Abstract
Functional near-infrared spectroscopy (fNIRS) has been proven reliable for investigation of low-level visual processing in both infants and adults. Similar investigation of fundamental auditory processes with fNIRS, however, remains only partially complete. Here we employed a systematic three-level validation approach to investigate whether fNIRS could capture fundamental aspects of bottom-up acoustic processing. We performed a simultaneous fNIRS-EEG experiment with visual and auditory stimulation in 24 participants, which allowed the relationship between changes in neural activity and hemoglobin concentrations to be studied. In the first level, the fNIRS results showed a clear distinction between visual and auditory sensory modalities. Specifically, the results demonstrated area specificity, that is, maximal fNIRS responses in visual and auditory areas for the visual and auditory stimuli respectively, and stimulus selectivity, whereby the visual and auditory areas responded mainly toward their respective stimuli. In the second level, a stimulus-dependent modulation of the fNIRS signal was observed in the visual area, as well as a loudness modulation in the auditory area. Finally in the last level, we observed significant correlations between simultaneously-recorded visual evoked potentials and deoxygenated hemoglobin (DeoxyHb) concentration, and between late auditory evoked potentials and oxygenated hemoglobin (OxyHb) concentration. In sum, these results suggest good sensitivity of fNIRS to low-level sensory processing in both the visual and the auditory domain, and provide further evidence of the neurovascular coupling between hemoglobin concentration changes and non-invasive brain electrical activity.
Similar content being viewed by others
References
Abla D, Okanoya K (2008) Statistical segmentation of tone sequences activates the left inferior frontal cortex: a near-infrared spectroscopy study. Neuropsychologia 46:2787–2795. doi:10.1016/j.neuropsychologia.2008.05.012
Debener S, Hine J, Bleeck S, Eyles J (2008) Source localization of auditory evoked potentials after cochlear implantation. Psychophysiology 45:20–24. doi:10.1111/j.1469-8986.2007.00610.x
Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21. doi:10.1016/j.jneumeth.2003.10.009
Driver J, Noesselt T (2008) Multisensory interplay reveals crossmodal influences on ‘sensory-specific’ brain regions, neural responses, and judgments. Neuron 57:11–23. doi:10.1016/j.neuron.2007.12.013
Duffy FH, Eksioglu YZ, Rotenberg A, Madsen JR, Shankardass A, Als H (2013) The frequency modulated auditory evoked response (FMAER), a technical advance for study of childhood language disorders: cortical source localization and selected case studies. BMC Neurol 13:12. doi:10.1186/1471-2377-13-12
Ehlis AC, Ringel TM, Plichta MM, Richter MM, Herrmann MJ, Fallgatter AJ (2009) Cortical correlates of auditory sensory gating: a simultaneous near-infrared spectroscopy event-related potential study. Neuroscience 159:1032–1043. doi:10.1016/j.neuroscience.2009.01.015
Ferrari M, Quaresima V (2012) A brief review on the history of human functional near-infrared spectroscopy (fNIRS) development and fields of application. NeuroImage 63:921–935. doi:10.1016/j.neuroimage.2012.03.049
Franceschini MA, Fantini S, Toronov V, Filiaci ME, Gratton E (2000) Cerebral hemodynamics measured by near-infrared spectroscopy at rest and during motor activation. In: Proceedings qof the Optical Society of America In Vivo Optical Imaging Workshop, 2000. Optical Society of America, pp 73–80
Giraud AL, Truy E, Frackowiak R (2001) Imaging plasticity in cochlear implant patients. Audiol Neurotol 6:381–393. doi:10.1159/000046847
Harms MP, Melcher JR (2002) Sound repetition rate in the human auditory pathway: representations in the waveshape and amplitude of fMRI activation. J Neurophysiol 88:1433–1450
Hauthal N, Sandmann P, Debener S, Thorne JD (2013) Visual movement perception in deaf and hearing individuals Advances in cognitive psychology/University of Finance and Management in Warsaw 9:53–61. doi:10.2478/v10053-008-0131-z
Hauthal N, Thorne JD, Debener S, Sandmann P (2014) Source localisation of visual evoked potentials in congenitally deaf individuals. Brain Topogr 27:412–424. doi:10.1007/s10548-013-0341-7
Hine J, Debener S (2007) Late auditory evoked potentials asymmetry revisited Clinical neurophysiology: official journal of the International Federation of. Clin Neurophysiol 118:1274–1285. doi:10.1016/j.clinph.2007.03.012
Hine J, Thornton R, Davis A, Debener S (2008) Does long-term unilateral deafness change auditory evoked potential asymmetries? Clin Neurophysiol 119:576–586
Jobsis FF (1977) Noninvasive, infrared monitoring of cerebral and myocardial oxygen sufficiency and circulatory parameters. Science 198:1264–1267
Koch SP, Koendgen S, Bourayou R, Steinbrink J, Obrig H (2008) Individual alpha-frequency correlates with amplitude of visual evoked potential and hemodynamic response. NeuroImage 41:233–242. doi:10.1016/j.neuroimage.2008.02.018
Kochel A, Schongassner F, Schienle A (2013) Cortical activation during auditory elicitation of fear and disgust: a near-infrared spectroscopy (NIRS) study. Neurosci Lett 549:197–200. doi:10.1016/j.neulet.2013.06.062
Langers DR, van Dijk P, Schoenmaker ES, Backes WH (2007) fMRI activation in relation to sound intensity and loudness. NeuroImage 35:709–718. doi:10.1016/j.neuroimage.2006.12.013
Luck SJ (2005) An introduction to the event-related potential technique. MIT press, Cambridge.
