Kupka, T.

Mildner, T.

Schroeter, M.

Uludag, K.

von Cramon, D.

English

Schroeter, Matthias L.

Kupka, Thomas

Mildner, Toralf

Uludag, Kamil

von Cramon, D. Yves

Max Planck Society eDoc Server

Investigating the post-stimulus undershoot of the BOLD signal – A simultaneous fMRI and fNIRS study

Measuring the hemodynamic response with functional magnetic resonance imaging (fMRI) together with functional near-infrared spectroscopy (fNIRS) may overcome limitations of single-method approaches. Accordingly, we measured the event-related hemodynamic response with both imaging methods simultaneously in young subjects during visual stimulation. An intertrial interval of 60 s was chosen to include the prolonged post-stimulus undershoot of the blood oxygenation level dependent (BOLD) signal. During visual stimulation, the BOLD signal, oxy-, and total hemoglobin (Hb) increased, whereas deoxy-Hb decreased. The post-stimulus period was characterized by an undershoot of the BOLD signal, oxy-Hb, and an overshoot of deoxy-Hb. Total Hb as measured by fNIRS returned to baseline immediately after the end of stimulation. Results suggest that the post-stimulus events as measured by fNIRS are dominated by a prolonged high-level oxygen consumption in the microvasculature. The contribution of a delayed return of blood volume to the BOLD post-stimulus undershoot in post-capillary veins as suggested by the Balloon and Windkessel models remains ambiguous. Temporal changes in the BOLD signal were highly correlated with deoxy-Hb, with lower correlation values for oxy- and total Hb. Furthermore, data show that fNIRS covers the outer 1 cm of the brain cortex. These results were confirmed by simultaneous fMRI/fNIRS measurements during rest. In conclusion, multimodal imaging approaches may contribute to the understanding of neurovascular coupling

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Investigating the post-stimulus undershoot of the BOLD signal: A simultaneous fMRI and fNIRS study

IntroductionMaterials  and MethodsConclusion2Matthias L. Schroeter*#, Thomas Kuppka*, Toralf Mildner*, Kâmil Uluda  § and D. Yves von Cramon*#1ResultsInvestigating the post-stimulus undershoot of the BOLD signal - a simultaneousfMRI and fNIRS studyThe origin of the post-stimulus undershoot of the blood-oxygenation level dependent (BOLD)signal is controversial (Aubert and Costalat, 2002; Buxton et al., 1999). Three mechanisms havebeen discussed:• The regional cerebral blood volume (rCBV) may return later to baseline than blood flow(rCBF) due to delayed venous compliance as proposed by the Balloon and Windkesselmodels.• The undershoot may reflect the persistence of a high oxygen consumption after rCBF hasreturned to baseline.• An undershoot of the rCBF could contribute to the BOLD signal undershoot.To explore the mechanisms of the post-stimulus undershoot we measured the hemodynamicresponse in the visual cortex simultaneously with functional near-infrared spectroscopy (fNIRS)and functional magnetic resonance imaging (fMRI) .• 12 healthy subjects participated in the study (mean age 24.8+1 years).• A simple visual task was employed (array of red L-shapes randomly rotating on ablack background for 6 s).• Changes in the concentration of oxy-, deoxy-hemoglobin (Hb) and the redox state of thecytochrome-c-oxidase (Cyt-Ox) were measured by a NIRO-300 spectrometer (HamamatsuPhotonics K.K., Japan).• Two emitter-detector pairs were placed crosswise centered at position O1 of the international10/20 system (Figure 1).• fMRI experiments were performed using a 3.0 T whole-body scanner (3.0 T Medspec Scanner,Bruker, Germany). 12 oblique slices were oriented parallel to the plane spanned between thetwo emitter detector pairs.As illustrated in Figure 2A for one subject stimulation led to an activation in the visual cortexbilaterally around the calcarine sulcus. If the time course of deoxy-Hb as measured by fNIRSwas used as a design function, the same area was activated (Figure 2B).• Our study is the first one that investigated the post-stimulus period by both, fNIRS and fMRI.• This multimodal approach investigates simultaneously events in the microvascular (fNIRS)and the postcapillary venous compartment (BOLD fMRI).• Results suggest that the post-stimulus events as measured by fNIRS are dominated by aprolonged high-level oxygen consumption in the microvasculature.• The contribution of a delayed return of rCBV to the BOLD post-stimulus undershoot in post-capillary veins as suggested by the Balloon and Windkessel models remains ambiguous.*Max-Planck-Institute for Human Cognitive and Brain Sciences, Stephanstr. 1A, Germany#Day Clinic of Cognitive Neurology, University of Leipzig, Liebigstr. 22A, 04103 Leipzig, Germany; §fMRI Center of the Department of Radiology,University of California San Diego, 9500 Gilman Drive/Osler Lane, La Jolla, CA 92039-0677, USAemail: schroet@cbs.mpg.deFigure 1 Sampling volume (blue) between the two emitter-detector pairs of fNIRS in relation to the slices of fMRI (white).Highest correlation between oxy-/deoxy-hemoglobin and the BOLD signal is expected for the slice in the center of the banana-shaped fNIRS sampling volume.REFERENCES:Aubert, A., Costalat, R., 2002. A model of the coupling between brain electrical activity, metabolism, and hemodynamics: Application to the interpretation of functional neuroimaging.NeuroImage 17, 1162-1181.Buxton, R.B., Wong, E.C., Frank, L.R., 1999. The post-stimulus undershoot of the functional MRI signal. In: Moonen, C.T.W., Bandettini, P.A. (Eds.), Functional MRI. Springer, Berlin, pp. 253-262.Schroeter, M.L., Kupka, T., Mildner, T., Uluda  , K., von Cramon, D.Y., 2006. Investigating the post-stimulus undershoot of the BOLD signal - a simultaneous fMRI and fNIRS study.NeuroImage 30, 349-358.Figure 2 Averaged correlation maps for one subject. BOLDcontrast. A. If a boxcar function was used as a design function(0.85 < r < 0.95). B. If the time course of deoxy-hemoglobinas measured by fNIRS was used as a design function (0.8 < r< 0.83). Optode positions are marked by vitamin E capsules(see first row in A).Right after stimulation onset oxy-Hb, total Hb, Cyt-Ox and the BOLD signal increased, whereasdeoxy-Hb decreased (Figure 3). During the post-stimulus period, oxy-Hb and the BOLD signaldecreased below, whereas deoxy-Hb increased above baseline values. Concentration of total Hband the redox-state of the Cyt-Ox did not change. Depth penetration of fNIRS was highest for15 mm distance from skin surface (Figure 4).Figure 3 Concentration changes of oxy-, deoxy-, totalhemoglobin (Hb), and cytochrome-c-oxidase (Cyt-Ox) asmeasured by fNIRS, and the BOLD signal as measured byfMRI. Visual stimulation started at 0 s and continued till 6s. Mean±SD.Figure 4 Depth penetration of fNIRS. Time courses ofdeoxy-hemoglobin (Hb) as measured by fNIRS werecorrelated with the BOLD signal for several distances tooptode layer. Correlation is shown for visual stimulationand rest (closed eyes). Pearson correlation coefficients andpartial correlation coefficients (adjusted for changes in totalHb; corr.) were normalized with a Fisher’s Z transformation.Mean±SEM. *** ### p<0.001, ** ## p<0.01, * # p<0.052-tailed paired Student’s t-test vs. values at 15 mm.43

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Investigating the post-stimulus undershoot of the BOLD signal – A simultaneous fMRI and fNIRS study

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