Pulsed Out of Awareness: EEG Alpha Oscillations Represent a Pulsed-Inhibition of Ongoing Cortical Processing

Mathewson, Kyle E.; Lleras, Alejandro; Beck, Diane M.; Fabiani, Monica; Ro, Tony; Gratton, Gabriele

doi:10.3389/fpsyg.2011.00099

Cited by 420 publications

(440 citation statements)

References 231 publications

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“…In particular, spiking was more likely to occur at the trough than at the peak of the α-cycle. These findings are consistent with the pulsed-inhibition hypothesis (5,28,29), which states that the α-oscillations are a consequence of bouts of inhibition that prevent firing and thus reduce neuronal processing.…”

Section: Discussionsupporting

confidence: 80%

“…However, given the strong oscillatory nature of the α-activity, it is less clear how it influences processing in a phasic manner. It has been suggested that α-oscillations serve to depress processing every ∼100 ms by a mechanism of pulsed inhibition (5,(28)(29)(30). In support of this notion, it has recently been demonstrated that perception is modulated by the prestimulus phase of the α-rhythm (31, 32).…”

mentioning

confidence: 55%

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α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking

Haegens

Nácher

Luna

et al. 2011

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

662

627

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Extensive work in humans using magneto-and electroencephalography strongly suggests that decreased oscillatory α-activity (8-14 Hz) facilitates processing in a given region, whereas increased α-activity serves to actively suppress irrelevant or interfering processing. However, little work has been done to understand how α-activity is linked to neuronal firing. Here, we simultaneously recorded local field potentials and spikes from somatosensory, premotor, and motor regions while a trained monkey performed a vibrotactile discrimination task. In the local field potentials we observed strong activity in the α-band, which decreased in the sensorimotor regions during the discrimination task. This α-power decrease predicted better discrimination performance. Furthermore, the α-oscillations demonstrated a rhythmic relation with the spiking, such that firing was highest at the trough of the α-cycle. Firing rates increased with a decrease in α-power. These findings suggest that α-oscillations exercise a strong inhibitory influence on both spike timing and firing rate. Thus, the pulsed inhibition by α-oscillations plays an important functional role in the extended sensorimotor system.T he prominent posterior α-rhythm (8-14 Hz) was first described by Hans Berger (1) and long considered to reflect cortical idling (2, 3). To a large extent, the α-rhythm has been ignored by animal neurophysiologists (but see ref. 4) and considered to be of little functional relevance. Thus, it remains largely unknown how ongoing α-oscillations relate to neuronal firing.In contrast to the idling hypothesis, converging electrophysiological evidence in humans suggests that α-oscillations play an important functional role in cognitive processing (5-7). In particular, α-activity might serve to shape the state of sensory brain regions to direct the flow of information and optimize performance (8). In support of this idea, several studies on visual perception have shown that anticipatory α-activity reflects the orienting of attention (9-14) and influences detection performance (15-17). Recently, it was shown that the functionality of α-oscillations can be generalized to the somatosensory system (18-21). Furthermore, α-activity has been implicated in visual (22-25), auditory (26), and somatosensory working-memory performance (27).These studies strongly suggest that decreased α-activity facilitates processing in task-relevant brain regions, whereas increased α-activity functions to suppress distracting input in task-irrelevant regions. However, given the strong oscillatory nature of the α-activity, it is less clear how it influences processing in a phasic manner. It has been suggested that α-oscillations serve to depress processing every ∼100 ms by a mechanism of pulsed inhibition (5,(28)(29)(30). In support of this notion, it has recently been demonstrated that perception is modulated by the prestimulus phase of the α-rhythm (31, 32). Likewise, it was recently shown that the magnitude of the blood-oxygen level-dependent signal in response to a visual...

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Section: Discussionsupporting

confidence: 80%

mentioning

confidence: 55%

α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking

Haegens

Nácher

Luna

et al. 2011

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

662

627

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“…One intriguing proposal is that cortical oscillations instantiate perceptual predictions by coordinating prestimulus neural activity to process the predicted stimulus optimally (1,2). A candidate neural mechanism for such coordination is low-frequency oscillations in the alpha band (8)(9)(10)(11)(12)(13)(14) Hz) of human electroencephalography (EEG) recordings, which are suggested to route information phasically through task-relevant networks (3,4). As evidence, recent work has demonstrated that the prestimulus alpha-band phase predicts visual detection (5,6), the perception of phosphenes (7), the magnitude of the functional MRI (fMRI) response in visual cortex (8), successful perceptual integration across the visual field and subsequent connectivity between visual and parietal cortex (9), as well as variability in working memory performance (10).…”

mentioning

confidence: 99%

Top-down control of the phase of alpha-band oscillations as a mechanism for temporal prediction