Majdani O et al. (2008) Demagnetization of cochlear implants and temperature changes in 3.0 T MRI environment. Otolaryngol–Head Neck Surg. 139:833–839
Malinen S, Hlushchuk Y, Hari R (2007) Towards natural stimulation in fMRI–issues of data analysis. NeuroImage 35:131–139. doi:10.1016/j.neuroimage.2006.11.015
May PJ, Tiitinen H (2010) Mismatch negativity (MMN), the deviance-elicited auditory deflection, explained. Psychophysiology 47:66–122. doi:10.1111/j.1469-8986.2009.00856.x
Mayhew SD, Dirckx SG, Niazy RK, Iannetti GD, Wise RG (2010) EEG signatures of auditory activity correlate with simultaneously recorded fMRI responses in humans NeuroImage 49:849–864. doi:10.1016/j.neuroimage.2009.06.080
Meek JH, Firbank M, Elwell CE, Atkinson J, Braddick O, Wyatt JS (1998) Regional hemodynamic responses to visual stimulation in awake infants. Pediatr Res 43:840–843. doi:10.1203/00006450-199806000-00019
Minagawa-Kawai Y, Mori K, Furuya I, Hayashi R, Sato Y (2002) Assessing cerebral representations of short and long vowel categories by NIRS. NeuroReport 13:581–584
Nasi T, Kotilahti K, Noponen T, Nissila I, Lipiainen L, Merilainen P (2010) Correlation of visual-evoked hemodynamic responses and potentials in human brain Experimental brain research 202:561–570. doi:10.1007/s00221-010-2159-9
Naue N, Rach S, Struber D, Huster RJ, Zaehle T, Korner U, Herrmann CS (2011) Auditory event-related response in visual cortex modulates subsequent visual responses in humans The Journal of neuroscience : the official journal of the society for. Neuroscience 31:7729–7736. doi:10.1523/JNEUROSCI.1076-11.2011
Nolte C, Kohl M, Scholz U, Weih M, Villringer A (1998) Characterization of the pulse signal over the human head by near infrared spectroscopy. Adv Exp Med Biol 454:115–123
Obrig H, Villringer A (2003) Beyond the visible–imaging the human brain with light. J Cereb Blood Flow Metab 23:1–18
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Pantev C, Dinnesen A, Ross B, Wollbrink A, Knief A (2006) Dynamics of auditory plasticity after cochlear implantation: a longitudinal study. Cereb Cortex 16:31–36. doi:10.1093/cercor/bhi081
Pernet CR, Chauveau N, Gaspar C, Rousselet GA (2011) LIMO EEG: a toolbox for hierarchical linear modeling of ElectroEncephaloGraphic data. Comput Intell Neurosci 2011:831409. doi:10.1155/2011/831409
Plichta MM, Herrmann MJ, Baehne CG, Ehlis AC, Richter MM, Pauli P, Fallgatter AJ (2006) Event-related functional near-infrared spectroscopy (fNIRS): are the measurements reliable? NeuroImage 31:116–124. doi:10.1016/j.neuroimage.2005.12.008
Plichta MM, Heinzel S, Ehlis AC, Pauli P, Fallgatter AJ (2007) Model-based analysis of rapid event-related functional near-infrared spectroscopy (NIRS) data: a parametric validation study. NeuroImage 35:625–634. doi:10.1016/j.neuroimage.2006.11.028
Raij T et al (2010) Onset timing of cross-sensory activations and multisensory interactions in auditory and visual sensory cortices. Eur J Neurosci 31:1772–1782. doi:10.1111/j.1460-9568.2010.07213.x
Remijn GB, Kojima H (2010) Active versus passive listening to auditory streaming stimuli: a near-infrared spectroscopy study. J Biomed Opt 15:037006. doi:10.1117/1.3431104
Rinne T et al (1999) Rapid communication scalp-recorded optical signals make sound processing in the auditory cortex visible? NeuroImage 10:620–624
Rohl M, Uppenkamp S (2012) Neural coding of sound intensity and loudness in the human auditory system. J Assoc Res Otolaryngol 13:369–379. doi:10.1007/s10162-012-0315-6
