Periodic Non-Sinusoidal Activity Can Produce Cross-Frequency Coupling in Cortical Signals in the Absence of Functional Interaction Between Neural Sources

Gerber, Edden M.; Sadeh, Boaz; Ward, Andrew; Knight, Robert T.; Deouell, Leon Y.

doi:10.1101/062190

Cited by 4 publications

(3 citation statements)

References 28 publications

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“…Additionally, the observed temporal dynamics of sharp waveforms and nested oscillations imply that both mechanisms must occur in concert for successful memory. Importantly, this confirmation of distinct neural mechanisms in human cortex as measured with PAC adds evidence to the emerging field of waveform based inference on the neurophysiological mechanisms underlying iEEG (Sherman et al, 2016; Gerber et al, 2016; Cole et al, 2016). …”

Section: Discussionsupporting

confidence: 54%

Dual origins of measured phase-amplitude coupling reveal distinct neural mechanisms underlying episodic memory in the human cortex

et al. 2017

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Phase-amplitude coupling (PAC) is hypothesized to coordinate neural activity, but its role in successful memory formation in the human cortex is unknown. Measures of PAC are difficult to interpret, however. Both increases and decreases in PAC have been linked to memory encoding, and PAC may arise due to different neural mechanisms. Here, we use a waveform analysis to examine PAC in the human cortex as participants with intracranial electrodes performed a paired associates memory task. We found that successful memory formation exhibited significant decreases in left temporal lobe and prefrontal cortical PAC, and these two regions exhibited changes in PAC within different frequency bands. Two underlying neural mechanisms, nested oscillations and sharp waveforms, were responsible for the changes in these regions. Our data therefore suggest that decreases in measured cortical PAC during episodic memory reflect two distinct underlying mechanisms that are anatomically segregated in the human brain.

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Section: Discussionsupporting

confidence: 54%

Dual origins of measured phase-amplitude coupling reveal distinct neural mechanisms underlying episodic memory in the human cortex

et al. 2017

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“…Spectral analysis of periodic signals whose wave morphologies systematically mismatch a given filter kernel (i.e., wavelet, sine/cosine) will produce harmonics, and in consequence, spurious CFC (Lozano-Soldevilla, 2015 ). This observation has been recently replicated by various independent research groups (Cole et al, 2016 ; Gerber et al, 2016 ; Jones, 2016 ; Scheffer-Teixeira and Tort, 2016 ).…”

Section: Discussionmentioning

confidence: 68%

Neuronal Oscillations with Non-sinusoidal Morphology Produce Spurious Phase-to-Amplitude Coupling and Directionality

Lozano-Soldevilla

Huurne

Oostenveld

2016

Front. Comput. Neurosci.

126

143

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Neuronal oscillations support cognitive processing. Modern views suggest that neuronal oscillations do not only reflect coordinated activity in spatially distributed networks, but also that there is interaction between the oscillations at different frequencies. For example, invasive recordings in animals and humans have found that the amplitude of fast oscillations (>40 Hz) occur non-uniformly within the phase of slower oscillations, forming the so-called cross-frequency coupling (CFC). However, the CFC patterns might be influenced by features in the signal that do not relate to underlying physiological interactions. For example, CFC estimates may be sensitive to spectral correlations due to non-sinusoidal properties of the alpha band wave morphology. To investigate this issue, we performed CFC analysis using experimental and synthetic data. The former consisted in a double-blind magnetoencephalography pharmacological study in which participants received either placebo, 0.5 or 1.5 mg of lorazepam (LZP; GABAergic enhancer) in different experimental sessions. By recording oscillatory brain activity with during rest and working memory (WM), we were able to demonstrate that posterior alpha (8–12 Hz) phase was coupled to beta-low gamma band (20–45 Hz) amplitude envelope during all sessions. Importantly, bicoherence values around the harmonics of the alpha frequency were similar both in magnitude and topographic distribution to the cross-frequency coherence (CFCoh) values observed in the alpha-phase to beta-low gamma coupling. In addition, despite the large CFCoh we found no significant cross-frequency directionality (CFD). Critically, simulations demonstrated that a sizable part of our empirical CFCoh between alpha and beta-low gamma coupling and the lack of CFD could be explained by two-three harmonics aligned in zero phase-lag produced by the physiologically characteristic alpha asymmetry in the amplitude of the peaks relative to the troughs. Furthermore, we showed that periodic signals whose waveform deviate from pure sine waves produce non-zero CFCoh with predictable CFD. Our results reveal the important role of the non-sinusoidal wave morphology on state of the art CFC metrics and we recommend caution with strong physiological interpretations of CFC and suggest basic data quality checks to enhance the mechanistic understanding of CFC.

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“…This approach allowed us to exclude multiple evoked transients that were present in the signal (e.g. cue onset, variable target onset, response), which are known to give rise to spurious CFC (Aru et al, 2015; Cole and Voytek, 2017; Gerber et al, 2016), when additional filtering is applied. Similar to spike-triggered averaging (Brown et al, 2004), we first detected all the HFB peaks in a given trial and at a given channel after the evoked response (> 0.3s) and prior to the target onset, which varied on a trial-by-trial basis.…”

Section: Star Methodsmentioning

confidence: 99%

Neural Mechanisms of Sustained Attention Are Rhythmic

Helfrich

Fiebelkorn

Szczepanski

et al. 2018

Neuron

Self Cite

386

408

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Classic models of attention suggest that sustained neural firing constitutes a neural correlate of sustained attention. However, recent evidence indicates that behavioral performance fluctuates over time, exhibiting temporal dynamics that closely resemble the spectral features of ongoing, oscillatory brain activity. Therefore, it has been proposed that periodic neuronal excitability fluctuations might shape attentional allocation and overt behavior. However, empirical evidence to support this notion is sparse. Here, we address this issue by examining data from large-scale subdural recordings, using two different attention tasks that track perceptual ability at high temporal resolution. Our results reveal that perceptual outcome varies as a function of the theta phase even in states of sustained spatial attention. These effects were robust at the single-subject level, suggesting that rhythmic perceptual sampling is an inherent property of the frontoparietal attention network. Collectively, these findings support the notion that the functional architecture of top-down attention is intrinsically rhythmic.

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Periodic Non-Sinusoidal Activity Can Produce Cross-Frequency Coupling in Cortical Signals in the Absence of Functional Interaction Between Neural Sources

Cited by 4 publications

References 28 publications

Dual origins of measured phase-amplitude coupling reveal distinct neural mechanisms underlying episodic memory in the human cortex

Dual origins of measured phase-amplitude coupling reveal distinct neural mechanisms underlying episodic memory in the human cortex

Neuronal Oscillations with Non-sinusoidal Morphology Produce Spurious Phase-to-Amplitude Coupling and Directionality

Neural Mechanisms of Sustained Attention Are Rhythmic

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