Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task

Brain activity during a verbal fluency task (VFT) has been the target of many functional imaging studies. Most studies using near-infrared spectroscopy (NIRS) have reported major activation in the frontal pole, but those using PET or fMRI have not. This led us to hypothesize that changes in the NIRS signals measured in the forehead during VFT were due to changes in skin blood flow. To test this hypothesis, we measured NIRS signals and the Doppler tissue blood flow signals in the foreheads of 50 participants. The measurements were performed while each participant produced words during two 60-s periods with an interval of 100 s. In addition to a conventional optode separation distance of 30 mm (FAR channels), we used a short distance--5mm (NEAR channels)--to measure NIRS signals that originated exclusively from surface tissues. The oxygenated hemoglobin (oxyHb) concentration in the FAR and NEAR channels, as well as the Doppler blood flow signal, increased in a similar manner during the two periods of word production; the signal increase in the first period was twice as high as that in the second period. Accordingly, the mean changes in oxyHb concentration in the FAR channels were correlated closely with the changes in the NEAR channels (R(2) = 0.91) and with the integrated Doppler skin blood flow signal (R(2) = 0.94). Furthermore, task-related NIRS responses disappeared when we blocked skin blood flows by pressing a small area that covered a pair of optodes. Additionally, changes in the FAR channel signals were correlated closely with the magnitude of pulsatile waves in the Doppler signal (R(2) = 0.92), but these signals were not highly correlated with the pulse rate (R(2) = 0.43). These results suggest that a major part of the task-related changes in the oxyHb concentration in the forehead is due to task-related changes in the skin blood flow, which is under different autonomic control than heart rate.

[1]  A. Villringer,et al.  Decrease in parietal cerebral hemoglobin oxygenation during performance of a verbal fluency task in patients with Alzheimer's disease monitored by means of near-infrared spectroscopy (NIRS) — correlation with simultaneous rCBF-PET measurements , 1997, Brain Research.

[2]  M. Tamura,et al.  Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. , 2001, Journal of applied physiology.

[3]  P D Drummond,et al.  The effect of adrenergic blockade on blushing and facial flushing. , 1997, Psychophysiology.

[4]  David T Delpy,et al.  Investigation of frontal cortex, motor cortex and systemic haemodynamic changes during anagram solving. , 2008, Advances in experimental medicine and biology.

[5]  Motohiro Okada,et al.  Intrasubject reproducibility of prefrontal cortex activities during a verbal fluency task over two repeated sessions using multi‐channel near‐infrared spectroscopy , 2009, Psychiatry and clinical neurosciences.

[6]  R. Saager,et al.  Measurement of layer-like hemodynamic trends in scalp and cortex: implications for physiological baseline suppression in functional near-infrared spectroscopy. , 2008, Journal of biomedical optics.

[7]  Masaki Kameyama,et al.  Sex and age dependencies of cerebral blood volume changes during cognitive activation: a multichannel near-infrared spectroscopy study , 2004, NeuroImage.

[8]  S. Arridge,et al.  Estimation of optical pathlength through tissue from direct time of flight measurement , 1988 .

[9]  Emery N Brown,et al.  Adaptive filtering to reduce global interference in evoked brain activity detection: a human subject case study. , 2007, Journal of biomedical optics.

[10]  M J Brammer,et al.  Attenuated frontal activation during a verbal fluency task in patients with schizophrenia. , 1998, The American journal of psychiatry.

[11]  S. Umeyama,et al.  Multidistance probe arrangement to eliminate artifacts in functional near-infrared spectroscopy. , 2009, Journal of biomedical optics.

[12]  Masato Fukuda,et al.  Association between Catechol-O-Methyltrasferase Val108/158Met Genotype and Prefrontal Hemodynamic Response in Schizophrenia , 2009, PloS one.

[13]  Rolf B. Saager,et al.  Two-detector Corrected Near Infrared Spectroscopy (C-NIRS) detects hemodynamic activation responses more robustly than single-detector NIRS , 2011, NeuroImage.

[14]  Heide Klumpp,et al.  Review of brain functioning in depression for semantic processing and verbal fluency. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  I. Miyai,et al.  Removal of the skin blood flow artifact in functional near-infrared spectroscopic imaging data through independent component analysis. , 2007, Journal of biomedical optics.

