Cerebral Vasomotion: A 0.1-Hz Oscillation in Reflected Light Imaging of Neural Activity

doi:10.1006/nimg.1996.0069

NeuroImage

Volume 4, Issue 3, December 1996, Pages 183-193

https://doi.org/10.1006/nimg.1996.0069 Get rights and content

Abstract

Imaging of scattered and reflected light from the surface of neural structures can reveal the functional architecture within large populations of neurons. These techniques exploit, as one of the principal signal sources, reflectance changes produced by local variation in blood volume and oxygen saturation related to neural activity. We found that a major source of variability in the captured light signal is a pervasive low-frequency (0.1-Hz) oscillation which apparently results from regional cerebral blood flow. This signal is present in brain parenchyma as well as the microvasculature and exhibits many characteristics of the low-frequency “vasomotion” signals observed in peripheral microcirculation. Concurrent measurements in brain with a laser Doppler flow meter contained an almost identical low-frequency signal. The presence of the 0.1-Hz oscillation in the cerebral microcirculation could underlie a portion of the previously described characteristics reported in reflected-light imaging studies. The prevalence of the oscillatory phenomena in the brain raises substantial temporal sampling issues for optical imaging and for other visualization techniques which depend on changes in regional cerebral blood dynamics, such as functional magnetic resonance imaging.

References (0)

Cited by (293)

