Differential neural mechanisms underlie cortical gating of visual spatial attention mediated by alpha-band oscillations.

Selective attention relies on neural mechanisms that facilitate processing of behaviorally relevant sensory information while suppressing irrelevant information, consistently linked to alpha-band oscillations in human M/EEG studies. We analyzed cortical alpha responses from intracranial electrodes implanted in eight epilepsy patients, who performed a visual spatial attention task. Electrocorticographic data revealed a spatiotemporal dissociation between attention-modulated alpha desynchronization, associated with the enhancement of sensory processing, and alpha synchronization, associated with the suppression of sensory processing, during the cue-target interval. Dorsal intraparietal areas contralateral to the attended hemifield primarily exhibited a delayed and sustained alpha desynchronization, while ventrolateral extrastriatal areas ipsilateral to the attended hemifield primarily exhibited an earlier and sustained alpha synchronization. Analyses of cross-frequency coupling between alpha phase and broadband high-frequency activity (HFA) further revealed cross-frequency interactions along the visual hierarchy contralateral to the attended locations. Directionality analyses indicate that alpha phase in early and extrastriatal visual areas modulated HFA power in downstream visual areas, thus potentially facilitating the feedforward processing of an upcoming, spatially predictable target. In contrast, in areas ipsilateral to the attended locations, HFA power modulated local alpha phase in early and extrastriatal visual areas, with suppressed interareal interactions, potentially attenuating the processing of distractors. Our findings reveal divergent alpha-mediated neural mechanisms underlying target enhancement and distractor suppression during the deployment of spatial attention, reflecting enhanced functional connectivity at attended locations, while suppressed functional connectivity at unattended locations. The collective dynamics of these alpha-mediated neural mechanisms play complementary roles in the efficient gating of sensory information.

Separate Cue- and Alpha-Related Mechanisms for Distractor Suppression.

Research on selective attention has largely focused on the enhancement of behaviorally important information, with less focus on the suppression of distracting information. Enhancement and suppression can operate through a push-pull relationship attributable to competitive interactions among neural populations. There has been considerable debate, however, regarding (1) whether suppression can be voluntarily deployed, independent of enhancement, and (2) whether voluntary deployment of suppression is associated with neural processes occurring prior to the distractor onset. Here, we investigated the interplay between pre- and post-distractor neural processes, while male and female human subjects performed a visual search task with a cue that indicated the location of an upcoming distractor. We utilized two established EEG markers of suppression: the distractor positivity (PD) and alpha power (∼8-15 Hz). The PD-a component of event-related potentials-has been linked with successful distractor suppression, and increased alpha power has been linked with attenuated sensory processing. Cueing the location of an upcoming distractor speeded responses and led to an earlier PD, consistent with earlier suppression due to strategic use of a spatial cue. In comparison, higher predistractor alpha power contralateral to distractors led to a later PD, consistent with later suppression. Lower alpha power contralateral to distractors instead led to distractor-related attentional capture. Lateralization of alpha power was not linked to the spatial cue. This observation, combined with differences in the timing of suppression-as indexed by earlier and later PD components-demonstrates that cue-related, voluntary suppression can occur separate from alpha-related gating of sensory processing.

There Is More Evidence of Rhythmic Attention than Can Be Found in Behavioral Studies: Perspective on Brookshire, 2022.

Recent research indicates periodicity in attention-related sampling and switching, with some of the initial findings coming from behavioral studies. Brookshire [Brookshire, G. Putative rhythms in attentional switching can be explained by aperiodic temporal structure. Nature Human Behaviour, 2022, https://doi.org/10.1038/s41562-022-01364-0], points out that widely used approaches to testing for rhythms in behavioral times series can misclassify consistent aperiodic patterns in temporal structure as periodic patterns. Evidence for rhythmic attention, however, is not limited to behavioral data. Here, I briefly discuss (i) issues with differentiating periodic and aperiodic structure in both behavioral and neural time series, (ii) findings from neural data that are consistent with rhythmic sampling and switching during attentional deployment, and (iii) whether alternative approaches to establishing periodicity in behavioral time series, recommended by Brookshire are appropriate for this particular research topic.

Functional Specialization in the Attention Network.

