The relevance of alpha phase in human perception

Ruzzoli, Manuela; Torralba, Mireia; Fernández, Luis Morís; Soto‐Faraco, Salvador

doi:10.1016/j.cortex.2019.05.012

Cited by 76 publications

(115 citation statements)

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“…Although with mixed evidence, several studies have demonstrated a link between the phase of ongoing neural oscillations and behavioral outcomes, especially in perception and attention tasks (Busch et al 2009;Mathewson et al 2009;VanRullen et al 2011). Conversely, a handful of studies have reported null results regarding this link (Ruzzoli et al 2019;Bompas et al 2015;Busch and VanRullen 2010;Benwell et al 2017). The interpretation of these phase-behavior correlation results capitalizes on the idea that brain oscillations reflect fluctuations in neural excitability and the coordinated action of neural populations across different brain regions.…”

Section: Discussionmentioning

confidence: 99%

“…In particular, some studies have related stimulus detection with the phase of the ongoing oscillations at or before stimulus onset. These studies have revealed cyclic alternations in behavioral performance mainly in the theta and alpha bands (~4-8 and 8-12 Hz, respectively) (Busch et al 2009;de Graaf et al 2013;Klimesch et al 2007;Mathewson et al 2009;Palva and Palva 2007;; but see also Ruzzoli et al 2019 for conflicting evidence). The main idea behind this phenomenon is that oscillatory neuronal activity reflects rhythmic fluctuations in the neuron's membrane potential, which are associated with changes in neuronal excitability (Buzsaki and Draguhn 2004;Lakatos et al 2005;Fries et al 2007).…”

Section: Introductionmentioning

confidence: 99%

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The phase of Theta oscillations modulates successful memory formation at encoding

Cruzat

Torralba

Ruzzoli

et al. 2020

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Several past studies have shown that attention and perception can depend upon the phase of ongoing neural oscillations at stimulus onset. Here, we extend this idea to the memory domain. We tested the hypothesis that ongoing fluctuations in neural activity have an impact on memory encoding using a picture paired-associates task to gauge episodic memory performance. Experiment 1 capitalized on the principle of phase reset. We tested if subsequent memory performance fluctuates rhythmically, time-locked to a reset cue presented before the to-be-remembered pairs. We found indication that behavioral performance was periodically and selectively modulated at theta frequency (~4 Hz). In Experiment 2 we focused on prestimulus ongoing activity using scalp EEG recorded while participants performed the pair-associate task. We analyzed subsequent memory performance as a function of theta and alpha activity around the presentation of the to-be-remembered pairs. The results of the pre-registered analyses, using large electrode clusters and generic spectral ranges, returned null results of prestimulus phase-behavior correlation. However, we found that post-stimulus theta-power modulations in left frontal scalp predicted subsequent memory performance. This post-stimulus effect in theta power was used to guide a post-hoc prestimulus phase analysis, narrowed down to more precise scalp location and frequency. This analysis returned a correlation between prestimulus theta phase and subsequent memory. Altogether, these results suggest that the prestimulus theta activity at encoding has an impact on later memory performance.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The phase of Theta oscillations modulates successful memory formation at encoding

Cruzat

Torralba

Ruzzoli

et al. 2020

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“…Specifically, both the power (Worden et al, 2000;Ergenoglu et al, 2004;Babiloni et al, 2006;Kelly et al, 2006;Thut et al, 2006;Klimesch et al, 2007;Palva & Palva, 2007;Foxe & Snyder, 2011) and the phase of the occipito-parietal α (Klimesch et al, 2007;Palva & Palva, 2007;Mathewson et al, 2009;Klimesch, 2012;Jensen et al, 2014;VanRullen, 2016b) have been linked to performance in visual perception (van Dijk et al, 2008;Jensen & Mazaheri, 2010;Jensen et al, 2011; VanRullen, 2016a). However, while the evidence for the role of α-power in perceptual judgments seems well-established (Walsh, 1952;Lansing et al, 1959;Jensen et al, 2011;Bompas et al, 2015; but see Benwell et al, 2017), the role of the α-phase is still not clearly settled (Walsh, 1952;O'Hare, 1954;Benwell et al, 2017;Ruzzoli et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Can the occipital alpha-phase speed up visual detection through a real-time EEG-based brain-computer interface (BCI)?

