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Fiebelkorn, I. C.

Publications and source records attributed to Fiebelkorn, I. C..

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Low-frequency phase temporally coordinates multiple working memory operations

Working memory unfolds over time, yet how different working memory operations are temporally coordinated remains unclear. Building on prior links between low-frequency neural oscillations and working memory maintenance and retrieval, as well as evidence that low-frequency oscillations help coordinate cognitive functions, we tested whether low-frequency neural oscillations bridge and/or differentiate distinct working memory operations. Specifically, we tested whether low-frequency phase was linked to memory accuracy and event-related neural responses across three operations: (i) encoding, (ii) retrieval, and (iii) distractor processing during maintenance. Using EEG in human participants, we found that encoding and retrieval were most strongly linked to memory accuracy through theta phase ([~]4-7 Hz), measured just prior to each task event. Pre-encoding theta phase also modulated the neural response to memory item onset, suggesting that theta phase influences encoding strength. Critically, the theta phase associated with better memory accuracy differed significantly between encoding and retrieval, consistent with temporally distinct and functionally specific states supporting each working memory operation. In contrast, the influence of distractors on memory accuracy was linked to alpha phase ([~]8-10 Hz), with distractor occurrence also appearing to re-engage theta-dependent processes associated with encoding and retrieval. Together, these findings suggest that low-frequency neural oscillations provide a temporal framework that bridges multiple operations of working memory. SignificanceWorking memory (WM) relies on multiple operations that must be coordinated over time, yet how these processes are temporally organized remains unclear. Neural oscillations have been proposed as a timing mechanism for cognition, yet evidence linking distinct oscillatory phases to distinct WM operations remains limited. Here, we show that memory accuracy depends on the phase of low-frequency neural activity, with encoding and retrieval linked to opposing theta phases ([~]4-7 Hz), and distractor interference during maintenance linked to alpha phase ([~]8-10 Hz). These findings indicate that distinct WM operations are temporally coordinated within oscillatory cycles, providing evidence that low-frequency neural activity both coordinates and segregates cognitive processes over time.

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Attention-related sampling of targets rhythmically alternates with increased susceptibility to co-occurring distractors

The Rhythmic Theory of Attention proposes that visual spatial attention is characterized by alternating states that promote either sampling at the present focus of attention or a higher likelihood of shifting attentional resources to another location. While theta-rhythmically (4-8 Hz) occurring windows of opportunity for shifting attentional resources might provide cognitive flexibility, these windows might also make us more susceptible to distractors. Here, we used EEG in humans to test how frequency-specific neural activity phasically influences behavioral performance and visual processing when high-contrast distractors co-occur with low-contrast targets. For trials with and without distractors, perceptual sensitivity at the cued target location depended on pre-stimulus theta phase ([~]7 Hz) recorded at central electrodes. For trials with distractors, there was a greater increase in false alarm rates at the same theta phase associated with lower hit rates (i.e., during the proposed shifting state), confirming theta-rhythmically occurring windows of increased susceptibility to distractors. In addition to these phase-behavior effects at central electrodes, we observed phase-behavior effects at frontocentral and occipital electrodes that (i) only occurred on trials with distractors, (ii) peaked in the alpha-frequency range ([~]9- 10 Hz) and (iii) were strongest at occipital electrodes that were contralateral to distractors. Alpha phase at these electrodes was also associated with fluctuations in the amplitude of distractor-evoked visual responses, consistent with an alpha-mediated gating of distractors. The present findings thus provide evidence for distinct theta- and alpha-mediated mechanisms of spatial attention that phasically modulate the influence of distractors on task performance. SignificanceThe Rhythmic Theory of Attention proposes that spatial attention is characterized by alternating states that promote either sampling at the present focus of attention or a higher likelihood of shifting attentional resources to another location. These alternating attentional states are associated with dynamic changes in attention-related neural and behavioral effects, occurring on a timescale in the theta-frequency range (4-8 Hz). Although interdigitated windows for shifting attentional resources might provide critical cognitive flexibility, they might also lead to an increased susceptibility to distractors. Here, we demonstrate such rhythmic fluctuations in susceptibility to high-contrast distractors that co-occur with low-contrast visual targets. Rhythmic attention-related sampling--while perhaps preventing us from becoming overly focused on any single location--can lead to behavioral disadvantages.

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A domain-general process for theta-rhythmic sampling of either environmental information or internally stored information

