Alpha oscillations link action to cognition: An oculomotor account of the brain’s dominant rhythm

Popov, Tzvetan; Miller, Gregory A.; Rockstroh, Brigitte; Jensen, Ole; Langer, Nicolas

doi:10.1101/2021.09.24.461634

Cited by 24 publications

(19 citation statements)

References 116 publications

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“…A possible confound in identifying relationships between pupil and cortical dynamics are eye movements: Saccades change pupil size ( Mathôt, 2018 ; Mathôt et al, 2015 ) and oculomotor behavior is functionally linked to cortical alpha oscillations ( Popov et al, 2021 ). Here, we controlled for saccade effects by regressing out canonical responses from pupil time series (as detailed in the Materials and methods section; see, e.g., Urai et al, 2017 ).…”

Section: Resultsmentioning

confidence: 99%

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Pfeffer

Keitel

Kluger

et al. 2022

eLife

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Fluctuations in arousal, controlled by subcortical neuromodulatory systems, continuously shape cortical state, with profound consequences for information processing. Yet, how arousal signals influence cortical population activity in detail has so far only been characterized for a few selected brain regions. Traditional accounts conceptualize arousal as a homogeneous modulator of neural population activity across the cerebral cortex. Recent insights, however, point to a higher specificity of arousal effects on different components of neural activity and across cortical regions. Here, we provide a comprehensive account of the relationships between fluctuations in arousal and neuronal population activity across the human brain. Exploiting the established link between pupil size and central arousal systems, we performed concurrent magnetoencephalographic (MEG) and pupillographic recordings in a large number of participants, pooled across three laboratories. We found a cascade of effects relative to the peak timing of spontaneous pupil dilations: Decreases in low-frequency (2-8 Hz) activity in temporal and lateral frontal cortex, followed by increased high-frequency (>64 Hz) activity in mid-frontal regions, followed by monotonic and inverted-U relationships with intermediate frequency-range activity (8-32 Hz) in occipito-parietal regions. Pupil-linked arousal also coincided with widespread changes in the structure of the aperiodic component of cortical population activity, indicative of changes in the excitation-inhibition balance in underlying microcircuits. Our results provide a novel basis for studying the arousal modulation of cognitive computations in cortical circuits.

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Section: Resultsmentioning

confidence: 99%

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Pfeffer

Keitel

Kluger

et al. 2022

eLife

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show abstract

“…At the same time, we show that alpha modulation is not a direct consequence attentiondirected microsaccades. Nevertheless, the fact that alpha modulation functionally co-varies with the timing and direction of microsaccades suggest oculomotor activity may be an important factor to consider in studies linking alpha activity to various cognitive functions (see also Popov et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Functional but not obligatory link between microsaccades and neural modulation by covert spatial attention

Liu

Nobre

Ede

2021

Preprint

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Covert spatial attention is associated with spatially specific modulation of neural activity as well as with directional biases in fixational eye-movements known as microsaccades. Recently, this link has been suggested to be obligatory, such that modulation of neural activity by covert spatial attention occurs only when paired with microsaccades toward the attended location. Here we revisited this link between microsaccades and neural modulation by covert spatial attention in humans. We investigated spatial modulation of 8-12 Hz EEG alpha activity and microsaccades in a context with no incentive for overt gaze behaviour: when attention is directed internally within the spatial layout of visual working memory. In line with a common attentional origin, we show that spatial modulations of alpha activity and microsaccades co-vary: alpha lateralisation is stronger in trials with microsaccades toward compared to away from the memorised location of the to-be-attended item and occurs earlier in trials with earlier microsaccades toward this item. Critically, however, trials without attention-driven microsaccades nevertheless showed clear spatial modulation of alpha activity – comparable to the neural modulation observed in trials with attention-driven microsaccades. Thus, directional biases in microsaccades are correlated with neural signatures of covert spatial attention, but they are not a prerequisite for neural modulation by covert spatial attention to be manifest.

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“…Complementing such cognitive interpretations, a recent account of alpha/beta activity argues for a view closer to the biological implementation of the association between alpha/beta power modulations and oculomotor action 33 . Building on recent evidence demonstrating this close relationship in a variety of tasks [34][35][36] , the account postulates a fundamental and domain-general functional organization linking visual cortical signals to oculomotor action.…”

Section: Introductionmentioning

confidence: 99%

Cortico-ocular coupling in the service of episodic memory formation

Popov

Staudigl

2022

Preprint

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Encoding of visual information is a necessary requirement for most types of episodic memories. In search for a neural signature of memory formation, amplitude modulation of neural activity has been repeatedly shown to correlate with and suggested to be functionally involved in successful memory encoding. We here report a complementary view on why and how brain activity relates to memory, indicating a functional role of cortico-ocular interactions for episodic memory formation. Recording simultaneous magnetoencephalography and eye tracking in 35 human participants, we demonstrate that gaze variability and amplitude modulations of alpha/beta oscillations (10-20 Hz) in visual cortex covary and predict subsequent memory performance between and within participants. Amplitude variation during pre-stimulus baseline was associated with gaze direction variability, echoing the co-variation observed during scene encoding. We conclude that encoding of visual information engages unison coupling between oculomotor and visual areas in the service of memory formation.

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Alpha oscillations link action to cognition: An oculomotor account of the brain’s dominant rhythm

Cited by 24 publications

References 116 publications

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Coupling of pupil- and neuronal population dynamics reveals diverse influences of arousal on cortical processing

Functional but not obligatory link between microsaccades and neural modulation by covert spatial attention

Cortico-ocular coupling in the service of episodic memory formation

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