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

516

490

Functional imaging of the human brain is an increasingly important technique for clinical and cognitive neuroscience research, with functional MRI (fMRI) of the blood oxygen level-dependent (BOLD) response and electroencephalography or magnetoencephalography (MEG) recordings of neural oscillations being 2 of the most popular approaches. However, the neural and physiological mechanisms that generate these responses are only partially understood and sources of interparticipant variability in these measures are rarely investigated. Here, we test the hypothesis that the properties of these neuroimaging metrics are related to individual levels of cortical inhibition by combining magnetic resonance spectroscopy to quantify resting GABA concentration in the visual cortex, MEG to measure stimulus-induced visual gamma oscillations and fMRI to measure the BOLD response to a simple visual grating stimulus. Our results demonstrate that across individuals gamma oscillation frequency is positively correlated with resting GABA concentration in visual cortex (R ‫؍‬ 0.68; P < 0.02), BOLD magnitude is inversely correlated with resting GABA (R ‫؍‬ ؊0.64; P < 0.05) and that gamma oscillation frequency is strongly inversely correlated with the magnitude of the BOLD response (R ‫؍‬ ؊0.88; P < 0.001). Our results are therefore supportive of recent theories suggesting that these functional neuroimaging metrics are dependent on the excitation/inhibition balance in an individual's cortex and have important implications for the interpretation of functional imaging results, particularly when making between-group comparisons in clinical research.functional magnetic resonance imaging ͉ magnetic resonance spectroscopy ͉ magnetoencephalography ͉ oscillations T he high spatial resolution and noninvasive nature of blood oxygen level-dependent (BOLD) functional MRI (fMRI) (1) have led to it becoming one of the most popular tools for measuring brain function in human neuroscience. However, fMRI provides only an indirect measure of neural activity by measuring task-related changes in cerebral haemodynamics that are coupled by a complex and only partially understood mechanism to changes in underlying neural activity. Recent evidence suggests that oscillations in the gamma frequency range, loosely defined as approximately 30-100 Hz, are well correlated temporally, spatially, and functionally with haemodynamic changes in cortex, suggesting a close relationship with the BOLD response (2-6). There is also increasing evidence that the most plausible mechanism for the generation of gamma oscillations is a neuronal network containing a mixture of interconnected pyramidal cells and GABAergic inhibitory interneurons (7-10) with the balance of excitation-inhibition setting the peak gamma oscillation frequency of the network (11). Similarly, it has recently been argued that the magnitude of the BOLD response is also sensitive to this excitation-inhibition balance (12, 13).In the current study, we tested the hypothesis that the local level of inhibition in an i...

Section: Discussionmentioning

confidence: 99%

Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans

Muthukumaraswamy

Edden

Jones

et al. 2009

516

490

“…Moreover, by taking advantage of the possibility to measure these parameters for each individual RBC (i.e., instantaneous values), we observed that the inst.RBC linear density varied continuously, more significantly than and independently of the inst.RBC velocity. The f luctuations of inst.RBC linear density or inst.RBC velocity were too rapid to be related to the 0.1-Hz vasomotion oscillations (38) and were present in conditions of normoxia (see Methods). To explain the independence of these two parameters, we hypothesize that a RBC arriving at capillary bifurcation with constant velocity will be directed to one of the two branches according primarily to the branch f low impedance but also to the bifurcation angle and the spatial orientation of the RBC (39).…”

Section: Discussionmentioning

confidence: 99%

Two-photon imaging of capillary blood flow in olfactory bulb glomeruli

Chaigneau

Oheim

Audinat

et al. 2003

280

239

Analysis of the spatiotemporal coupling between neuronal activity and cerebral blood flow requires the precise measurement of the dynamics of RBC flow in individual capillaries that irrigate activated neurons. Here, we use two-photon microscopy in vivo to image individual RBCs in glomerular capillaries in the rat dorsal olfactory bulb. We find that odor stimulation evokes capillary vascular responses that are odorant-and glomerulus-specific. These responses consist of increases as well as decreases in RBC flow, both resulting from independent changes in RBC velocity or linear density. Finally, measuring RBC flow with micrometer spatial resolution and millisecond temporal resolution, we demonstrate that, in olfactory bulb superficial layers, capillary vascular responses precisely outline regions of synaptic activation.N oninvasive imaging techniques have been widely used to determine the distributions of brain regions activated by sensory stimulations. Although several techniques detect contrast changes based on activity-dependent hemodynamic changes, the precise coupling between neuronal activation, energy demand, and changes in blood flow remains unclear (for review, see refs. 1-3). Analysis of the coupling requires a simultaneous measurement of the activity of neurons and the dynamics of local blood flow. Recently, measurements of extracellular activity combined with functional MRI (fMRI) have shown that field potential amplitude (4) and spiking frequency (5) are related to blood oxygen level-dependent (BOLD) signals (6, 7). These observations are a technical tour de force; yet, the spatial and temporal resolutions of fMRI are not sufficient to provide a precise understanding of the entire chain of cellular and vascular events elicited by the stimulation. In the cerebellar cortex, recent ''semiinvasive'' techniques requiring a craniotomy and using electrophysiological recordings combined with laser Doppler flowmetry have allowed more precise investigations and have demonstrated that the relationship between presynaptic and postsynaptic activity with blood flow varies according to the activated input (8-11). However, these studies did not measure blood flow in the individual capillaries that precisely irrigate the activated neurons, a prerequisite to analyzing the neurovascular coupling in detail.Two-photon microscopy imaging of blood flow represents an alternative approach to studying this coupling (12) in vivo. It allows measurements of RBC flow with micrometer spatial resolution and millisecond temporal resolution in individual capillaries and can be combined with electrophysiological recordings (13,14). If performed in a brain region where synaptic interactions are topographically organized, two-photon imaging should allow measurements of vascular flow in a given capillary irrigating a small population of neurons and glial cells. Because of its anatomical and functional organization, the rodent main olfactory bulb (15) is particularly suitable for such a study: all sensory cells expressing a given odorant r...

“…The main contribution to the optical signal is due to the metabolically induced changes in the microcirculation (28) and, thus, inherits all cardiovascular artifacts. The major components of the hemodynamics are cyclic: heart beat, respiration, and vasomotor signal (29). Conventional methods of intrinsic optical imaging have been used for functional mapping of the auditory cortex (30)(31)(32)(33)).…”

mentioning

confidence: 99%

Fine functional organization of auditory cortex revealed by Fourier optical imaging

Kalatsky

Polley

Merzenich

et al. 2005

123

146

We provide an overall view of the functional tonotopic organization of the auditory cortex in the rat. We apply a recently developed technique for acquiring intrinsic signal optical maps, Fourier imaging, in the rat auditory cortex. These highly detailed maps, derived in a several-minute-long recording procedure, delineate multiple auditory cortical areas and demonstrate their shapes, sizes, and tonotopic order. Beyond the primary auditory cortex, there are at least three distinct areas with fine-scale tonotopic organization, as well as at least one additional high-frequency field. The arrangement of all of these cortical areas is consistent across subjects. The accuracy of these optical maps was confirmed by microelectrode mapping in the same subjects. This imaging method allows fast mapping of the auditory cortex at high spatial resolution comparable to that provided by conventional microelectrode technique. Although spiking activity is largely responsible for the evoked intrinsic signals, certain features of the optical signal cannot be explained by spiking activity only, and should probably be attributed to other mechanisms inducing metabolic activity, such as subthreshold membrane phenomena.optical imaging of intrinsic signals ͉ rat ͉ tonotopy ͉ cortical maps