Vigué‐Guix¹,

Fernández

Torralba³

et al. 2020

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ABSTRACTElectrical brain oscillations reflect fluctuations in neural excitability. Fluctuations in the alpha band (α, 8-12 Hz) in the occipito-parietal cortex are thought to regulate sensory responses, leading to cyclic variations in visual perception. Inspired by this theory, some past and recent studies have addressed the relationship between α-phase from extra-cranial EEG and behavioural responses to visual stimuli in humans. The latest studies have used offline approaches to confirm α-gated cyclic patterns. However, a particularly relevant implication is the possibility to use this principle online for real-time neurotechnology, whereby stimuli are time-locked to specific α-phases leading to predictable outcomes in performance. Here we aimed at providing a proof-of-concept for such real-time neurotechnology. Participants performed a speeded response task to visual targets that were presented upon a real-time estimation of the α-phase via an EEG closed-loop brain-computer interface (BCI). We predicted, according to the theory, a modulation of reaction times (RTs) along the α-cycle. Our BCI system achieved reliable trial-to-trial phase-locking of stimuli to the phase of individual occipito-parietal α-oscillations. Yet, the behavioural results did not support a consistent relation between RTs and the phase of the α-cycle neither at group nor single participant levels. We must conclude that although the α-phase might play a role in perceptual decisions from a theoretical perspective, its impact on EEG-based BCI application appears negligible.

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“…Several experiments in humans have highlighted a relationship between pre-stimulus alpha phase and different aspects of visual performance in near-threshold detection or discrimination tasks [11][12][13][14]28,35,36 , but see 37,38 . Given the evidence here for a feedforward impact of alpha phase on early visual responses, a reasonable hypothesis is that thalamic gating may underlie the effect of alpha phase on behavior, yet no study has directly linked early sensory responses, alpha phase, and psychophysical performance.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, the precise effect of alpha phase on behavior is itself still not clear, as one report has found effects of alpha phase on response criterion, rather than detection sensitivity 35 , another paper found effects on discrimination accuracy 13 (putatively reflecting sensitivity changes), and most other studies have only analyzed hit rates 10,11,[14][15][16]28 , which are ambiguous between a change in sensitivity or criterion. Moreover, several studies have reported no phase effects on stimulus detection/discrimination [37][38][39] , though a recent experiment, optimized in many ways to detect an effect, found a rather large change in detection rates of ~20% between stimuli presented during the peak versus trough of occipital alpha 10 . Model-based approaches 40 , as have recently been applied to the study of oscillatory amplitude dynamics 41 , may serve well to better understand the link between oscillatory phase, sensory responses, and perceptual behavior.…”

Section: Discussionmentioning

confidence: 99%

Pre-Stimulus Alpha-Band Phase Gates Afferent Visual Cortex Responses

Dou

Morrow

Iemi

et al. 2021

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The neurogenesis of alpha-band (8-13 Hz) activity has been characterized across many different animal experiments. However, the functional role that alpha oscillations play in perception and behavior has largely been attributed to two contrasting hypotheses, with human evidence in favor of either (or both or neither) remaining sparse. On the one hand, alpha generators have been observed in relay sectors of the visual thalamus and are postulated to phasically inhibit afferent visual input in a feedforward manner 1-4. On the other hand, evidence also suggests that the direction of influence of alpha activity propagates backwards along the visual hierarchy, reflecting a feedback influence upon the visual cortex 5-9. The primary source of human evidence regarding the role of alpha phase in visual processing has been on perceptual reports 10-16, which could be modulated either by feedforward or feedback alpha activity. Thus, although these two hypotheses are not mutually exclusive, human evidence clearly supporting either one is lacking. Here, we present human subjects with large, high-contrast visual stimuli that elicit robust C1 event-related potentials (ERP), which peak between 70-80 milliseconds post-stimulus and are thought to reflect afferent primary visual cortex (V1) input 17-20. We find that the phase of ongoing alpha oscillations modulates the global field power (GFP) of the EEG during this first volley of stimulus processing (the C1 time-window). On the standard assumption 21-23 that this early activity reflects postsynaptic potentials being relayed to visual cortex from the thalamus, our results suggest that alpha phase gates visual responses during the first feed-forward sweep of processing.

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The relevance of alpha phase in human perception

Cited by 76 publications

References 68 publications

The phase of Theta oscillations modulates successful memory formation at encoding

The phase of Theta oscillations modulates successful memory formation at encoding

Can the occipital alpha-phase speed up visual detection through a real-time EEG-based brain-computer interface (BCI)?

Pre-Stimulus Alpha-Band Phase Gates Afferent Visual Cortex Responses

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