Stimulus-driven brain rhythms within the alpha band: The attentional-modulation conundrum

Two largely independent research lines use rhythmic sensory stimulation to study visual processing. Despite the use of strikingly similar experimental paradigms, they differ crucially in their notion of the stimulus-driven periodic brain responses: One regards them mostly as synchronised (entrained) intrinsic brain rhythms; the other assumes they are predominantly evoked responses (classically termed steady-state responses, or SSRs) that add to the ongoing brain activity. This conceptual difference can produce contradictory predictions about, and interpretations of, experimental outcomes. The effect of spatial attention on brain rhythms in the alpha-band (8-13 Hz) is one such instance: alpha-range SSRs have typically been found to increase in power when participants focus their spatial attention on laterally presented stimuli, in line with a gain control of the visual evoked response. In nearly identical experiments, retinotopic decreases in entrained alpha-band power have been reported, in line with the inhibitory function of intrinsic alpha. Here we reconcile these contradictory findings by showing that they result from a small but far-reaching difference between two common approaches to EEG spectral decomposition. In a new analysis of previously published EEG data, recorded during bilateral rhythmic visual stimulation, we find the typical SSR gain effect when emphasising stimulus-locked neural activity and the typical retinotopic alpha suppression when focusing on ongoing rhythms. These opposite but parallel effects suggest that spatial attention may bias the neural processing of dynamic visual stimulation via two complementary neural mechanisms.

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Alpha oscillations do not implement gain control in early visual cortex but rather gating in parieto-occipital regions

10.1101/2020.04.03.021485 ◽

2020 ◽

Author(s):

Alexander Zhigalov ◽

Ole Jensen

Keyword(s):

Visual Cortex ◽

Spatial Attention ◽

Neuronal Excitability ◽

Brain Activity ◽

Gain Control ◽

Alpha Power ◽

Alpha Band ◽

Alpha Oscillations ◽

Early Visual Cortex ◽

Broadband Frequency

AbstractSpatial attention provides a mechanism for respectively enhancing relevant and suppressing irrelevant information. While it is well-established that attention modulates oscillations in the alpha band, it remains unclear if alpha oscillations are involved in directly modulating the neuronal excitability associated with the allocation of spatial attention. In this study in humans, we utilized a novel broadband frequency (60 – 70 Hz) tagging paradigm to quantify neuronal excitability in relation to alpha oscillations in a spatial attention paradigm. We used magnetoencephalography to characterize ongoing brain activity as it allows for localizing the sources of both the alpha and frequency tagging responses. We found that attentional modulation of alpha power and the frequency tagging response are uncorrelated over trials. Importantly, the neuronal sources of the tagging response were localized in early visual cortex (V1) whereas the sources of the alpha activity were identified around parieto-occipital sulcus. Moreover, we found that attention did not modulate the latency of the frequency tagged responses. Our findings point to alpha band oscillations serving a downstream gating role rather than implementing gain control of excitability in early visual regions.Significance StatementBy combining magnetoencephalography and a novel broadband frequency tagging approach, we show that spatial attention differently modulates alpha oscillations and neuronal excitability. Importantly, the sources of the alpha oscillations and tagging responses were spatially distinct and the alpha power and tagging response were not related over trials. These results are inconsistent with previous ideas suggesting that alpha oscillations are involved in gain control of early sensory regions; rather alpha oscillations are involved in the allocation of neuronal resources in downstream regions.

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The Temporal Dynamics of Object Processing in Visual Cortex during the Transition from Distributed to Focused Spatial Attention

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00045 ◽

2011 ◽

Vol 23 (12) ◽

pp. 4094-4105 ◽

Cited By ~ 2

Author(s):

Chien-Te Wu ◽

Melissa E. Libertus ◽

Karen L. Meyerhoff ◽

Marty G. Woldorff

Keyword(s):