[16]  D. Delpy,et al.  Performance comparison of several published tissue near-infrared spectroscopy algorithms. , 1995, Analytical biochemistry.

[17]  Ann-Christine Ehlis,et al.  Functional near-infrared spectroscopy: A long-term reliable tool for measuring brain activity during verbal fluency , 2008, NeuroImage.

[18]  S C Williams,et al.  Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. , 1997, Magnetic resonance imaging.

[19]  Michael J Brammer,et al.  Functional magnetic resonance imaging of verbal fluency and confrontation naming using compressed image acquisition to permit overt responses , 2003, Human brain mapping.

[20]  M. Herrmann,et al.  Frontal activation during a verbal-fluency task as measured by near-infrared spectroscopy , 2003, Brain Research Bulletin.

[21]  C. Sato,et al.  Reevaluation of near-infrared light propagation in the adult human head: implications for functional near-infrared spectroscopy. , 2005, Journal of biomedical optics.

[22]  S. Arridge,et al.  A Monte Carlo investigation of optical pathlength in inhomogeneous tissue and its application to near-infrared spectroscopy. , 1993, Physics in medicine and biology.

[23]  Albert Gjedde,et al.  Putative Tests of Frontal Lobe Function: A PET-Study of Brain Activation During Stroop's Test and Verbal Fluency , 2002, Journal of clinical and experimental neuropsychology.

[24]  David A Boas,et al.  Monte Carlo simulation of photon migration in 3D turbid media accelerated by graphics processing units. , 2009, Optics express.

[25]  M. Herrmann,et al.  Bilaterally reduced frontal activation during a verbal fluency task in depressed patients as measured by near-infrared spectroscopy. , 2004, The Journal of neuropsychiatry and clinical neurosciences.

[26]  R. Saager,et al.  Direct characterization and removal of interfering absorption trends in two-layer turbid media. , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[27]  亀山 正樹,et al.  Frontal lobe function in bipolar disorder : a multichannel near-infrared spectroscopy study , 2005 .

[28]  M. Schweiger,et al.  Theoretical and experimental investigation of near-infrared light propagation in a model of the adult head. , 1997, Applied optics.

[29]  P. Drummond,et al.  Adrenergic receptors in the forehead microcirculation , 1996, Clinical Autonomic Research.

[30]  D. Louis Collins,et al.  Design and construction of a realistic digital brain phantom , 1998, IEEE Transactions on Medical Imaging.

[31]  Masato Fukuda,et al.  Reduced frontopolar activation during verbal fluency task in schizophrenia: A multi-channel near-infrared spectroscopy study , 2008, Schizophrenia Research.

[32]  David A Boas,et al.  Near-infrared spectroscopy measurement of the pulsatile component of cerebral blood flow and volume from arterial oscillations. , 2007, Journal of biomedical optics.

[33]  Masao Iwase,et al.  Discriminant analysis in schizophrenia and healthy subjects using prefrontal activation during frontal lobe tasks: A near-infrared spectroscopy , 2010, Schizophrenia Research.

[34]  Jarl Risberg,et al.  Lateralized frontal blood flow increases during fluency tasks: influence of cognitive strategy , 1998, Neuropsychologia.

[35]  N. Kato,et al.  Alteration of hemoglobin oxygenation in the frontal region in elderly depressed patients as measured by near-infrared spectroscopy. , 2000, The Journal of neuropsychiatry and clinical neurosciences.

[36]  須藤 友博.  Multichannel near-infrared spectroscopy in depression and schizophrenia : Cognitive brain activation study , 2004 .

[37]  E. Okada,et al.  Monte Carlo prediction of near-infrared light propagation in realistic adult and neonatal head models. , 2003, Applied optics.

[38]  E. Phelps,et al.  FMRI of the prefrontal cortex during overt verbal fluency , 1997, Neuroreport.

[39]  B. Rosen,et al.  Evidence of a Cerebrovascular Postarteriole Windkessel with Delayed Compliance , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[40]  Toru Yamada,et al.  Monte Carlo study of global interference cancellation by multidistance measurement of near-infrared spectroscopy. , 2009, Journal of biomedical optics.

[41]  Philippe Lahorte,et al.  Verbal fluency as a prefrontal activation probe: a validation study using 99mTc-ECD brain SPET , 2000, European Journal of Nuclear Medicine.