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 (i) whether suppression can be voluntarily deployed, independent of enhancement, and (ii) whether the voluntary deployment of suppression is associated with neural processes that occur prior to 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 the strategic use of a spatial cue. In comparison, higher pre-distractor 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 successful 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.Significance Statement Selective suppression of distracting information is important for survival. There are ongoing debates, however, regarding whether and how selective enhancement can be voluntarily deployed independent of selective enhancement. Here, we recorded EEG while subjects performed a visual search task with cues that indicated the location of upcoming distractors. Behavioral and electrophysiological results revealed that foreknowledge of a distractor's location speeded suppression (relative to non-cued trials), thereby facilitating target detection. The results further revealed that such cue-related suppression of a distractor can occur separate from alpha-related gating of sensory processing. That is, alpha-related suppression in the present task occurred independent of the spatially informative cue (i.e., on both cued and non-cued trials) and later than cue-related suppression (as indexed by later and earlier PD components).

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.

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.

Attentional sampling of visual and auditory objects is captured by theta-modulated neural activity.

Recent evidence suggests that visual attention alternately samples two behaviourally relevant objects at approximately 4 Hz, rhythmically shifting between the objects. Whether similar attentional rhythms exist in other sensory modalities, however, is not yet clear. We therefore adapted and extended an established paradigm to investigate visual and potential auditory attentional rhythms, as well as possible interactions, on both a behavioural (detection performance, N = 33) and a neural level (EEG, N = 18). The results during unimodal attention demonstrate that both visual- and auditory-target detection fluctuate at frequencies of approximately 4-8 Hz, confirming that attentional rhythms are not specific to visual processing. The EEG recordings provided evidence of oscillatory activity that underlies these behavioural effects. At right and left occipital EEG electrodes, we detected counter-phasic theta-band activity (4-8 Hz), mirroring behavioural evidence of alternating sampling between the objects presented right and left of central fixation, respectively. Similarly, alpha-band activity as a signature of relatively suppressed sensory encoding showed a theta-rhythmic, counter-phasic change in power. Moreover, these theta-rhythmic changes in alpha power were predictive of behavioural performance in both sensory modalities. Overall, the present findings provide a new perspective on the multimodal rhythmicity of attention.

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.

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.

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.

The mediodorsal pulvinar coordinates the macaque fronto-parietal network during rhythmic spatial attention.

Spatial attention is discontinuous, sampling behaviorally relevant locations in theta-rhythmic cycles (3-6 Hz). Underlying this rhythmic sampling are intrinsic theta oscillations in frontal and parietal cortices that provide a clocking mechanism for two alternating attentional states that are associated with either engagement at the presently attended location (and enhanced perceptual sensitivity) or disengagement (and diminished perceptual sensitivity). It has remained unclear, however, how these theta-dependent states are coordinated across the large-scale network that directs spatial attention. The pulvinar is a candidate for such coordination, having been previously shown to regulate cortical activity. Here, we examined pulvino-cortical interactions during theta-rhythmic sampling by simultaneously recording from macaque frontal eye fields (FEF), lateral intraparietal area (LIP), and pulvinar. Neural activity propagated from pulvinar to cortex during periods of engagement, and from cortex to pulvinar during periods of disengagement. A rhythmic reweighting of pulvino-cortical interactions thus defines functional dissociations in the attention network.

The Puzzling Pulvinar.

The functional role of the pulvinar, with its widespread cortical connectivity, has remained elusive. In this issue of Neuron, Jaramillo et al. (2019) provide a computational roadmap for how the pulvinar might influence various cognitive behaviors across multiple large-scale networks.

A Rhythmic Theory of Attention.

Recent evidence has demonstrated that environmental sampling is a fundamentally rhythmic process. Both perceptual sensitivity during covert spatial attention and the probability of overt exploratory movements are tethered to theta-band activity (3-8Hz) in the attention network. The fronto-parietal part of this network is positioned at the nexus of sensory and motor functions, directing two tightly coupled processes related to environmental exploration: preferential routing of sensory input and saccadic eye movements. We propose that intrinsic theta rhythms temporally resolve potential functional conflicts by periodically reweighting functional connections between higher-order brain regions and either sensory or motor regions. This rhythmic reweighting alternately promotes either sampling at a behaviorally relevant location (i.e., sensory functions) or shifting to another location (i.e., motor functions).