Visual Cortex ◽

Spatial Attention ◽

Cognitive Neuroscience ◽

Visual Processing ◽

Object Representation ◽

Temporal Dynamics ◽

Brain Activity ◽

Object Processing ◽

Electrical Brain Activity

Several major cognitive neuroscience models have posited that focal spatial attention is required to integrate different features of an object to form a coherent perception of it within a complex visual scene. Although many behavioral studies have supported this view, some have suggested that complex perceptual discrimination can be performed even with substantially reduced focal spatial attention, calling into question the complexity of object representation that can be achieved without focused spatial attention. In the present study, we took a cognitive neuroscience approach to this problem by recording cognition-related brain activity both to help resolve the questions about the role of focal spatial attention in object categorization processes and to investigate the underlying neural mechanisms, focusing particularly on the temporal cascade of these attentional and perceptual processes in visual cortex. More specifically, we recorded electrical brain activity in humans engaged in a specially designed cued visual search paradigm to probe the object-related visual processing before and during the transition from distributed to focal spatial attention. The onset times of the color popout cueing information, indicating where within an object array the subject was to shift attention, was parametrically varied relative to the presentation of the array (i.e., either occurring simultaneously or being delayed by 50 or 100 msec). The electrophysiological results demonstrate that some levels of object-specific representation can be formed in parallel for multiple items across the visual field under spatially distributed attention, before focal spatial attention is allocated to any of them. The object discrimination process appears to be subsequently amplified as soon as focal spatial attention is directed to a specific location and object. This set of novel neurophysiological findings thus provides important new insights on fundamental issues that have been long-debated in cognitive neuroscience concerning both object-related processing and the role of attention.

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Individual alpha peak frequency predicts 10 Hz flicker effects on selective attention

10.1101/185132 ◽

2017 ◽

Cited By ~ 1

Author(s):

Rasa Gulbinaite ◽

Tara van Viegen ◽

Martijn Wieling ◽

Michael X Cohen ◽

Rufin VanRullen

Keyword(s):

Selective Attention ◽

Task Performance ◽

Visual Stimulation ◽

Peak Frequency ◽

Alpha Band ◽

Attention Task ◽

Stimulus Processing ◽

Brain Rhythms ◽

Attention Demands ◽

Alpha Peak

ABSTRACTRhythmic visual stimulation (“flicker”) is primarily used to “tag” processing of low-level visual and high-level cognitive phenomena. However, preliminary evidence suggests that flicker may also entrain endogenous brain oscillations, thereby modulating cognitive processes supported by those brain rhythms. Here we tested the interaction between 10 Hz flicker and endogenous alpha-band (~10 Hz) oscillations during a selective visuospatial attention task. We recorded EEG from human participants (both genders) while they performed a modified Eriksen flanker task in which distractors and targets flickered within (10 Hz) or outside (7.5 or 15 Hz) the alpha band. By using a combination of EEG source separation, time-frequency, and single-trial linear mixed effects modeling, we demonstrate that 10 Hz flicker interfered with stimulus processing more on incongruent than congruent trials (high vs. low selective attention demands). Crucially, the effect of 10 Hz flicker on task performance was predicted by the distance between 10 Hz and individual alpha peak frequency (estimated during the task). Finally, the flicker effect on task performance was more strongly predicted by EEG flicker responses during stimulus processing than during preparation for the upcoming stimulus, suggesting that 10 Hz flicker interfered more with reactive than proactive selective attention. These findings are consistent with our hypothesis that visual flicker entrained endogenous alpha-band networks, which in turn impaired task performance. Our findings also provide novel evidence for frequency-dependent exogenous modulation of cognition that is determined by the correspondence between the exogenous flicker frequency and the endogenous brain rhythms.SignificanceHere we provide novel evidence that the interaction between exogenous rhythmic visual stimulation and endogenous brain rhythms can have frequency-specific behavioral effects. We show that alpha-band (10 Hz) flicker impairs stimulus processing in a selective attention task when the stimulus flicker rate matches individual alpha peak frequency. The effect of sensory flicker on task performance was stronger when selective attention demands were high, and was stronger during stimulus processing and response selection compared to the pre-stimulus anticipatory period. These findings provide novel evidence that frequency-specific sensory flicker affects online attentional processing, and also demonstrate that the correspondence between exogenous and endogenous rhythms is an overlooked prerequisite when testing for frequency-specific cognitive effects of flicker.

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Audio-visual synchrony and spatial attention enhance processing of dynamic visual stimulation independently and in parallel: a frequency-tagging study

10.1101/128918 ◽

2017 ◽

Author(s):

Amra Covic ◽

Christian Keitel ◽

Emanuele Porcu ◽

Erich Schröger ◽

Matthias M Müller

Keyword(s):