Selective attention is the collection of mechanisms through which the brain preferentially processes behaviorally important information. Many everyday tasks, such as shopping for groceries, require selective sampling (i.e., attention-related sampling) of both external information (i.e., information from the environment) and internally stored information (i.e., information being maintained in working memory). While there is clear evidence that selective sampling of external information is influenced by internally stored information (and vice versa), the extent to which selective sampling of external and internal information share neural resources remains a focus of debate. Previous research has linked theta-rhythmic (3-8 Hz) neural activity in higher-order (e.g., frontal cortices) and sensory regions to theta-rhythmic changes in behavioral performance during selective sampling. Here, we used EEG and a dual-task design (i.e., a task that required both external and internal information), in male and female humans, to directly compare theta-dependent fluctuations in behavioral performance during external sampling with those during internal sampling. Our findings are consistent with a shared theta-rhythmic process for selectively sampling external information or internal information. This theta-rhythmic sampling is associated with both phase-dependent changes in sensory responses (i.e., as measured with the N1 component) and phase-dependent changes in interactions between external and internal information. The theta phase associated with weaker sensory responses and relatively worse behavioral performance (i.e., the bad phase) is also associated with a slowed perceptual decision-making process (as measured with the CPP component), specifically during dual-task trials when to-be-detected external information matches to-be-remembered internal information. SIGNIFICANCE STATEMENTMost everyday tasks require information from both the external environment and internal memory stores; however, the extent to which selective processing of external and internal information rely on shared neural mechanisms and resources remains a subject of debate. Recent work has demonstrated attention-related, theta-rhythmic fluctuations (3-8 Hz) in neural activity and behavioral performance, perhaps reflecting the temporal coordination of competing functions (e.g., attention-related sampling and shifting). Here, we used EEG and a dual-task design to provide evidence of a shared, theta-rhythmic process for alternately boosting the sampling of either external or internal information. This shared, theta-rhythmic process also modulates interactions between external and internal information on dual-task trials, when these sources of information compete for limited processing resources.

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Attentional Information Routing in The Human Brain

Brain-wide communication supporting flexible behavior requires coordination between sensory and associative regions but how brain networks route sensory information at fast timescales to guide action remains unclear. Using human intracranial electrophysiology and spiking neural networks during spatial attention tasks, where participants detected targets at cued locations, we show that high-frequency activity bursts (HFAb) mark temporal windows of elevated population firing that enable fast, long-range communications. HFAbs were evoked by sensory cues and targets, dynamically coupled to low-frequency rhythms. Notably, both the strength of cue-evoked HFAbs and their decoupling from slow rhythms predicted behavioral accuracy. HFAbs synchronized across the brain, revealing distinct cue- and target-activated subnetworks. These subnetworks exhibited lead-lag dynamics following target onset, with cue-activated subnetworks preceding target-activated subnetworks when cues were informative. Computational modeling suggested that HFAbs reflect transitions to population spiking, denoting temporal windows for network communications supporting attentional performance. These findings establish HFAbs as signatures of population state transitions, supporting information routing across distributed brain networks.

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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. SIGNIFICANCE STATEMENTSelective attention relies on neural mechanisms involved in target enhancement and distractor suppression to guide behavior. Using electrocorticographic data in humans, we show a spatiotemporal dissociation between cortical activities engaged in target facilitation and distractor inhibition during attentional deployment. We also found that, at attended locations, interareal interactions are enhanced through cross-frequency coupling along the visual hierarchy to potentially facilitate the processing of a spatially predictable target. In contrast, at unattended locations, intraareal interactions are enhanced through cross-frequency coupling, and interareal interactions are suppressed, together to potentially attenuate the processing of distractors. Our findings reveal that such a distributed cortical organization and complementary neural mechanisms enable efficient gating and filtering of sensory information in the anticipatory processing of spatial attention.

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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 (PD). Increased alpha power has been linked with attenuated sensory processing, while the PD--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 PD, 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 StatementSelective suppression of distracting information is important for survival, contributing to preferential processing of behaviorally important information. Does foreknowledge of an upcoming distractors 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 distractors 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.

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Rhythmic temporal coordination of neural activity avoids representational conflict during working memory

Selective attention1 is characterized by alternating states associated with either attentional sampling or attentional shifting, helping to avoid functional conflicts by isolating function-specific neural activity in time2-5. We hypothesized that such rhythmic temporal coordination might also help to avoid representational conflicts during working memory6. Multiple items can be simultaneously held in working memory, and these items can be represented by overlapping neural populations7-9. Traditional theories propose that short-term storage of to-be-remembered items occurs through persistent neural activity10-12, 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 the short-term storage of to-be-remembered items13-16. Transient bursts in neural activity17, rather than persistent activity, could serve to occasionally refresh these synaptic changes. Here, we used EEG and response times (RTs) to test whether rhythmic temporal coordination helps to isolate neural activity associated with different to-be-remembered items, which would help to avoid representational conflicts. Consistent with this hypothesis, we report that the relative strength of different item representations alternates over time as a function of frequency-specific phase. Although RTs were linked to theta (~6Hz) and beta (~25 Hz) phase during a memory delay, the relative strength of item representations only alternated as a function of beta phase. The present findings (i) are consistent with rhythmic temporal coordination being a general mechanism for avoiding either functional or representational conflicts during cognitive processes, and (ii) inform models describing the role of oscillatory dynamics in organizing working memory13,18-21.

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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 , {beta}, and{gamma} 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{theta} -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.

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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 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.

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Thalamo-cortical interactions define functional dissociations across the macaque attention network

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. We therefore examined pulvino-cortical interactions during theta-rhythmic sampling by simultaneously recording from FEF, LIP, and the pulvinar. Neural activity propagated from (i) pulvinar to cortex during periods of engagement and (ii) from cortex to pulvinar during periods of disengagement. A rhythmic reweighting of pulvino-cortical interactions thus defines functional dissociations in the macaque attention network.

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