Neural Mechanisms of Sustained Attention Are Rhythmic.

Classic models of attention suggest that sustained neural firing constitutes a neural correlate of sustained attention. However, recent evidence indicates that behavioral performance fluctuates over time, exhibiting temporal dynamics that closely resemble the spectral features of ongoing, oscillatory brain activity. Therefore, it has been proposed that periodic neuronal excitability fluctuations might shape attentional allocation and overt behavior. However, empirical evidence to support this notion is sparse. Here, we address this issue by examining data from large-scale subdural recordings, using two different attention tasks that track perceptual ability at high temporal resolution. Our results reveal that perceptual outcome varies as a function of the theta phase even in states of sustained spatial attention. These effects were robust at the single-subject level, suggesting that rhythmic perceptual sampling is an inherent property of the frontoparietal attention network. Collectively, these findings support the notion that the functional architecture of top-down attention is intrinsically rhythmic.

A Dynamic Interplay within the Frontoparietal Network Underlies Rhythmic Spatial Attention.

Classic studies of spatial attention assumed that its neural and behavioral effects were continuous over time. Recent behavioral studies have instead revealed that spatial attention leads to alternating periods of heightened or diminished perceptual sensitivity. Yet, the neural basis of these rhythmic fluctuations has remained largely unknown. We show that a dynamic interplay within the macaque frontoparietal network accounts for the rhythmic properties of spatial attention. Neural oscillations characterize functional interactions between the frontal eye fields (FEF) and the lateral intraparietal area (LIP), with theta phase (3-8 Hz) coordinating two rhythmically alternating states. The first is defined by FEF-dominated beta-band activity, associated with suppressed attentional shifts, and LIP-dominated gamma-band activity, associated with enhanced visual processing and better behavioral performance. The second is defined by LIP-specific alpha-band activity, associated with attenuated visual processing and worse behavioral performance. Our findings reveal how network-level interactions organize environmental sampling into rhythmic cycles.

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.

Rhythmic sampling within and between objects despite sustained attention at a cued location.

The brain directs its limited processing resources through various selection mechanisms, broadly referred to as attention. The present study investigated the temporal dynamics of two such selection mechanisms: space- and object-based selection. Previous evidence has demonstrated that preferential processing resulting from a spatial cue (i.e., space-based selection) spreads to uncued locations if those locations are part of the same object (i.e., resulting in object-based selection), but little is known about the relationship between these fundamental selection mechanisms. Here, we used human behavioral data to determine how space- and object-based selection simultaneously evolve under conditions that promote sustained attention at a cued location, varying the cue-to-target interval from 300 to 1100 ms. We tracked visual-target detection at a cued location (i.e., space-based selection), at an uncued location that was part of the same object (i.e., object-based selection), and at an uncued location that was part of a different object (i.e., in the absence of space- and object-based selection). The data demonstrate that even under static conditions, there is a moment-to-moment reweighting of attentional priorities based on object properties. This reweighting is revealed through rhythmic patterns of visual-target detection both within (at 8 Hz) and between (at 4 Hz) objects.

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.

Atypical category processing and hemispheric asymmetries in high-functioning children with autism: revealed through high-density EEG mapping.

Behavioral evidence for an impaired ability to group objects based on similar physical or semantic properties in autism spectrum disorders (ASD) has been mixed. Here, we recorded brain activity from high-functioning children with ASD as they completed a visual-target detection task. We then assessed the extent to which object-based selective attention automatically generalized from targets to non-target exemplars from the same well-known object class (e.g., dogs). Our results provide clear electrophysiological evidence that children with ASD (N=17, aged 8-13 years) process the similarity between targets (e.g., a specific dog) and same-category non-targets (SCNT) (e.g., another dog) to a lesser extent than do their typically developing (TD) peers (N=21). A closer examination of the data revealed striking hemispheric asymmetries that were specific to the ASD group. These findings align with mounting evidence in the autism literature of anatomic underconnectivity between the cerebral hemispheres. Years of research in individuals with TD have demonstrated that the left hemisphere (LH) is specialized toward processing local (or featural) stimulus properties and the right hemisphere (RH) toward processing global (or configural) stimulus properties. We therefore propose a model where a lack of communication between the hemispheres in ASD, combined with typical hemispheric specialization, is a root cause for impaired categorization and the oft-observed bias to process local over global stimulus properties.

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.