Functional Signal- and Paradigm-Dependent Linear Relationships between Synaptic Activity and Hemodynamic Responses in Rat Somatosensory Cortex

Nemoto, Minoru; Sheth, Sameer A.; Guiou, Michael; Pouratian, Nader; Chen, James W. Y.; Toga, Arthur W.

doi:10.1523/jneurosci.4870-03.2004

Cited by 99 publications

(84 citation statements)

References 60 publications

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“…Thus we attribute the observed parenchyma patches mostly to a passive, highly local increase in [Hbr], which is attributable to an increase in oxygen extraction by the activated neurons or the surrounding glia rather than to effects of the active blood-volume response. After ϳ2 s, also at 605 nm, blood vessels became predominant because of the large CBV and CBF response, as seen in previous experiments performed on anesthetized and awake preparations (Frostig et al, 1990;Grinvald et al, 2000;Nemoto et al, 2004). To increase the SNR in the functional single-condition maps, the first 0.8 s of Figure 6 and stretched to Ϯ1.5 SD.…”

Section: Oximetric Functional Maps Estimated By Reflection Measuremenmentioning

confidence: 87%

“…Recent evidence suggests that the active vascular response (underlying the positive BOLD signal) reflects synaptic rather than spiking activity (Caesar et al, 2003a,b;Logothetis, 2003), whereas the stimulus-evoked tissue deoxygenation underlying the initial dip has been found to correlate, at least spatially, with spiking activity (Thompson et al, 2003). Furthermore, Sheth et al (2003) and Nemoto et al (2004) found that field potential measurements correlated differently with the 570 nm and the early 605 nm optical signals. This raises the question of whether some of the observed differences between the functional maps obtained using the initial hypo-oxygenation and those obtained using the CBV response might not result from a different coupling of the two hemodynamic processes to spiking and synaptic activity, respectively.…”

Section: Implications For Functional Brain Imagingmentioning

confidence: 99%

“…Such high absorption could be achieved using relatively low dye concentrations, which did not affect the physiology of the preparation because, unlike in previous studies using Texas Red (Frostig et al, 1990), the excitation and emission peaks of the probe were far from the range of high hemoglobin absorption. In previous reports (Grinvald et al, 1986;Frostig et al, 1990;Malonek et al, 1997;Grinvald, 1999, 2001;Erinjeri and Woolsey, 2002;Nemoto et al, 2004), the activity-dependent CBV changes have been studied simply by imaging reflection changes at published isosbestic wavelengths. Because of the large amplitude of the overall CBV response investigated in those studies, it was possible to ignore several possible artifacts affecting the measurements, notably the effects of oximetric contributions attributable to small deviations of the hemoglobin absorption spectra in vivo with respect to the published in vitro values (but see Sheth et al, 2004), RBC density (hematocrit) changes and static and dynamic intercompartmental inhomogeneities, nonideal illumination filters of finite width, and possibly light-scattering changes.…”

Section: Activity-dependent Oximetric and Red Blood Cell Density Changesmentioning

confidence: 99%

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Compartment-Resolved Imaging of Activity-Dependent Dynamics of Cortical Blood Volume and Oximetry

