Investigating the post-stimulus undershoot of the BOLD signal—a simultaneous fMRI and fNIRS study

Abstract

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.

Introduction

Several recent studies compared the hemodynamic response to brain activation as measured by functional near-infrared spectroscopy (fNIRS) with another imaging method, such as functional magnetic resonance imaging (fMRI) (Hoge et al., 2005, Kennan et al., 2002, Kleinschmidt et al., 1996, Mehagnoul-Schipper et al., 2002, Obrig et al., 2000b, Seiyama et al., 2004, Siegel et al., 2003, Strangman et al., 2002, Toronov et al., 2001a, Toronov et al., 2001b, Toronov et al., 2003, Wenzel et al., 2000) or positron emission tomography (PET) (Hock et al., 1997, Villringer et al., 1997). While optical measurements are poorer in spatial resolution and depth penetration than fMRI, they are biochemical specific and, consequently, provide information about changes in oxy-, deoxy-, and total hemoglobin (Hb) with a high temporal resolution (Hoshi, 2003, Villringer and Chance, 1997). Moreover, it was suggested that fNIRS is particularly sensitive to the microvasculature (Boushel et al., 2001, Cannestra et al., 2001) because, for larger vessels such as arteries and veins, entering light cannot escape (Liu et al., 1995a, Liu et al., 1995b). The blood oxygenation level dependent (BOLD) signal represents, on the other hand, all spatial scales of venous vessels (Lee et al., 2001, Strangman et al., 2002, Weisskoff, 1999). These advantages of fNIRS can be used to better understand the nature of the hemodynamic response to neuronal activation and the origin of the BOLD signal. On the other hand, optical studies are limited because anatomical information is not obtained. Simultaneously acquired optical and fMRI data may synergize and overcome this limitation as the MRI data provide information about the location of the optical probes.

The present study aimed at comparing the temporal behavior of the hemodynamic response between fMRI and fNIRS in the visual cortex of young healthy humans. All previous studies that combined fNIRS with another imaging method did not investigate the post-stimulus period of the hemodynamic response. To include that period, we chose a long intertrial interval of 60 s (Mildner et al., 2001). An event-related approach was employed to detect the hemodynamic response to a single trial (Burock et al., 1998, Schroeter et al., 2002, Schroeter et al., 2004c, Schroeter et al., 2004d). Measurements were performed simultaneously with fMRI and fNIRS.