Spatial attention is comprised of neural mechanisms that boost sensory processing at a behaviorally relevant location while filtering out competing information. The present review examines functional specialization in the network of brain regions that directs such preferential processing. This attention network includes both cortical (e.g., frontal and parietal cortices) and subcortical (e.g., the superior colliculus and the pulvinar nucleus of the thalamus) structures. Here, we piece together existing evidence that these various nodes of the attention network have dissociable functional roles by synthesizing results from electrophysiology and neuroimaging studies. We describe functional specialization across several dimensions (e.g., at different processing stages and within different behavioral contexts), while focusing on spatial attention as a dynamic process that unfolds over time. Functional contributions from each node of the attention network can change on a moment-to-moment timescale, providing the necessary cognitive flexibility for sampling from highly dynamic environments.

Neuro-oscillatory phase alignment drives speeded multisensory response times: an electro-corticographic investigation.

Even simple tasks rely on information exchange between functionally distinct and often relatively distant neuronal ensembles. Considerable work indicates oscillatory synchronization through phase alignment is a major agent of inter-regional communication. In the brain, different oscillatory phases correspond to low- and high-excitability states. Optimally aligned phases (or high-excitability states) promote inter-regional communication. Studies have also shown that sensory stimulation can modulate or reset the phase of ongoing cortical oscillations. For example, auditory stimuli can reset the phase of oscillations in visual cortex, influencing processing of a simultaneous visual stimulus. Such cross-regional phase reset represents a candidate mechanism for aligning oscillatory phase for inter-regional communication. Here, we explored the role of local and inter-regional phase alignment in driving a well established behavioral correlate of multisensory integration: the redundant target effect (RTE), which refers to the fact that responses to multisensory inputs are substantially faster than to unisensory stimuli. In a speeded detection task, human epileptic patients (N = 3) responded to unisensory (auditory or visual) and multisensory (audiovisual) stimuli with a button press, while electrocorticography was recorded over auditory and motor regions. Visual stimulation significantly modulated auditory activity via phase reset in the delta and theta bands. During the period between stimulation and subsequent motor response, transient synchronization between auditory and motor regions was observed. Phase synchrony to multisensory inputs was faster than to unisensory stimulation. This sensorimotor phase alignment correlated with behavior such that stronger synchrony was associated with faster responses, linking the commonly observed RTE with phase alignment across a sensorimotor network.

Attentional Information Routing in The Human Brain.

Brain-wide communication supports behaviors that require coordination between sensory and associative regions. However, how large-scale brain networks route sensory information at fast timescales to guide upcoming actions remains unclear. Using spiking neural networks and human intracranial electrophysiology during spatial attention tasks, where participants detected a target at cued locations, we show that high-frequency activity bursts (HFAb) serve as information-carrying events, facilitating fast and long-range communications. HFAbs emerged as bouts of neural population spiking and were coordinated brain-wide through low-frequency rhythms. At the network-level, HFAb coordination identified distinct cue- and target-activated subnetworks. HFAbs following the cue onset in cue-subnetworks predicted successful target detection and preceded the information in target-subnetworks following target onset. Our findings suggest HFAbs as a neural mechanism for fast brain-wide information routing that supports attentional performance.

Multisensory representation of frequency across audition and touch: high density electrical mapping reveals early sensory-perceptual coupling.

The frequency of environmental vibrations is sampled by two of the major sensory systems, audition and touch, notwithstanding that these signals are transduced through very different physical media and entirely separate sensory epithelia. Psychophysical studies have shown that manipulating frequency in audition or touch can have a significant cross-sensory impact on perceived frequency in the other sensory system, pointing to intimate links between these senses during computation of frequency. In this regard, the frequency of a vibratory event can be thought of as a multisensory perceptual construct. In turn, electrophysiological studies point to temporally early multisensory interactions that occur in hierarchically early sensory regions where convergent inputs from the auditory and somatosensory systems are to be found. A key question pertains to the level of processing at which the multisensory integration of featural information, such as frequency, occurs. Do the sensory systems calculate frequency independently before this information is combined, or is this feature calculated in an integrated fashion during preattentive sensory processing? The well characterized mismatch negativity, an electrophysiological response that indexes preattentive detection of a change within the context of a regular pattern of stimulation, served as our dependent measure. High-density electrophysiological recordings were made in humans while they were presented with separate blocks of somatosensory, auditory, and audio-somatosensory "standards" and "deviants," where the deviant differed in frequency. Multisensory effects were identified beginning at ∼200 ms, with the multisensory mismatch negativity (MMN) significantly different from the sum of the unisensory MMNs. This provides compelling evidence for preattentive coupling between the somatosensory and auditory channels in the cortical representation of frequency.

Auditory-driven phase reset in visual cortex: human electrocorticography reveals mechanisms of early multisensory integration.

