Neurophysiologic correlates of fMRI in human motor cortex

Hermes, Dora; Miller, Kai J.; Vansteensel, Mariska J.; Aarnoutse, Erik J.; Leijten, Frans S.S.; Ramsey, Nick F.

doi:10.1002/hbm.21314

Cited by 177 publications

(205 citation statements)

References 54 publications

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“…This remaining saturation in the measured BOLD amplitude in S1 could be explained by neuronal processes that are not captured by the HFB power but by lower frequency bands. 23,41 Although we found a significant decrease in the HFB power for subsequent movements at high movement rates, we observed no movement rate effect for the amplitude in the lower frequency, beta-band power, response (12 to 28 Hz). 17 The beta-band activity, however, remained suppressed between movements at faster movement rates in both motor and sensory cortex, in contrast with the slower movement rates where the beta-band activity recovered to baseline values.…”

Section: Discussioncontrasting

confidence: 71%

“…Studies have shown that power in higher frequencies (440 Hz) correlates well with neuronal firing rates [19][20][21] and also with BOLD signal change. 22,23 The ECoG high-frequency broadband power thus provided a direct measure of electrical activity in confined neuronal ensembles, which we compared with BOLD fMRI measurements. We examined whether addition of the measured neuro-electrophysiological response in a model for the BOLD response affects the mismatch between model-predicted andmeasured BOLD response.…”

Section: Introductionmentioning

confidence: 99%

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BOLD Consistently Matches Electrophysiology in Human Sensorimotor Cortex at Increasing Movement Rates: A Combined 7T fMRI and ECoG Study on Neurovascular Coupling

Siero

Hermes

Hoogduin

et al. 2013

J Cereb Blood Flow Metab

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Blood oxygenation level-dependent (BOLD) functional magnetic resonance imaging (fMRI) is widely used to measure human brain function and relies on the assumption that hemodynamic changes mirror the underlying neuronal activity. However, an often reported saturation of the BOLD response at high movement rates has led to the notion of a mismatch in neurovascular coupling. We combined BOLD fMRI at 7T and intracranial electrocorticography (ECoG) to assess the relationship between BOLD and neuronal population activity in human sensorimotor cortex using a motor task with increasing movement rates. Though linear models failed to predict BOLD responses from the task, the measured BOLD and ECoG responses from the same tissue were in good agreement. Electrocorticography explained almost 80% of the mismatch between measured-and model-predicted BOLD responses, indicating that in human sensorimotor cortex, a large portion of the BOLD nonlinearity with respect to behavior (movement rate) is well predicted by electrophysiology. The results further suggest that other reported examples of BOLD mismatch may be related to neuronal processes, rather than to neurovascular uncoupling.

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Section: Discussioncontrasting

confidence: 71%

Section: Introductionmentioning

confidence: 99%

BOLD Consistently Matches Electrophysiology in Human Sensorimotor Cortex at Increasing Movement Rates: A Combined 7T fMRI and ECoG Study on Neurovascular Coupling

Siero

Hermes

Hoogduin

et al. 2013

J Cereb Blood Flow Metab

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“…For functional electrode selection and the bulk of analysis reported, we focused on the event-related changes in broad-frequency high γ-power (HG; 70-180 Hz), as used by previous investigators (13,15,16). Changes in power across this frequency range reflect one of the most robust measures of local population activity as recorded by ECoG, particularly given that power in this range is functionally selective, spatially restricted (20), and well-correlated with both population firing rate (17) and fMRI responses (21). Given the RT-based variability of trial duration, we studied both stimulus onset-locked and response-locked data, but focused our quantitative comparisons upon response-locked data, as detailed below (SI Materials and Methods).…”

Section: Resultsmentioning

confidence: 99%

Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing

Foster

Dastjerdi

Parvizi

2012

Proc. Natl. Acad. Sci. U.S.A.