Rovati L, Salvatori G, Bulf L, Fonda S (2007) Optical and electrical recording of neural activity evoked by graded contrast visual stimulus. Biomed Eng Online 6:28. doi:10.1186/1475-925X-6-28
Rover J, Bach M (1985) Visual evoked potentials to various check patterns documenta ophthalmologica. Adv Ophthalmol 59:143–147
Sandmann P et al (2012) Visual activation of auditory cortex reflects maladaptive plasticity in cochlear implant users. Brain 135:555–568. doi:10.1093/brain/awr329
Schroeter ML, Zysset S, von Cramon DY (2004) Shortening intertrial intervals in event-related cognitive studies with near-infrared spectroscopy. NeuroImage 22:341–346. doi:10.1016/j.neuroimage.2003.12.041
Sigalovsky IS, Melcher JR (2006) Effects of sound level on fMRI activation in human brainstem, thalamic and cortical centers. Hear Res 215:67–76. doi:10.1016/j.heares.2006.03.002
Smith SM (2004) Overview of fMRI analysis. Br J Radiol 77:S167–S175. doi:10.1259/bjr/33553595
Takahashi K et al (2000) Activation of the visual cortex imaged by 24-channel near-infrared spectroscopy. Journal Biomed Opt 5:93–96. doi:10.1117/1.429973
Takeuchi M et al (2009) Brain cortical mapping by simultaneous recording of functional near infrared spectroscopy and electroencephalograms from the whole brain during right median nerve stimulation. Brain Topogr 22:197–214. doi:10.1007/s10548-009-0109-2
Thorne JD, De Vos M, Viola FC, Debener S (2011) Cross-modal phase reset predicts auditory task performance in humans The Journal of neuroscience : the official journal of the Society for. Neuroscience 31:3853–3861. doi:10.1523/JNEUROSCI.6176-10.2011
Uppenkamp S, Rohl M (2014) Human auditory neuroimaging of intensity and loudness. Hear Res 307:65–73. doi:10.1016/j.heares.2013.08.005
Viola FC, Thorne J, Edmonds B, Schneider T, Eichele T, Debener S (2009) Semi-automatic identification of independent components representing EEG artifact Clinical neurophysiology : official journal of the International Federation of. Clin Neurophysiol 120:868–877. doi:10.1016/j.clinph.2009.01.015
Wobst P, Wenzel R, Kohl M, Obrig H, Villringer A (2001) Linear aspects of changes in deoxygenated hemoglobin concentration and cytochrome oxidase oxidation during brain activation. NeuroImage 13:520–530. doi:10.1006/nimg.2000.0706
Ye JC, Tak S, Jang KE, Jung J, Jang J (2009) NIRS-SPM: statistical parametric mapping for near-infrared spectroscopy. NeuroImage 44:428–447. doi:10.1016/j.neuroimage.2008.08.036
Yesilyurt B, Whittingstall K, Ugurbil K, Logothetis NK, Uludag K (2010) Relationship of the BOLD signal with VEP for ultrashort duration visual stimuli (0.1 to 5 ms) in humans. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism 30:449–458. doi:10.1038/jcbfm.2009.224
Zemon V, Ratliff F (1982) Visual evoked potentials: evidence for lateral interactions. Proc Natl Acad Sci USA 79:5723–5726
Acknowledgments
The research leading to these results has received funding from the European Community’s Seventh Framework Programme FP7/2007–2013 under grant agreement number PITN-GA-2011-290011 and the cluster of excellance Hearing4all Oldenburg, Germany.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chen, LC., Sandmann, P., Thorne, J.D. et al. Association of Concurrent fNIRS and EEG Signatures in Response to Auditory and Visual Stimuli. Brain Topogr 28, 710–725 (2015). https://doi.org/10.1007/s10548-015-0424-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10548-015-0424-8