Spatial Attention ◽

Visual Stimulus ◽

Visual Processing ◽

Visual Stimulation ◽

Visual Fields ◽

Tone Presentation ◽

Neural Processing ◽

Brain Responses ◽

Neural Processes ◽

Steady State Responses

ABSTRACTThe neural processing of a visual stimulus can be facilitated by attending to its position or by a co-occurring auditory tone. Using frequency-tagging we investigated whether facilitation by spatial attention and audio-visual synchrony rely on similar neural processes. Participants attended to one of two flickering Gabor patches (14.17 and 17 Hz) located in opposite lower visual fields. Gabor patches further “pulsed” (i.e. showed smooth spatial frequency variations) at distinct rates (3.14 and 3.63 Hz). Frequency-modulating an auditory stimulus at the pulse-rate of one of the visual stimuli established audio-visual synchrony. Flicker and pulsed stimulation elicited stimulus-locked rhythmic electrophysiological brain responses that allowed tracking the neural processing of simultaneously presented stimuli. These steady-state responses (SSRs) were quantified in the spectral domain to examine visual stimulus processing under conditions of synchronous vs. asynchronous tone presentation and when respective stimulus positions were attended vs. unattended. Strikingly, unique patterns of effects on pulse- and flicker driven SSRs indicated that spatial attention and audiovisual synchrony facilitated early visual processing in parallel and via different cortical processes. We found attention effects to resemble the classical top-down gain effect facilitating both, flicker and pulse-driven SSRs. Audio-visual synchrony, in turn, only amplified synchrony-producing stimulus aspects (i.e. pulse-driven SSRs) possibly highlighting the role of temporally co-occurring sights and sounds in bottom-up multisensory integration.

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Spatial Attentional Selection Modulates Early Visual Stimulus Processing Independently of Visual Alpha Modulations

Cerebral Cortex ◽

10.1093/cercor/bhz335 ◽

2020 ◽

Vol 30 (6) ◽

pp. 3686-3703 ◽

Cited By ~ 9

Author(s):

C Gundlach ◽

S Moratti ◽

N Forschack ◽

M M Müller

Keyword(s):

Visual Cortex ◽

Spatial Attention ◽

Sensory Processing ◽

Sensory Information ◽

Gain Control ◽

Relevant Information ◽

Task Demands ◽

Alpha Band ◽

Stimulus Processing ◽

Early Visual Cortex

Abstract The capacity-limited human brain is constantly confronted with a huge amount of sensory information. Selective attention is needed for biasing neural processing towards relevant information and consequently allows meaningful interaction with the environment. Activity in the alpha-band has been proposed to be related to top-down modulation of neural inhibition and could thus represent a viable candidate to control the priority of stimulus processing. It is, however, unknown whether modulations in the alpha-band directly relate to changes in the sensory gain control of the early visual cortex. Here, we used a spatial cueing paradigm while simultaneously measuring ongoing alpha-band oscillations and steady-state visual evoked potentials (SSVEPs) as a marker of continuous early sensory processing in the human visual cortex. Thereby, the effects of spatial attention for both of these signals and their potential interactions were assessed. As expected, spatial attention modulated both alpha-band and SSVEP responses. However, their modulations were independent of each other and the corresponding activity profiles differed across task demands. Thus, our results challenge the view that modulations of alpha-band activity represent a mechanism that directly alters or controls sensory gain. The potential role of alpha-band oscillations beyond sensory processing will be discussed in light of the present results.

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Graded Effects of Spatial and Featural Attention on Human Area MT and Associated Motion Processing Areas

Journal of Neurophysiology ◽

10.1152/jn.1997.78.1.516 ◽

1997 ◽

Vol 78 (1) ◽

pp. 516-520 ◽

Cited By ~ 161

Author(s):

Michael S. Beauchamp ◽

Robert W. Cox ◽

Edgar A. Deyoe

Keyword(s):

Spatial Attention ◽

Visual Processing ◽

Human Subjects ◽

Brain Activity ◽

Motion Processing ◽

Related Factors ◽

Area Mt ◽

Subtle Change ◽

Normal Human ◽

High Degree

Beauchamp, Michael S., Robert W. Cox, and Edgar A. DeYoe. Graded effects of spatial and featural attention on human area MT and associated motion processing areas. J. Neurophysiol. 78: 516–520, 1997. Functional magnetic resonance imaging was used to quantify the effects of changes in spatial and featural attention on brain activity in the middle temporal visual area and associated motion processing regions (hMT+) of normal human subjects. When subjects performed a discrimination task that directed their spatial attention to a peripherally presented annulus and their featural attention to the speed of points in the annulus, activity in hMT+ was maximal. If subjects were instead asked to discriminate the color of points in the annulus, the magnitude and volume of activation in hMT+ fell to 64 and 35%, respectively, of the previously observed maximum response. In another experiment, subjects were asked to direct their spatial attention away from the annulus toward the fixation point to detect a subtle change in luminance. The response magnitude and volume dropped to 40 and 9% of maximum. These experiments demonstrate that both spatial and featural attention modulate hMT+ and that their effects can work in concert to modulate cortical activity. The high degree of modulation by attention suggests that an understanding of the stimulus-driven properties of visual cortex needs to be complemented with an investigation of the effects of task-related factors on visual processing.

