Functional MRI (fMRI) has uncovered widespread hemodynamic fluctuations in the brain during rest. Recent electroencephalographic work in humans and microelectrode recordings in anesthetized monkeys have shown this activity to be correlated with slow changes in neural activity. Here we report that the spontaneous fluctuations in the local field potential (LFP) measured from a single cortical site in monkeys at rest exhibit widespread, positive correlations with fMRI signals over nearly the entire cerebral cortex. This correlation was especially consistent in a band of upper gamma-range frequencies (40-80 Hz), for which the hemodynamic signal lagged the neural signal by 6-8 s. A strong, positive correlation was also observed in a band of lower frequencies (2-15 Hz), albeit with a lag closer to zero. The global pattern of correlation with spontaneous fMRI fluctuations was similar whether the LFP signal was measured in occipital, parietal, or frontal electrodes. This coupling was, however, dependent on the monkey's behavioral state, being stronger and anticipatory when the animals' eyes were closed. These results indicate that the often discarded global component of fMRI fluctuations measured during the resting state is tightly coupled with underlying neural activity.cortex | electrophysiology | local field potential | functional connectivity | monkey T he mammalian cerebral cortex is subdivided into specialized regions for various cognitive functions, such as the processing of sensory stimuli, memory, and the execution of movements. This functional specialization notwithstanding, the brain does not cease to show pronounced dynamic activity in the absence of cognitive or sensory stimulation. Significant ongoing spontaneous activity has been demonstrated using optical (1, 2), electrophysiological (3-5), and functional imaging (6, 7) techniques in several species under a variety of behavioral states. FMRI allows for visualization of large-scale, spatial patterns of such intrinsic activity, which is achieved by mapping patterns of activity covariation between brain regions. The temporal correlation between fluctuations in different regions is then often taken as a measure of "functional connectivity" between the corresponding brain areas (8-11). These fluctuations typically exhibit their highest intervoxel coherence at low temporal frequencies (<0.1 Hz) and can be observed during alertness (12, 13), sleep (14, 15), light sedation (16), and general anesthesia (17,18). Experiments are beginning to address the spatiotemporal characteristics of these spontaneous fluctuations in animal models (19)(20)(21), with initial studies in macaques suggesting a human-like pattern of functional connectivity (7,22).In humans, spontaneous activity is typically investigated in the so-called resting state, a term that is only loosely defined and which typically amounts to a subject lying in the scanner without an explicit stimulus or task. Under these conditions, analysis of spatiotemporal coherence of fMRI activity reveals several distin...
Summary While the mammalian neocortex has a clear laminar organization, layer-specific neuronal computations remain to be uncovered. Several studies suggest that gamma band activity in primary visual cortex (V1) is produced in granular and superficial layers and is associated with the processing of visual input [1–3]. Oscillatory alpha band activity in deeper layers has been proposed to modulate neuronal excitability associated with changes in arousal and cognitive factors [4–7]. To investigate the layer-specific interplay between these two phenomena, we characterized the coupling between alpha and gamma band activity of the local field potential (LFP) in V1 of the awake macaque. Using multicontact laminar electrodes to measure spontaneous signals simultaneously from all layers of V1, we found a robust coupling between alpha phase in the deeper layers and gamma amplitude in granular and superficial layers. Moreover, the power in the two frequency bands was anticorrelated. Taken together, these findings demonstrate robust inter-laminar cross-frequency coupling in the visual cortex, supporting the view that neuronal activity in the alpha frequency range phasically modulates processing in the cortical microcircuit in a top-down manner [7].
Spatial patterns of spontaneous neural activity at rest have previously been associated with specific networks in the brain, including those pertaining to the functional architecture of the primary visual cortex (V1). However, despite the prominent anatomical differences between cortical layers, little is known about the laminar pattern of spontaneous activity in V1. We address this topic by investigating the amplitude and coherence of ongoing local field potential (LFP) signals measured from different layers in V1 of macaque monkeys during rest and upon presentation of a visual stimulus. We used a linear microelectrode array to measure LFP signals at multiple, evenly spaced positions throughout the cortical thickness. Analyzing both the mean LFP amplitudes and between-contact LFP coherences, we identified two distinct zones of activity, roughly corresponding to superficial and deep layers, divided by a sharp transition near the bottom of layer 4. The LFP signals within each laminar zone were highly coherent, whereas those between zones were not. This functional compartmentalization was found not only during rest, but also when the receptive field was stimulated during a visual task. These results demonstrate the existence of distinct superficial and deep functional domains of coherent LFP activity in V1 that may reflect the intrinsic interplay of V1 microcircuitry with cortical and subcortical targets, respectively.