Findings in animal models demonstrate that activity within hierarchically early sensory cortical regions can be modulated by cross-sensory inputs through resetting of the phase of ongoing intrinsic neural oscillations. Here, subdural recordings evaluated whether phase resetting by auditory inputs would impact multisensory integration processes in human visual cortex. Results clearly showed auditory-driven phase reset in visual cortices and, in some cases, frank auditory event-related potentials (ERP) were also observed over these regions. Further, when audiovisual bisensory stimuli were presented, this led to robust multisensory integration effects which were observed in both the ERP and in measures of phase concentration. These results extend findings from animal models to human visual cortices, and highlight the impact of cross-sensory phase resetting by a non-primary stimulus on multisensory integration in ostensibly unisensory cortices.

Distractor suppression does and does not depend on pre-distractor alpha-band activity.

Selective attention enhances behaviorally important information and suppresses distracting information. Research on the neural basis of selective attention has largely focused on sensory enhancement, with less focus on sensory suppression. Enhancement and suppression can operate through a push-pull relationship that arises from competitive interactions among neural populations. There has been considerable debate, however, regarding (i) whether suppression can also operate independent of enhancement and (ii) whether neural processes associated with the voluntary deployment of suppression can occur prior to distractor onset. We provide further behavioral and electrophysiological evidence of independent suppression at cued distractor locations while humans performed a visual search task. We specifically utilize two established EEG markers of suppression: alpha power (∼8-15 Hz) and the distractor positivity (P D ). Increased alpha power has been linked with attenuated sensory processing, while the P D -a component of event-related potentials-has been linked with successful distractor suppression. The present results demonstrate that cueing the location of an upcoming distractor speeded responding and led to an earlier onset P D , consistent with earlier suppression due to strategic use of a spatial cue. We further demonstrate that higher pre-distractor alpha power contralateral to distractors was generally associated with successful suppression on both cued and non-cued trials. However, there was no consistent change in alpha power associated with the spatial cue, meaning cueing effects on behavioral and neural measures occurred independent of alpha-related gating of sensory processing. These findings reveal the importance of pre-distractor neural processes for subsequent distractor suppression. Significance Statement: Selective suppression of distracting information is important for survival, contributing to preferential processing of behaviorally important information. Does foreknowledge of an upcoming distractor's location help with suppression? Here, we recorded EEG while subjects performed a target detection task with cues that indicated the location of upcoming distractors. Behavioral and electrophysiological results revealed that foreknowledge of a distractor's location speeded suppression, thereby facilitating target detection. The results further revealed a significant relationship between pre-stimulus alpha-band activity and successful suppression; however, pre-stimulus alpha-band activity was not consistently lateralized relative to the spatially informative cues. The present findings therefore demonstrate that target detection can benefit from foreknowledge of distractor location in a process that is independent of alpha-related gating of sensory processing.

Rhythmic temporal coordination of neural activity prevents representational conflict during working memory.

Selective attention1 is characterized by alternating states associated with either attentional sampling or attentional shifting, helping to prevent functional conflicts by isolating function-specific neural activity in time.2,3,4,5 We hypothesized that such rhythmic temporal coordination might also help to prevent representational conflicts during working memory.6 Multiple items can be simultaneously held in working memory, and these items can be represented by overlapping neural populations.7,8,9 Traditional theories propose that the short-term storage of to-be-remembered items occurs through persistent neural activity,10,11,12 but when neurons are simultaneously representing multiple items, persistent activity creates a potential for representational conflicts. In comparison, more recent, "activity-silent" theories of working memory propose that synaptic changes also contribute to short-term storage of to-be-remembered items.13,14,15,16 Transient bursts in neural activity,17 rather than persistent activity, could serve to occasionally refresh these synaptic changes. Here, we used EEG and response times to test whether rhythmic temporal coordination helps to isolate neural activity associated with different to-be-remembered items, thereby helping to prevent representational conflicts. Consistent with this hypothesis, we report that the relative strength of different item representations alternates over time as a function of the frequency-specific phase. Although RTs were linked to theta (∼6 Hz) and beta (∼25 Hz) phases during a memory delay, the relative strength of item representations only alternated as a function of the beta phase. The present findings (1) are consistent with rhythmic temporal coordination being a general mechanism for preventing functional or representational conflicts during cognitive processes and (2) inform models describing the role of oscillatory dynamics in organizing working memory.13,18,19,20,21.

Interacting rhythms enhance sensitivity of target detection in a fronto-parietal computational model of visual attention.

