No Evidence for Early Decrease in Blood Oxygenation in Rat Whisker Cortex in Response to Functional Activation

Lindauer, Ute; Royl, Georg; Leithner, Christoph; Kühl, Marc; Gold, Lorenz; Gethmann, Jörn; Kohl‐Bareis, Matthias; Villringer, Arno; Dirnagl, Ulrich

doi:10.1006/nimg.2000.0709

Cited by 149 publications

(105 citation statements)

References 45 publications

(91 reference statements)

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“…By calculating changes in HbO 2 , Hbr, and Hbt, we examined the spatiotemporal evolution of functional CBV and oxygenation changes with high resolution across various parenchymal and vascular compartments. The time course of changes in hemodynamic parameters we observed is similar to what others have measured using traditional spectroscopy (Jones et al, 2001;Lindauer et al, 2001;Malonek et al, 1997).…”

Section: Two-dimensional Optical Spectroscopic Imagingsupporting

confidence: 88%

Spatiotemporal Evolution of Functional Hemodynamic Changes and Their Relationship to Neuronal Activity

Sheth

Nemoto

Guiou

et al. 2005

J Cereb Blood Flow Metab

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Brain imaging techniques such as functional magnetic resonance imaging (fMRI) have provided a wealth of information about brain organization, but their ability to investigate fine-scale functional architecture is limited by the spatial specificity of the hemodynamic responses upon which they are based. We investigated the spatiotemporal evolution of hemodynamic responses in rat somatosensory cortex to electrical hindpaw stimulation. We combined the advantages of optical intrinsic signal imaging and spectroscopy to produce high-resolution two-dimensional maps of functional changes in tissue oxygenation and blood volume. Cerebral blood flow changes were measured with laser-Doppler flowmetry, and simultaneously recorded field potentials allowed comparison between hemodynamic changes and underlying neuronal activity. For the first 2 to 3 secs of activation, hemodynamic responses overlapped in a central parenchymal focus. Over the next several seconds, cerebral blood volume changes propagated retrograde into feeding arterioles, and oxygenation changes anterograde into draining veins. By 5 to 6 secs, responses localized primarily in vascular structures distant from the central focus. The peak spatial extent of the hemodynamic response increased linearly with synaptic activity. This spatial spread might be because of lateral subthreshold activation or passive vascular overspill. These results imply early microvascular changes in volume and oxygenation localize to activated neural columns, and that spatial specificity will be optimal within a 2-to 3-sec window after neuronal activation.

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Section: Two-dimensional Optical Spectroscopic Imagingsupporting

confidence: 88%

Spatiotemporal Evolution of Functional Hemodynamic Changes and Their Relationship to Neuronal Activity

Sheth

Nemoto

Guiou

et al. 2005

J Cereb Blood Flow Metab

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“…17 and 27). Path length correction, although missing from prior work in monkeys and cats, is necessary to avoid errors in the spectral decomposition and interpretation of ISOI signals (17,27) This quantitative analysis showed that the earliest stimulus-evoked response was driven by a rapid increase in [HbT] with no change in [HbR]. The full multiphasic time course of typical imaging signals, including the initial dip, rebound, and undershoot, could be well explained by a fast increase in [HbT] preceding a more transient decrease in [HbR].…”

Section: Resultsmentioning

confidence: 99%

Spatiotemporal precision and hemodynamic mechanism of optical point spreads in alert primates

Sirotin

Hillman

Bordier

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

116

144

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In functional brain imaging there is controversy over which hemodynamic signal best represents neural activity. Intrinsic signal optical imaging (ISOI) suggests that the best signal is the early darkening observed at wavelengths absorbed preferentially by deoxyhemoglobin (HbR). It is assumed that this darkening or "initial dip" reports local conversion of oxyhemoglobin (HbO) to HbR, i.e., oxygen consumption caused by local neural activity, thus giving the most specific measure of such activity. The blood volume signal, by contrast, is believed to be more delayed and less specific. Here, we used multiwavelength ISOI to simultaneously map oxygenation and blood volume [i.e., total hemoglobin (HbT)] in primary visual cortex (V1) of the alert macaque. We found that the hemodynamic ''point spread,'' i.e., impulse response to a minimal visual stimulus, was as rapid and retinotopically specific when imaged by using blood volume as when using the initial dip. Quantitative separation of the imaged signal into HbR, HbO, and HbT showed, moreover, that the initial dip was dominated by a fast local increase in HbT, with no increase in HbR. We found only a delayed HbR decrease that was broader in retinotopic spread than HbO or HbT. Further, we show that the multiphasic time course of typical ISOI signals and the strength of the initial dip may reflect the temporal interplay of monophasic HbO, HbR, and HbT signals. Characterizing the hemodynamic response is important for understanding neurovascular coupling and elucidating the physiological basis of imaging techniques such as fMRI.fMRI ͉ imaging ͉ macaque ͉ visual ͉ neurovascular coupling C erebral hemodynamics respond quickly and specifically to local neural activity (1, 2). Hemodynamic signals are thus used extensively as proxies for such activity in functional neuroimaging techniques like fMRI and intrinsic signal optical imaging (ISOI). There has been considerable debate, however, as to which of the possible hemodynamic signals, e.g., changes in local blood oxygenation, volume, or flow, with their distinct response properties, constitutes the ''best'' signal for inferring neural activity (1,(3)(4)(5).The debate regarding the best signal sharpened with reports of initial dips in both ISOI and fMRI signals. ISOI studies consistently found a brief stimulus-evoked darkening followed by a strong brightening at imaging wavelengths preferentially absorbed in deoxyhemoglobin (HbR) [e.g., at 605 nm (6)]. The darkening, later termed the initial dip*, was interpreted as a local conversion of oxyhemoglobin (HbO) to HbR caused by increased oxygen consumption by local neurons before any active vascular response (1, 7) The subsequent brightening was taken to measure the ''rebound'' in [HbO] † caused by a delayed, stimulus-triggered increase in cerebral blood flow (7).In parallel, some fMRI studies reported finding an initial dip before the rise in the blood oxygen level-dependent (BOLD) signal (8). Because the BOLD signal measures changes in [HbR] alone ‡ , the fMRI initial dip was seen a...

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“…similar changes of oxy-and deoxy-Hb during the post-stimulus period. These studies investigated whisker deflection in the rat (Lindauer et al, 2001(Lindauer et al, , 2003 or visual and motor stimulation in humans (Jasdzewski et al, 2003;Schroeter et al, 2004a).…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2006

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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. D

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No Evidence for Early Decrease in Blood Oxygenation in Rat Whisker Cortex in Response to Functional Activation

Cited by 149 publications

References 45 publications

Spatiotemporal Evolution of Functional Hemodynamic Changes and Their Relationship to Neuronal Activity

Spatiotemporal Evolution of Functional Hemodynamic Changes and Their Relationship to Neuronal Activity

Spatiotemporal precision and hemodynamic mechanism of optical point spreads in alert primates

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

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