Coupling between neuronal activity and microcirculation: Implications for functional brain imaging

Vanzetta, Ivo; Grinvald, Amiram

doi:10.2976/1.2889618

Cited by 73 publications

(64 citation statements)

References 243 publications

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“…21, 22, and 34). Discrepancies between rodent and earlier monkey results had been attributed to species differences (35,36). By contrast, our findings add to a growing body of evidence suggesting that neurovascular coupling mechanisms may be conserved across species.…”

Section: Discussioncontrasting

confidence: 53%

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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Section: Discussioncontrasting

confidence: 53%

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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“…The need for anesthesia depends on the methodology applied in neurovascular coupling studies (for reviews, see Grinvald, 2008 andDirnagl, 1995). The electrophysiological techniques that have been used to represent neural activity as a quantitative index to compare vascular responses involves local field potentials (LFPs), and single unit and multiunit spiking activity (Lauritzen, 2001;Logothetis et al, 2001).…”

Section: Why Is Anesthesia Needed?mentioning

confidence: 99%

Anesthesia and the Quantitative Evaluation of Neurovascular Coupling

Masamoto

Kanno²

2012

J Cereb Blood Flow Metab

241

191

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Anesthesia has broad actions that include changing neuronal excitability, vascular reactivity, and other baseline physiologies and eventually modifies the neurovascular coupling relationship. Here, we review the effects of anesthesia on the spatial propagation, temporal dynamics, and quantitative relationship between the neural and vascular responses to cortical stimulation. Previous studies have shown that the onset latency of evoked cerebral blood flow (CBF) changes is relatively consistent across anesthesia conditions compared with variations in the time-to-peak. This finding indicates that the mechanism of vasodilation onset is less dependent on anesthesia interference, while vasodilation dynamics are subject to this interference. The quantitative coupling relationship is largely influenced by the type and dosage of anesthesia, including the actions on neural processing, vasoactive signal transmission, and vascular reactivity. The effects of anesthesia on the spatial gap between the neural and vascular response regions are not fully understood and require further attention to elucidate the mechanism of vascular control of CBF supply to the underlying focal and surrounding neural activity. The in-depth understanding of the anesthesia actions on neurovascular elements allows for better decision-making regarding the anesthetics used in specific models for neurovascular experiments and may also help elucidate the signal source issues in hemodynamic-based neuroimaging techniques.

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“…Electrophysiological recordings [5] and optical imaging techniques have been developed through various experiments in order to obtain fast and spatially reliable functional mapping of the barrel cortex [6,7]. Intrinsic optical imaging has been used to map sensory processing in the mouse neocortex and relies on blood flow changes through coupling with neuronal activity [8]. This technique is widely used since it allows rapid and reliable measurements.…”

Section: Introductionmentioning

confidence: 99%

BOLD responses to trigeminal nerve stimulation

Just

Petersen

Gruetter

2010

Magnetic Resonance Imaging

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The current study investigates a new model of barrel cortex activation using stimulation of the infraorbital branch of the trigeminal nerve. A robust and reproducible activation of the rat barrel cortex was obtained following trigeminal nerve stimulation. Blood oxygen leveldependent (BOLD) effects were obtained in the primary somatosensory barrel cortex (S1BF), the secondary somatosensory cortex (S2) and the motor cortex. These cortical areas were reached from afferent pathways from the trigeminal ganglion, the trigeminal nuclei and thalamic nuclei from which neurons project their axons upon whisker stimulation. The maximum BOLD responses were obtained for a stimulus frequency of 1 Hz, a stimulus pulse width of 100 μs and for current intensities between 1.5 and 3 mA. The BOLD response was nonlinear as a function of frequency and current intensity. Additionally, modeling BOLD responses in the rat barrel cortex from separate cerebral blood flow (CBF) and cerebral metabolic rate of oxygen (CMRO 2 ) measurements showed good agreement with the shape and amplitude of measured BOLD responses as a function of stimulus frequency and will potentially allow to identify the sources of BOLD nonlinearities. Activation of the rat barrel cortex using trigeminal nerve stimulation will contribute to the interpretation of the BOLD signals from functional magnetic resonance imaging studies.

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Coupling between neuronal activity and microcirculation: Implications for functional brain imaging

Cited by 73 publications

References 243 publications

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

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

Anesthesia and the Quantitative Evaluation of Neurovascular Coupling

BOLD responses to trigeminal nerve stimulation

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