Even during sustained attention, enhanced processing of attended stimuli waxes and wanes rhythmically, with periods of enhanced and relatively diminished visual processing (and subsequent target detection) alternating at 4 or 8 Hz in a sustained visual attention task. These alternating attentional states occur alongside alternating dynamical states, in which lateral intraparietal cortex (LIP), the frontal eye field (FEF), and the mediodorsal pulvinar (mdPul) exhibit different activity and functional connectivity at α, ß, and γ frequencies-rhythms associated with visual processing, working memory, and motor suppression. To assess whether and how these multiple interacting rhythms contribute to periodicity in attention, we propose a detailed computational model of FEF and LIP. When driven by θ-rhythmic inputs simulating experimentally-observed mdPul activity, this model reproduced the rhythmic dynamics and behavioral consequences of observed attentional states, revealing that the frequencies and mechanisms of the observed rhythms allow for peak sensitivity in visual target detection while maintaining functional flexibility.

Ready, set, reset: stimulus-locked periodicity in behavioral performance demonstrates the consequences of cross-sensory phase reset.

The simultaneous presentation of a stimulus in one sensory modality often enhances target detection in another sensory modality, but the neural mechanisms that govern these effects are still under investigation. Here, we test a hypothesis proposed in the neurophysiological literature: that auditory facilitation of visual-target detection operates through cross-sensory phase reset of ongoing neural oscillations (Lakatos et al., 2009). To date, measurement limitations have prevented this potentially powerful neural mechanism from being directly linked with its predicted behavioral consequences. The present experiment uses a psychophysical approach in humans to demonstrate, for the first time, stimulus-locked periodicity in visual-target detection, following a temporally informative sound. Our data further demonstrate that periodicity in behavioral performance is strongly influenced by the probability of audiovisual co-occurrence. We argue that fluctuations in visual-target detection result from cross-sensory phase reset, both at the moment it occurs and persisting for seconds thereafter. The precise frequency at which this periodicity operates remains to be determined through a method that allows for a higher sampling rate.

Common or redundant neural circuits for duration processing across audition and touch.

Certain features of objects or events can be represented by more than a single sensory system, such as roughness of a surface (sight, sound, and touch), the location of a speaker (audition and sight), and the rhythm or duration of an event (by all three major sensory systems). Thus, these properties can be said to be sensory-independent or amodal. A key question is whether common multisensory cortical regions process these amodal features, or does each sensory system contain its own specialized region(s) for processing common features? We tackled this issue by investigating simple duration-detection mechanisms across audition and touch; these systems were chosen because fine duration discriminations are possible in both. The mismatch negativity (MMN) component of the human event-related potential provides a sensitive metric of duration processing and has been elicited independently during both auditory and somatosensory investigations. Employing high-density electroencephalographic recordings in conjunction with intracranial subdural recordings, we asked whether fine duration discriminations, represented by the MMN, were generated in the same cortical regions regardless of the sensory modality being probed. Scalp recordings pointed to statistically distinct MMN topographies across senses, implying differential underlying cortical generator configurations. Intracranial recordings confirmed these noninvasive findings, showing generators of the auditory MMN along the superior temporal gyrus with no evidence of a somatosensory MMN in this region, whereas a robust somatosensory MMN was recorded from postcentral gyrus in the absence of an auditory MMN. The current data clearly argue against a common circuitry account for amodal duration processing.

Pitting binding against selection--electrophysiological measures of feature-based attention are attenuated by Gestalt object grouping.

Humans have limited cognitive resources to process the nearly limitless information available in the environment. Endogenous, or 'top-down', selective attention to basic visual features such as color or motion is a common strategy for biasing resources in favor of the most relevant information sources in a given context. Opposing this top-down separation of features is a 'bottom-up' tendency to integrate, or bind, the various features that constitute objects. We pitted these two processes against each other in an electrophysiological experiment to test if top-down selective attention can overcome constitutive binding processes. Our results demonstrate that bottom-up binding processes can dominate top-down feature-based attention even when explicitly detrimental to task performance.

Auditory facilitation of visual-target detection persists regardless of retinal eccentricity and despite wide audiovisual misalignments.

It is well established that sounds can enhance visual-target detection, but the mechanisms that govern these cross-sensory effects, as well as the neural pathways involved, are largely unknown. Here, we tested behavioral predictions stemming from the neurophysiologic and neuroanatomic literature. Participants detected near-threshold visual targets presented either at central fixation or peripheral to central fixation that were sometimes paired with sounds that originated from widely misaligned locations (up to 104° from the visual target). Our results demonstrate that co-occurring sounds improve the likelihood of visual-target detection (1) regardless of retinal eccentricity and (2) despite wide audiovisual misalignments. With regard to the first point, these findings suggest that auditory facilitation of visual-target detection is unlikely to operate through previously described corticocortical pathways from auditory cortex that predominantly terminate in regions of visual cortex that process peripheral visual space. With regard to the second point, auditory facilitation of visual-target detection seems to operate through a spatially non-specific modulation of visual processing.

