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

Scheeringa, René; Koopmans, Peter J.; Mourik, Tim van; Jensen, Ole; Norris, David G.

doi:10.1073/pnas.1522577113

Cited by 158 publications

(188 citation statements)

References 74 publications

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“…The power effect in the current study was broadly limited to gamma band (24–150 Hz), and oscillations in this frequency range show a robust relationship with BOLD responses (Boorman et al, 2015; Hutchison et al, 2015; Scheeringa et al, 2016), rendering the two findings rather consistent. Interestingly, other fMRI studies on anxiety-like behavior in approach–avoidance conflict have also suggested an encoding of conflict per se and/or action tendencies in multivariate patterns of hippocampal BOLD signal (O'Neil et al, 2015; Loh et al, 2017).…”

Section: Discussionsupporting

confidence: 49%

Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model

et al. 2017

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Neural oscillations in hippocampus and medial prefrontal cortex (mPFC) are a hallmark of rodent anxiety models that build on conflict between approach and avoidance. Yet, the function of these oscillations, and their expression in humans, remain elusive. Here, we used magnetoencephalography (MEG) to investigate neural oscillations in a task that simulated approach–avoidance conflict, wherein 23 male and female human participants collected monetary tokens under a threat of virtual predation. Probability of threat was signaled by color and learned beforehand by direct experience. Magnitude of threat corresponded to a possible monetary loss, signaled as a quantity. We focused our analyses on an a priori defined region-of-interest, the bilateral hippocampus. Oscillatory power under conflict was linearly predicted by threat probability in a location consistent with right mid-hippocampus. This pattern was specific to the hippocampus, most pronounced in the gamma band, and not explained by spatial movement or anxiety-like behavior. Gamma power was modulated by slower theta rhythms, and this theta modulation increased with threat probability. Furthermore, theta oscillations in the same location showed greater synchrony with mPFC theta with increased threat probability. Strikingly, these findings were not seen in relation to an increase in threat magnitude, which was explicitly signaled as a quantity and induced similar behavioral responses as learned threat probability. Thus, our findings suggest that the expression of hippocampal and mPFC oscillatory activity in the context of anxiety is specifically linked to threat memory. These findings resonate with neurocomputational accounts of the role played by hippocampal oscillations in memory.SIGNIFICANCE STATEMENT We use a biologically relevant approach–avoidance conflict test in humans while recording neural oscillations with magnetoencephalography to investigate the expression and function of hippocampal oscillations in human anxiety. Extending nonhuman studies, we can assign a possible function to hippocampal oscillations in this task, namely threat memory communication. This blends into recent attempts to elucidate the role of brain synchronization in defensive responses to threat.

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Section: Discussionsupporting

confidence: 49%

Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model

et al. 2017

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“…Therefore, studies using laminar fMRI have typically divided gray matter into several evenly spaced bins, as an approximation of the underlying cortical laminae ( Figure 1A and B). Consistent with the known functional architecture of the cortical column, these studies find feedback responses in deep and superficial, but not middle, cortical bins Kok et al, 2016;Muckli et al, 2015;Scheeringa et al, 2016). …”

Section: Forward Backward and Lateral Message-passing Within The Nesupporting

confidence: 71%

“…In this review, we have described some recent successful applications of laminar fMRI that characterized bottom-up and top-down responses in the contexts of visual prediction (Kok et al, 2016;Muckli et al, 2015) and selective attention Scheeringa et al, 2016). We have also outlined other areas of cognitive neuroscience research that stand to gain new insights from laminar fMRI, offering some specific hypotheses from the literature that yield testable predictions for laminar fMRI experiments.…”

Section: Discussionmentioning

confidence: 99%

“…Effects of attention in sensory cortex, therefore, could be expected to be most pronounced in superficial and deep layers, where feedback projections terminate (Anderson & Martin, 2009;Rockland & Virga, 1989). Indeed, a combined human laminar fMRI and EEG study found that BOLD responses in superficial and deep layers of early visual cortex covaried with EEG oscillations that occurred in response to an attentional task manipulation (Scheeringa et al, 2016). Furthermore, another laminar fMRI study shows that frequency tuning curves in human primary auditory cortex sharpen towards an attended tone, and that this sharpening is more pronounced in superficial compared to other layers .…”

Section: Selective Attentionmentioning

confidence: 99%

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Laminar fMRI: Applications for cognitive neuroscience

et al. 2019

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Highlights Recent developments in high spatial resolution fMRI allow for functional imaging of human cortical layers (laminar fMRI)  Feedforward and feedback responses can be dissociated by their laminar profiles  In vivo measurements of feedforward and feedback responses in humans with laminar fMRI have many, far-reaching applications for cognitive neuroscience  We review recent laminar fMRI studies, and several areas of cognitive neuroscience that stand to benefit from this exciting technological development AbstractThe cortex is a massively recurrent network, characterised by feedforward and feedback connections between brain areas as well as lateral connections within an area. areas at a more fine-grained level than previously possible in the human species. In this review,we highlight recent studies that successfully used laminar fMRI to isolate layer-specific feedback responses in human sensory cortex. In addition, we review several areas of cognitive neuroscience that stand to benefit from this new technological development, highlighting contemporary hypotheses that yield testable predictions for laminar fMRI. We hope to encourage researchers with the opportunity to embrace this development in fMRI research, as we expect that many future advancements in our current understanding of human brain function will be gained from measuring lamina-specific brain responses.

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“…Using variance in one type of response to guide analysis of another response provides a unique opportunity to bootstrap the spatial resolution of fMRI and temporal resolution of EEG. For example, Scheering, Koopmans, Van Mourik, Jensen, and Norris (2016) use combined EEG/fMRI to show the laminar specific origin of oscillatory EEG responses (e.g. that gamma-band EEG is linked to BOLD responses in superficial cortical lamina); thereby replicating in human cortex observations that could previously only have been obtained from invasive methods.…”

Section: Future Directionsmentioning

confidence: 99%