Samaha

Bauer

Cimaroli

et al. 2015

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

221

179

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The physiological state of the brain before an incoming stimulus has substantial consequences for subsequent behavior and neural processing. For example, the phase of ongoing posterior alpha-band oscillations (8–14 Hz) immediately before visual stimulation has been shown to predict perceptual outcomes and downstream neural activity. Although this phenomenon suggests that these oscillations may phasically route information through functional networks, many accounts treat these periodic effects as a consequence of ongoing activity that is independent of behavioral strategy. Here, we investigated whether alpha-band phase can be guided by top-down control in a temporal cueing task. When participants were provided with cues predictive of the moment of visual target onset, discrimination accuracy improved and targets were more frequently reported as consciously seen, relative to unpredictive cues. This effect was accompanied by a significant shift in the phase of alpha-band oscillations, before target onset, toward each participant’s optimal phase for stimulus discrimination. These findings provide direct evidence that forming predictions about when a stimulus will appear can bias the phase of ongoing alpha-band oscillations toward an optimal phase for visual processing, and may thus serve as a mechanism for the top-down control of visual processing guided by temporal predictions.

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“…Trial-to-trial fluctuations in power might account for variations in the detectability of stimuli: A weak stimulus might be sufficient to produce a response from a region in a low-alpha, high-excitability state, but insufficient when that region is in a high-alpha, low-excitability state. Alpha oscillations may thus reflect pulses of cortical inhibition (Mathewson et al, 2011), as a sensory region adjusts to temporal expectations of the delivery of a stimulus by ensuring it is in high-excitability state when a stimulus is expected. Top-down manipulation of alpha power may also be a mechanism for the suppression of irrelevant stimuli (Haegens, Händel, & Jensen, 2011), through the inhibition of cortical regions dealing with, for example, unattended regions of space.…”

Section: Introductionmentioning

confidence: 99%

Pre-stimulus alpha oscillations over somatosensory cortex predict tactile misperceptions

et al. 2017

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Cite this article as: Matt Craddock, Ellen Poliakoff, Wael El-deredy, Ekaterini Klepousniotou and Donna M. Lloyd, Pre-stimulus alpha oscillations over somatosensory cortex predict tactile misperceptions, Neuropsychologia, http://dx.doi.org/10. 1016/j.neuropsychologia.2016.12.030 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. AbstractFluctuations of pre-stimulus oscillatory activity in the somatosensory alpha band (8-14 Hz) observed using human EEG and MEG have been shown to influence the detection of supraand peri-threshold somatosensory stimuli. However, some reports of touch occur even without a stimulus. We investigated the possibility that pre-stimulus alpha oscillations might also influence these false reports of touch -known as tactile misperceptions. We recorded EEG while participants performed the Somatic Signal Detection Task (SSDT), in which participants must detect brief, peri-threshold somatosensory targets. We found that prestimulus oscillatory power in the somatosensory alpha range exhibited a negative linear 2 relationship with reporting of touch at electrode clusters over both contralateral and ipsilateral somatosensory regions. As pre-stimulus alpha power increased, the probability of reporting a touch declined; as it decreased, the probability of reporting a touch increased. This relationship was stronger on trials without a somatosensory stimulus than on trials with a somatosensory stimulus, although was present for both trial types. Spatio-temporal clusterbased permutation analysis also found that pre-stimulus alpha was lower on trials when touch was reported -irrespective of whether it was present -over contralateral and ipsilateral somatosensory cortices, as well as left frontocentral areas. We argue that alpha power may reflect changes in response criterion rather than sensitivity alone. Low alpha power relates to a low barrier to reporting a touch even when one is not present, while high alpha power is linked to less frequent reporting of touch overall.

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Pulsed Out of Awareness: EEG Alpha Oscillations Represent a Pulsed-Inhibition of Ongoing Cortical Processing

Cited by 420 publications

References 231 publications

α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking

α-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking

Top-down control of the phase of alpha-band oscillations as a mechanism for temporal prediction

Pre-stimulus alpha oscillations over somatosensory cortex predict tactile misperceptions

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