Dual mechanisms for the cross-sensory spread of attention: how much do learned associations matter?

The spread of attention-related processing across anatomically separated cortical regions plays an important role in the binding of an object's features, both within and across sensory modalities. We presented multiple exemplars of semantically congruent multisensory objects (e.g., dogs with barks) and semantically incongruent multisensory objects (e.g., guitars with barks) while recording high-density event-related potentials and tested whether highly learned associations among the multisensory features of well-known objects modulated the spread of attention from an attended visual stimulus to its paired, task-irrelevant sound. Our findings distinguish dual mechanisms for the cross-sensory spread of attention: 1) a stimulus-driven spread of attention that occurs whenever a task-irrelevant sound is simultaneously presented with an attended visual stimulus, independent of highly learned associations, and 2) a representation-driven spread of attention that occurs in response to a task-irrelevant sound that is semantically congruent with a visual target and is therefore dependent on highly learned associations. The first mechanism is thought to reflect bottom-up feature binding, whereas the second mechanism is thought to reflect the top-down activation of a stored object representation that includes the well-known object's multisensory features. When a semantically congruent, task-irrelevant sound is simultaneously presented with a well-known visual target, the combined spread of attention through both mechanisms appears additive.

Spike Timing in the Attention Network Predicts Behavioral Outcome Prior to Target Selection.

There has been little evidence linking changes in spiking activity that occur prior to a spatially predictable target (i.e., prior to target selection) to behavioral outcomes, despite such preparatory changes being widely assumed to enhance the sensitivity of sensory processing. We simultaneously recorded from frontal and parietal nodes of the attention network while macaques performed a spatial cueing task. When anticipating a spatially predictable target, different patterns of coupling between spike timing and the oscillatory phase in local field potentials-but not changes in spike rate-were predictive of different behavioral outcomes. These behaviorally relevant differences in local and between-region synchronization occurred among specific cell types that were defined based on their sensory and motor properties, providing insight into the mechanisms underlying enhanced sensory processing prior to target selection. We propose that these changes in neural synchronization reflect differential anticipatory engagement of the network nodes and functional units that shape attention-related sampling.

Staying within the lines: the formation of visuospatial boundaries influences multisensory feature integration.

The brain processes multisensory features of an object (e.g., its sound and shape) in separate cortical regions. A key question is how representations of these features bind together to form a coherent percept (the 'binding problem'). Here we tested the hypothesis that the determination of an object's visuospatial boundaries is paramount to the linking of its multisensory features (i.e., that the refinement of attended space through the formation of visual boundaries establishes the boundaries for multisensory feature integration). We recorded both scalp and intracranial electrophysiological data in response to Kanizsa-type illusory contour stimuli (in which pacman-like elements give the impression of a single object), their non-illusory counterparts, and auditory stimuli. Participants performed a visual task and ignored sounds. Enhanced processing of task-irrelevant sounds when paired with attended visual stimuli served as our metric for multisensory feature integration [e.g., Busse et al. (2005) Proc. Natl Acad. Sci. USA 102: 18751-18756]. According to our hypothesis, task-irrelevant sounds paired with Kanizsa-type illusory contour stimuli (which have well-defined boundaries) should receive enhanced processing relative to task-irrelevant sounds paired with non-illusory contour stimuli (which have ambiguous boundaries). The scalp data clearly support this prediction and, combined with the intracranial data, advocate for an important extension of models for multisensory feature integration. We propose a model in which (i) the visual boundaries of an object are established through processing in occipitotemporal cortex, and (ii) attention then spreads to cortical regions that process features that fall within the object's established visual boundaries, including its task-irrelevant multisensory features.

Dynamic pulvino-cortical interactions in the primate attention network.

While research in previous decades demonstrated a link between the pulvinar nucleus of the thalamus and visual selective attention, the pulvinar's specific functional role has remained elusive. However, methodological advances in electrophysiological recordings in non-human primates, including simultaneous recordings in multiple brain regions, have recently begun to reveal the pulvinar's functional contributions to selective attention. These new findings suggest that the pulvinar is critical for the efficient transmission of sensory information within and between cortical regions, both synchronizing cortical activity across brain regions and controlling cortical excitability. These new findings further suggest that the pulvinar's influence on cortical processing is embedded in a dynamic selection process that balances sensory and motor functions within the large-scale network that directs selective attention.