. Neuper, Spatio-temporal differences in brain oxygenation between movement execution and imagery: a multichannel near-infrared spectroscopy study. Int J Psychophysiol, 2008. 67(1): p. 54-63.
Tachtsidis, I., et al., Investigation of frontal cortex, motor cortex and systemic haemodynamic changes during anagram solving. Adv Exp Med Biol, 2008. 614: p. 21-8.
Biswal, B.B., et al., Decoupling of the hemodynamic and activation-induced delays in functional magnetic resonance imaging. J Comput Assist Tomogr, 2003. 27(2): p. 219-25.
