Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest

By Amir Shmuel, David A. Leopold. Human Brain Mapping, 2008

610 citations recorded by the source corpus.

Recent studies have demonstrated large amplitude spontaneous fluctuations in functional‐MRI (fMRI) signals in humans in the resting state. Importantly, these spontaneous fluctuations in blood‐oxygenation‐level‐dependent (BOLD) signal are often synchronized over distant parts of the brain, a phenomenon termed functional‐connectivity. Functional‐connectivity is widely assumed to reflect interregional coherence of fluctuations in activity of the underlying neuronal networks. Despite the large body of human imaging literature on spontaneous activity and functional‐connectivity in the resting state, the link to underlying neural activity remains tenuous. Through simultaneous fMRI and intracortical neurophysiological recording, we demonstrate correlation between slow fluctuations in BOLD signals and concurrent fluctuations in the underlying locally measured neuronal activity. This correlation varied with time‐lag of BOLD relative to neuronal activity, resembling a traditional hemodynamic response function with peaks at ∼6 s lag of BOLD signal. The correlations were reliably detected when the neuronal signal consisted of either the spiking rate of a small group of neurons, or relative power changes in the multi‐unit activity band, and particularly in the local field potential gamma band. Analysis of correlation between the voxel‐by‐voxel fMRI time‐series and the neuronal activity measured within one cortical site showed patterns of correlation that slowly traversed cortex. BOLD fluctuations in widespread areas in visual cortex of both hemispheres were significantly correlated with neuronal activity from a single recording site in V1. To the extent that our V1 findings can be generalized to other cortical areas, fMRI‐based functional‐connectivity between remote regions in the resting state can be linked to synchronization of slow fluctuations in the underlying neuronal signals. Hum Brain Mapp 2008. © 2008 Wiley‐Liss, Inc.

Subfields: Cognitive Neuroscience, Radiology, Nuclear Medicine and Imaging

View Paper: https://www.semanticscholar.org/paper/c8c084b6e1f73ec67ebaf8004e80303206e296eb

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Citations in the corpus

Efficiency of Functional Brain Networks and Intellectual Performance (2009, background): “This latter view is supported by recent observations that report that resting state BOLD time-series show a high correlation with concurrent fluctuations in neuronal spiking, suggesting a direct link between resting-state time-lag BOLD signals and intrinsic neuronal activity (Nir et al., 2008; Shmue”
Exploring mechanisms of spontaneous functional connectivity in MEG: How delayed network interactions lead to structured amplitude envelopes of band-pass filtered oscillations (2014, neutral): “…the neurophysiological counterpart of resting-state BOLD signal fluctuations using simultaneous fMRI and intra-cranial recordings (Nir et al., 2008; Shmuel and Leopold, 2008), simultaneous fMRI and EEG (de Munck et al., 2007; Difrancesco et al., 2008; Goldman et al., 2002; Laufs et al., 2003b;…”
Role of local network oscillations in resting-state functional connectivity (2011, methodology): “…with experimental data, in the direction of reproducing the more recent experimental findings at the neural activity level (Leopold et al., 2003; Shmuel and Leopold, 2008;Nir et al., 2008; He et al., 2008;Miller et al., 2009; Schölvinck et al., 2010), where neural activity markers of RSNs have…”
Spectral fingerprints of large-scale neuronal interactions (2012, background): “and seem to be closely linked to slow co-modulations of spontaneous fMRI signal fluctuations in distant cortical region”
Small-world and scale-free organization of voxel-based resting-state functional connectivity in the human brain (2008, neutral): “In this context, it is believed that the resting-state BOLD fluctuations of cortical and sub-cortical regions, at least in part, originate from intrinsic neuronal activity (Biswal et al., 1995; Greicius et al., in press; Gusnard et al., 2001; Shmuel and Leopold, 2008) and that the observed temporal ”
Functionally linked resting‐state networks reflect the underlying structural connectivity architecture of the human brain (2009, background): “Furthermore, resting-state BOLD fluctuations have been reported to strongly correlate with concurrent fluctuations in neuronal spiking [Shmuel and Leopold, 2008], linking resting-state fMRI time-series directly to neuronal activation and synchronization [Shmuel and Leopold, 2008].”
Functional segmentation of the brain cortex using high model order group PICA (2009, background): “Intracortical local ﬁeld potential and multiunit activity ﬂuctuations partly correlate with the ﬂuctuations of the BOLD signal with a six second lag in anesthetized conditions [Logothetis et al., 2001; Shmuel and Leopold, 2008].”
EEG correlates of time-varying BOLD functional connectivity (2013, neutral): “Gamma-band power may also be relevant, as fluctuations in gamma power have been found to correlate with spontaneous BOLD signal activity on spatially widespread scales (Scholvinck et al., 2010; Shmuel and Leopold, 2008).”
Exploring the brain network: a review on resting-state fMRI functional connectivity. (2010, background): “…resting-state fMRI correlations and electrophysiological recordings of neuronal firing (Nir et al., 2008) and from studies showing a strong association between spontaneous BOLD fluctuations and simultaneous measured fluctuations in neuronal spiking (Shmuel and Leopold, 2008; Shmuel et al., 2002).”
The role of physiological noise in resting-state functional connectivity (2012, neutral): “, 2009), and even direct recordings in animal models (Leopold and Logothetis, 2003; Leopold et al., 2003; Shmuel and Leopold, 2008).”
Dynamic functional connectivity: Promise, issues, and interpretations (2013, background): “…allowing invasive, multimodal studies that can compare electrical measures of neural activity to the indirect response of the BOLD signal (Brinker et al., 1999; Logothetis et al., 2001; Lu et al., 2007; Magri et al., 2012; Pan et al., 2010, 2011; Schölvinck et al., 2010; Shmuel and Leopold, 2008).”
Multi-level bootstrap analysis of stable clusters in resting-state fMRI (2009, methodology): “…et al., 2009), diffusion imaging (Damoiseaux and Greicius, 2009), maps of anatomical connectivity derived using retrograde tracers in macaques (Vincent et al., 2007; Margulies et al., 2009) and electrophysiology either on the scalp (Laufs et al., 2003) or on the cortex (Shmuel and Leopold, 2008).”