101

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Our understanding of the human default mode network derives primarily from neuroimaging data but its electrophysiological correlates remain largely unexplored. To address this limitation, we recorded intracranially from the human posteromedial cortex (PMC), a core structure of the default mode network, during various conditions of internally directed (e.g., autobiographical memory) as opposed to externally directed focus (e.g., arithmetic calculation). We observed late-onset (>400 ms) increases in broad high γ-power (70-180 Hz) within PMC subregions during memory retrieval. High γ-power was significantly reduced or absent when subjects retrieved self-referential semantic memories or responded to selfjudgment statements, respectively. Conversely, a significant deactivation of high γ-power was observed during arithmetic calculation, the duration of which correlated with reaction time at the signaltrial level. Strikingly, at each recording site, the magnitude of activation during episodic autobiographical memory retrieval predicted the degree of suppression during arithmetic calculation. These findings provide important anatomical and temporal details-at the neural population level-of PMC engagement during autobiographical memory retrieval and address how the same populations are actively suppressed during tasks, such as numerical processing, which require externally directed attention.electrocorticography | episodic memory | numerical cognition O ur ability to successfully direct and maintain attention to the external world relies on the coordinated activation of several putative attentional brain networks. Over the past decade brain imaging techniques, such as functional MRI (fMRI), have also revealed a select group of brain regions, now well-known as the default mode network (DMN), which deactivate during tasks of externally directed attention (1, 2). Conversely, the DMN shows higher activity during tasks requiring internally focused "self-referential" processing (3-5). Despite the many advances made by neuroimaging studies of DMN function, similar progress in the electrophysiological domain has remained relatively limited. This scarcity of investigation is mostly because the core structures of the DMN are anatomically hidden on the medial surface of the brain, and thus their location and orientation is suboptimal for detection with scalp electroencephalography (EEG). One region of particular interest is the posteromedial cortex (PMC), which is the main hub of the DMN in the human (2, 6) and nonhuman primate (7, 8) brains (Fig. 1), and encompasses the posterior cingulate cortex (PCC), retrosplenial cortex (RSC), precuneus, and Brodmann area 31 (9). Ultimately, more invasive techniques using intracranial electrophysiological recordings from the human brain are methodologically preferable for studying these regions, but obtaining such data has been rare and logistically challenging.Recent invasive electrophysiological studies of the DMN have highlighted its well-known deactivation during conditions of externally d...

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“…A wide variety of features in the local field potential (LFP) or EEG, related to several cognitive processes, have now been found to correlate with the BOLD signal (19,20,(22)(23)(24)(25)(26). Most relevant for this study, α-and β-power changes in EEG correlate negatively with the BOLD signal whereas γ-band changes have a positive relation (20,(22)(23)(24)27). Moreover, we and others have demonstrated that neuronal dynamics underlying changes in power in the γ-range contribute independently to the BOLD signal from those in the α-and β-bands (22,27).…”

mentioning

confidence: 99%

The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

Scheeringa

Koopmans

Mourik

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

158

152

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Electrophysiological recordings in animals have indicated that visual cortex γ-band oscillatory activity is predominantly observed in superficial cortical layers, whereas α-and β-band activity is stronger in deep layers. These rhythms, as well as the different cortical layers, have also been closely related to feedforward and feedback streams of information. Recently, it has become possible to measure laminar activity in humans with high-resolution functional MRI (fMRI). In this study, we investigated whether these different frequency bands show a differential relation with the laminar-resolved blood-oxygen level-dependent (BOLD) signal by combining data from simultaneously recorded EEG and fMRI from the early visual cortex. Our visual attention paradigm allowed us to investigate how variations in strength over trials and variations in the attention effect over subjects relate to each other in both modalities. We demonstrate that γ-band EEG power correlates positively with the superficial layers' BOLD signal and that β-power is negatively correlated to deep layer BOLD and α-power to both deep and superficial layer BOLD. These results provide a neurophysiological basis for human laminar fMRI and link human EEG and high-resolution fMRI to systems-level neuroscience in animals.cortical layers | oscillations | high-resolution fMRI | EEG T he different cortical layers have distinct anatomical connections with subcortical, upstream, and downstream cortical regions (1). Intracranial electrophysiological recordings in animals have linked neuronal oscillations in different frequency bands to the cortical feedforward and feedback information flow and to cortico-subcortical interactions (2-5). In line with these findings, electrophysiological recordings in animals have also demonstrated that changes in α-, β-, and γ-bands can be localized to specific cortical layers (6-12).These findings are almost exclusively based on nonhuman animal research. Although a recent study explored the feasibility of measuring laminar-specific activity with magnetoencephalography (MEG) (13), most recent advances in measuring laminar activity in humans have been made using high-resolution functional MRI (fMRI) (14-18). In this study, we make use of these recent developments to investigate the relationship between electrophysiology and the laminar-specific blood oxygen level-dependent (BOLD) signal. By simultaneously measuring EEG and high-resolution fMRI in humans performing a visual attention task, we demonstrate that changes in specific frequency bands in the EEG can be related to changes in the BOLD signal measured at different cortical depths.The BOLD signal is thought to be closely related to variations in local field potentials (19-21). A wide variety of features in the local field potential (LFP) or EEG, related to several cognitive processes, have now been found to correlate with the BOLD signal (19,20,(22)(23)(24)(25)(26). Most relevant for this study, α-and β-power changes in EEG correlate negatively with the BOLD signal whereas γ-band...

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Neurophysiologic correlates of fMRI in human motor cortex

Cited by 177 publications

References 54 publications

BOLD Consistently Matches Electrophysiology in Human Sensorimotor Cortex at Increasing Movement Rates: A Combined 7T fMRI and ECoG Study on Neurovascular Coupling

BOLD Consistently Matches Electrophysiology in Human Sensorimotor Cortex at Increasing Movement Rates: A Combined 7T fMRI and ECoG Study on Neurovascular Coupling

Neural populations in human posteromedial cortex display opposing responses during memory and numerical processing

The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

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