Vanzetta¹,

Hildesheim²,

Grinvald³

2005

J. Neurosci.

115

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Optical imaging, positron emission tomography, and functional magnetic resonance imaging (fMRI) all rely on vascular responses to image neuronal activity. Although these imaging techniques are used successfully for functional brain mapping, the detailed spatiotemporal dynamics of hemodynamic events in the various microvascular compartments have remained unknown. Here we used highresolution optical imaging in area 18 of anesthetized cats to selectively explore sensory-evoked cerebral blood-volume (CBV) changes in the various cortical microvascular compartments. To avoid the confounding effects of hematocrit and oximetry changes, we developed and used a new fluorescent blood plasma tracer and combined these measurements with optical imaging of intrinsic signals at a near-isosbestic wavelength for hemoglobin (565 nm). The vascular response began at the arteriolar level, rapidly spreading toward capillaries and venules. Larger veins lagged behind. Capillaries exhibited clear blood-volume changes. Arterioles and arteries had the largest response, whereas the venous response was smallest. Information about compartment-specific oxygen tension dynamics was obtained in imaging sessions using 605 nm illumination, a wavelength known to reflect primarily oximetric changes, thus being more directly related to electrical activity than CBV changes. Those images were radically different: the response began at the parenchyma level, followed only later by the other microvascular compartments. These results have implications for the modeling of fMRI responses (e.g., the balloon model). Furthermore, functional maps obtained by imaging the capillary CBV response were similar but not identical to those obtained using the early oximetric signal, suggesting the presence of different regulatory mechanisms underlying these two hemodynamic processes.

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Section: Oximetric Functional Maps Estimated By Reflection Measuremenmentioning

confidence: 87%

Section: Implications For Functional Brain Imagingmentioning

confidence: 99%

Section: Activity-dependent Oximetric and Red Blood Cell Density Changesmentioning

confidence: 99%

See 1 more Smart Citation

Compartment-Resolved Imaging of Activity-Dependent Dynamics of Cortical Blood Volume and Oximetry

Vanzetta¹,

Hildesheim²,

Grinvald³

2005

J. Neurosci.

115

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“…The [HbT] signal is as rapid and spatially focused and more than an order of magnitude stronger and longer-lived. For ISOI maps, e.g., of orientation, the initial dip has been reported to give cleaner maps than the [HbT] signal, i.e., with fewer vascular artifacts (1,10 (5).…”

Section: Discussionmentioning

confidence: 99%

“…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).…”

mentioning

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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Functional Neuroimaging of Nociceptive and Pain‐Related Activity in the Spinal Cord and Brain: Insights From Neurovascular Coupling Studies

Paquette

Jeffrey-Gauthier

Leblond

et al. 2018

The Anatomical Record

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Spinal cord and brain processes underlie pain perception, which produces systemic cardiovascular changes. In turn, the autonomic nervous system regulates vascular function in the spinal cord and brain in order to adapt to these systemic changes, while neuronal activity induces local vascular changes. Thus, autonomic regulation and pain processes in the brain and spinal cord are tightly linked and interrelated. The objective of this topical review is to discuss work on neurovascular coupling during nociceptive processing in order to highlight supporting evidence and limitations for the use of cerebral and spinal fMRI to investigate pain mechanisms and spinal nociceptive processes. Work on functional neuroimaging of pain is presented and discussed in relation to available neurovascular coupling studies and related issues. Perspectives on future work are also discussed with an emphasis on differences between the brain and the spinal cord and on different approaches that may be useful to improve current methods, data analyses and interpretation. In summary, this review highlights the lack of data on neurovascular coupling during nociceptive stimulation and indicates that hemodynamic and BOLD responses measured with fMRI may be biased by nonspecific vascular changes. Future neuroimaging studies on nociceptive and pain-related processes would gain further understanding of neurovascular coupling in the brain and spinal cord and should take into account the effects of systemic vascular changes that may affect hemodynamic responses. Anat Rec, 301:1585-1595, 2018. © 2018 Wiley Periodicals, Inc.

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Functional Signal- and Paradigm-Dependent Linear Relationships between Synaptic Activity and Hemodynamic Responses in Rat Somatosensory Cortex

Cited by 99 publications

References 60 publications

Compartment-Resolved Imaging of Activity-Dependent Dynamics of Cortical Blood Volume and Oximetry

Compartment-Resolved Imaging of Activity-Dependent Dynamics of Cortical Blood Volume and Oximetry

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

Functional Neuroimaging of Nociceptive and Pain‐Related Activity in the Spinal Cord and Brain: Insights From Neurovascular Coupling Studies

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