Dose-dependent changes in orientation amplitude maps in the cat visual cortex after propofol bolus injections
2024, IBRO Neuroscience Reports
A general intravenous anesthetic propofol (2,6-diisopropylphenol) is widely used in clinical, veterinary practice and animal experiments. It activates gamma- aminobutyric acid (GABAa) receptors. Though the cerebral cortex is one of the major targets of propofol action, no study of dose dependency of propofol action on cat visual cortex was performed yet. Also, no such investigation was done until now using intrinsic signal optical imaging. Here, we report for the first time on the dependency of optical signal in the visual cortex (area 17/area 18) on the propofol dose. Optical imaging of intrinsic responses to visual stimuli was performed in cats before and after propofol bolus injections at different doses on the background of continuous propofol infusion. Orientation amplitude maps were recorded. We found that amplitude of optical signal significantly decreased after a bolus dose of propofol. The effect was dose- and time-dependent producing stronger suppression of optical signal under the highest bolus propofol doses and short time interval after injection. In each hemisphere, amplitude at cardinal and oblique orientations decreased almost equally. However, surprisingly, amplitude at cardinal orientations in the ipsilateral hemisphere was depressed stronger than in contralateral cortex at most time intervals. As the magnitude of optical signal represents the strength of orientation tuned component, these our data give new insights on the mechanisms of generation of orientation selectivity. Our results also provide new data toward understanding brain dynamics under anesthesia and suggest a recommendation for conducting intrinsic signal optical imaging experiments on cortical functioning under propofol anesthesia.
Aging affects the phase coherence between spontaneous oscillations in brain oxygenation and neural activity
2023, Brain Research Bulletin
The risk of neurodegenerative disorders increases with age, due to reduced vascular nutrition and impaired neural function. However, the interactions between cardiovascular dynamics and neural activity, and how these interactions evolve in healthy aging, are not well understood. Here, the interactions are studied by assessment of the phase coherence between spontaneous oscillations in cerebral oxygenation measured by fNIRS, the electrical activity of the brain measured by EEG, and cardiovascular functions extracted from ECG and respiration effort, all simultaneously recorded. Signals measured at rest in 21 younger participants (31.1 ± 6.9 years) and 24 older participants (64.9 ± 6.9 years) were analysed by wavelet transform, wavelet phase coherence and ridge extraction for frequencies between 0.007 and 4 Hz. Coherence between the neural and oxygenation oscillations at ∼ 0.1 Hz is significantly reduced in the older adults in 46/176 fNIRS-EEG probe combinations. This reduction in coherence cannot be accounted for in terms of reduced power, thus indicating that neurovascular interactions change with age. The approach presented promises a noninvasive means of evaluating the efficiency of the neurovascular unit in aging and disease.
Systemic low-frequency oscillations in resting-state fMRI
2023, Advances in Resting-State Functional MRI: Methods, Interpretation, and Applications
Low-frequency oscillation (LFOs: 0.01∼0.15 Hz) signals are dominant in the blood-oxygenation-level-dependent (BOLD) resting-state fMRI. In this chapter, we will focus on one unique LFO signal, which likely has an extracerebral origin and is found to move in the brain. Because of these features, the LFOs are referred to as systemic low-frequency oscillations (sLFOs), to be distinguished from other physiological and neuronal oscillations. The source of this signal, and its method of production and propagation in the body, has not been conclusively determined. In this chapter, we will discuss the features of these sLFOs in detail, the possible physiological origins, and their applications in resting-state fMRI studies.
Cortical connectivity is embedded in resting state at columnar resolution
2022, Progress in Neurobiology
Resting state (RS) fMRI is now widely used for gaining insight into the organization of brain networks. Functional connectivity (FC) inferred from RS-fMRI is typically at macroscale, which is too coarse for much of the detail in cortical architecture. Here, we examined whether imaging RS at higher contrast and resolution could reveal cortical connectivity with columnar granularity. In longitudinal experiments (~1.5 years) in squirrel monkeys, we partitioned sensorimotor cortex using dense microelectrode mapping and then recorded RS with intrinsic signal optical imaging (RS-ISOI, 20 µm/pixel). FC maps were benchmarked against microstimulation-evoked activation and traced anatomical connections. These direct comparisons showed high correspondence in connectivity patterns across methods. The fidelity of FC maps to cortical connections indicates that granular details of network organization are embedded in RS. Thus, for recording RS, the field-of-view and effective resolution achieved with ISOI fills a wide gap between fMRI and invasive approaches (2-photon imaging, electrophysiology). RS-ISOI opens exciting opportunities for high resolution mapping of cortical networks in living animals.
Hemodynamic and metabolic correspondence of resting-state voxel-based physiological metrics in healthy adults
2022, NeuroImage
Voxel-based physiological (VBP) variables derived from blood oxygen level dependent (BOLD) fMRI time-course variations include: amplitude of low frequency fluctuations (ALFF), fractional amplitude of low frequency fluctuations (fALFF) and regional homogeneity (ReHo). Although these BOLD-derived variables can detect between-group (e.g. disease vs control) spatial pattern differences, physiological interpretations are not well established. The primary objective of this study was to quantify spatial correspondences between BOLD VBP variables and PET measurements of cerebral metabolic rate and hemodynamics, being well-validated physiological standards. To this end, quantitative, whole-brain PET images of metabolic rate of glucose (MRGlu; ¹⁸FDG) and oxygen (MRO₂; ¹⁵OO), blood flow (BF; H₂¹⁵O) and blood volume (BV; C¹⁵O) were obtained in 16 healthy controls. In the same subjects, BOLD time-courses were obtained for computation of ALFF, fALFF and ReHo images. PET variables were compared pair-wise with BOLD variables. In group-averaged, across-region analyses, ALFF corresponded significantly only with BV (R = 0.64; p < 0.0001). fALFF corresponded most strongly with MRGlu (R = 0.79; p < 0.0001), but also significantly (p < 0.0001) with MRO₂ (R = 0.68), BF (R = 0.68) and BV (R=0.68). ReHo performed similarly to fALFF, with significant strong correspondence (p < 0.0001) with MRGlu (R = 0.78), MRO₂ (R = 0.54), and, but less strongly with BF (R = 0.50) and BV (R=0.50). Mutual information analyses further clarified these physiological interpretations. When conditioned by BV, ALFF retained no significant MRGlu, MRO₂ or BF information. When conditioned by MRGlu, fALFF and ReHo retained no significant MRO₂, BF or BV information. Of concern, however, the strength of PET-BOLD correspondences varied markedly by brain region, which calls for future investigation on physiological interpretations at a regional and per-subject basis.
Astrocytes regulate ultra-slow arteriole oscillations via stretch-mediated TRPV4-COX-1 feedback
2021, Cell Reports
Citation Excerpt :
Brain microvasculature constricts and dilates to control cerebral blood flow (CBF) at very low frequencies (0.01–0.3 Hz) in response to neural activity as well as systemic influences. For example, rhythmic relaxations and contractions of microvasculature, termed vasomotion (∼0.1 Hz, range 0.05–0.3 Hz), are driven by the “ultra-slow” periodicity of intrinsic, resting-state neural activity (Martuzzi et al., 2009; Mateo et al., 2017; Mayhew et al., 1996). Here, microvasculature possess the molecular machinery for vasomotion (Aalkjær et al., 2011; Cole et al., 2019), but the timing of the oscillations is entrained by neurons.
Very-low-frequency oscillations in microvascular diameter cause fluctuations in oxygen delivery that are important for fueling the brain and for functional imaging. However, little is known about how the brain regulates ongoing oscillations in cerebral blood flow. In mouse and rat cortical brain slice arterioles, we find that selectively enhancing tone is sufficient to recruit a TRPV4-mediated Ca²⁺ elevation in adjacent astrocyte endfeet. This endfoot Ca²⁺ signal triggers COX-1-mediated “feedback vasodilators” that limit the extent of evoked vasoconstriction, as well as constrain fictive vasomotion in slices. Astrocyte-Ptgs1 knockdown in vivo increases the power of arteriole oscillations across a broad range of very low frequencies (0.01–0.3 Hz), including ultra-slow vasomotion (∼0.1 Hz). Conversely, clamping astrocyte Ca²⁺ in vivo reduces the power of vasomotion. These data demonstrate bidirectional communication between arterioles and astrocyte endfeet to regulate oscillatory microvasculature activity.

View all citing articles on Scopus

¹: To whom correspondence should be addressed at AIVRU, University of Sheffield, Sheffield, S10 2TP UK. E-mail: J.E.W.Mayhew@aivru. sheffield.ac.uk.

View full text

Regular ArticleCerebral Vasomotion: A 0.1-Hz Oscillation in Reflected Light Imaging of Neural Activity

Abstract

Regular Article
Cerebral Vasomotion: A 0.1-Hz Oscillation in Reflected Light Imaging of Neural Activity