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Altered low frequency brain rhythms precede changes in gamma power during tauopathy

10.1101/2021.08.03.454865 ◽

2021 ◽

Author(s):

Fabio R Rodrigues ◽

Amalia Papanikolaou ◽

Joanna Holeniewska ◽

Keith G Phillips ◽

Aman B Saleem ◽

...

Keyword(s):

Visual Stimulation ◽

Brain Activity ◽

Field Potential ◽

Low Frequency ◽

Wide Band ◽

Low Frequencies ◽

Brain Rhythms ◽

Gamma Range ◽

Gamma Rhythm ◽

Gamma Rhythms

Alzheimer's disease and other dementias are associated with disruptions of electrophysiological brain activity, including low frequency and gamma rhythms. Many of these dementias are also associated with the malfunction of the membrane associated protein tau. Tauopathy disrupts neuronal function and the stability of synapses and is a key driver of neurodegeneration. Here we ask how brain rhythms are affected by tauopathy, at different stages of its progression. We performed local field potential recordings from visual cortex of rTg4510 and control animals at early stages of neurodegeneration (5 months) and at a more advanced stage where pathology is evident (8 months). We measured brain activity in the presence or absence of external visual stimulation, and while monitoring pupil diameter and locomotion to establish animal behavioural states. At 5 months, before substantial pathology, we found an increase in low frequency rhythms during resting state in tauopathic animals. This was because tauopathic animals entered intermittent periods of increased neural synchronisation, where activity across a wide band of low frequencies was strongly correlated. At 8 months, when the degeneration was more advanced, the increased synchronisation and low frequency power was accompanied by a reduction in power in the gamma range, with diverse effects across different components of the gamma rhythm. Our results indicate that slower rhythms are impaired earlier than gamma rhythms in tauopathy, suggesting that electrophysiological measurements can indicate both the presence and progression of tauopathic degeneration.

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Abnormal Low-Gamma Small-World Response After Visual Stimulation in Schizophrenia

10.21203/rs.3.rs-690074/v1 ◽

2021 ◽

Author(s):

Lucas Galdino ◽

Thiago Fernandes ◽

Kerstin Erika Schmidt ◽

Natanael Antonio dos Santos

Keyword(s):

Graph Theory ◽

Evoked Potentials ◽

Visual Processing ◽

Visual Stimulation ◽

Network Connectivity ◽

Small World ◽

Sensory Stimulation ◽

Clustering Coefficient ◽

Characteristic Path Length ◽

Eeg Recordings

Abstract Schizophrenia can be described as a functional dysconnectivity syndrome that affects the brain’s circuits in a generalized way. Global disconnection in schizophrenia has been manifold described by applying graph theory and quantifying parameters of network connectivity. However, little is known about how sensory stimulation modulates networks in schizophrenia, such as small-worldness during visual processing. In order to address this question, we applied graph theory algorithms to EEG recordings and classified the functional network in the alpha (8–13 Hz) and low-gamma (36–55 Hz) bands of 13 patients with schizophrenia (SCZ) and 13 healthy controls (HC) during the presentation of a visual stimulus. We measured the amplitude of visual-evoked potentials and the number of nodes, edges, mean degree centrality, clustering coefficient, characteristic path length (L), and small-worldness (SW). As expected, patients presented smaller peak amplitudes of evoked-potentials than HC. Interestingly, in contrast to the controls, SCZ did not change their small worldness index during visual stimulation. This implies that schizophrenia-related dysconnectivity has an impact on the ability of the low-gamma network to react to new sensory input. These results provide evidence about a possible electrophysiological signature of the global deficits revealed by the application of graph theory onto the EEG in schizophrenia.

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

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1503686112 ◽

2015 ◽

Vol 112 (27) ◽

pp. 8439-8444 ◽

Cited By ~ 118

Author(s):

Jason Samaha ◽

Phoebe Bauer ◽

Sawyer Cimaroli ◽

Bradley R. Postle

Keyword(s):

Visual Processing ◽

Visual Stimulation ◽

Physiological State ◽

Significant Shift ◽

Alpha Band ◽

Target Onset ◽

Top Down ◽

Temporal Prediction ◽

Subsequent Behavior ◽

The Moment

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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