The role of primary visual cortex (V1) in determining the contents of perception is controversial. Human functional imaging (fMRI) studies of perceptual suppression have revealed a robust drop in V1 activity when a stimulus is subjectively invisible. In contrast, monkey single unit recordings have failed to demonstrate such perception locked changes in V1. To investigate the basis of this discrepancy, we measured both the blood oxygenation level-dependent (BOLD) response and several electrophysiological signals in two behaving monkeys. We found that during conventional stimulus presentation, all signals were in good agreement, showing strong visual modulation to presentation and removal of a stimulus. However, during perceptual suppression, only the BOLD response and low frequency local field potential (LFP) signals exhibited decreases, while the spiking and high frequency LFP signals were unaffected. These results demonstrate that the coupling between the BOLD and electrophysiological signals in V1 is context dependent, with a marked dissociation occurring during perceptual suppression.
During the viewing of certain patterns, widely known as ambiguous or puzzle figures, perception lapses into a sequence of spontaneous alternations, switching every few seconds between two or more visual interpretations of the stimulus. Although their nature and origin remain topics of debate, these stochastic switches are generally thought to be the automatic and inevitable consequence of viewing a pattern without a unique solution. We report here that in humans such perceptual alternations can be slowed, and even brought to a standstill, if the visual stimulus is periodically removed from view. We also show, with a visual illusion, that this stabilizing effect hinges on perceptual disappearance rather than on actual removal of the stimulus. These findings indicate that uninterrupted subjective perception of an ambiguous pattern is required for the initiation of the brain-state changes underlying multistable vision.
During the viewing of certain patterns, widely known as ambiguous or puzzle figures, perception lapses into a sequence of spontaneous alternations, switching every few seconds between two or more visual interpretations of the stimulus. Although their nature and origin remain topics of debate, these stochastic switches are generally thought to be the automatic and inevitable consequence of viewing a pattern without a unique solution. We report here that in humans such perceptual alternations can be slowed, and even brought to a standstill, if the visual stimulus is periodically removed from view. We also show, with a visual illusion, that this stabilizing effect hinges on perceptual disappearance rather than on actual removal of the stimulus. These findings indicate that uninterrupted subjective perception of an ambiguous pattern is required for the initiation of the brain-state changes underlying multistable vision.
A local field potential (LFP) response can be measured throughout the visual cortex in response to the abrupt appearance of a visual stimulus. Averaging LFP responses to many stimulus presentations isolates transient, phase-locked components of the response that are consistent from trial to trial. However, stimulus responses are also composed of sustained components, which differ in their phase from trial to trial and therefore must be evaluated using other methods, such as computing the power of the response of each trial before averaging. Here, we investigate the basis of phase-locked and non-phase-locked LFP responses in the primary visual cortex of the macaque monkey using a novel variant of current source density (CSD) analysis. We applied a linear array of electrode contacts spanning the thickness of the cortex to measure the LFP and compute band-limited CSD power to identify the laminar sites of persistent current exchange that may be the basis of sustained visual LFP responses. In agreement with previous studies, we found a short-latency phaselocked current sink, thought to correspond to thalamocortical input to layer 4C. In addition, we found a prominent non-phase-locked component of the CSD that persisted as long as the stimulus was physically present. The latter was relatively broadband, lasted throughout the stimulus presentation, and was centered ϳ500 m deeper than the initial current sink. These findings demonstrate a fundamental difference in the neural mechanisms underlying the initial and sustained processing of simple visual stimuli in the V1 microcircuit.
We postulate that the stabilization observed with repetitive presentation of ambiguous patterns can be at least partially accounted for by processes that retain a recent perceptual interpretation, and we speculate that such memory may be important in natural vision. We further propose that the interleaved paradigm introduced here may be of great value to gauge aspects of stimulus similarity that appeal to particular mechanisms of perceptual organization.
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