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Schuele, S. U.

Publications and source records attributed to Schuele, S. U..

9 recordsLinked to original sources

The development of slow and fast theta oscillations in the human brain

Theta oscillations are pivotal for attention and memory, with developmental shifts in theta activity and connectivity tracking memory ability across the lifespan. Building on initial evidence that the theta band separates into slow and fast sub-bands across development within the medial temporal lobe (MTL) and the prefrontal cortex (PFC), this preregistered study (https://osf.io/gsru7) characterized the frequencies of slow (~1.5-4.5 Hz) and fast (~4.5-9.0 Hz) theta oscillations across the brain in a large developmental cohort. We analyzed intracranial EEG (iEEG) recordings from widespread brain regions in 101 children and adults (5.93-54.00 years, 63 males; n electrodes = 5691) using task-based (attention to to-be-remembered visual stimuli) and task-free (resting-state) data. We reveal distinct slow and fast theta oscillations in all regions and identify a spatial gradient in both frequency ranges, with slow theta oscillations speeding up and fast theta oscillations slowing down from posterior to anterior regions. The dissociation between slow and fast theta frequencies peaks during young adulthood, mirroring the developmental trajectory of attention and memory. In the hippocampus and PFC, attentional state (task-based, task-free) modulated age effects, and individual differences in task-based slow theta frequencies predicted individual differences in memory performance, linking the development of slow theta oscillations to the development of memory. Gray matter volume was not associated with age- or task-related differences in theta frequencies, suggesting that the development of theta oscillations is independent of regional brain structure. This study establishes developmental trajectories of slow and fast theta oscillations in localized brain regions and links the maturation of hippocampal and PFC slow theta oscillations to the development of attention and memory.

neuroscience↗

Differential roles of frontoparietal regions in working memory and decision-making

Working memory (WM) and decision-making (DM) are closely linked cognitive processes that rely on frontoparietal regions, yet their distinct and shared neural dynamics remain unclear. Using intracranial EEG recordings from 24 human subjects performing a delayed match-to-sample task, we examined high-frequency broadband (HFB) activity to dissociate WM- and DM-related processes with high spatiotemporal resolution. Principal component analysis of frontoparietal HFB activity revealed multiple temporally distinct patterns spanning stimulus presentation and delay phases. The most dominant component reflected sustained WM-related activity across task phases, consistent with persistent maintenance of internal representations. Additional components captured transient WM encoding across trial phases, as well as both stimulus-linked and ramping DM-related activity suggesting dual early and late stages of evaluative processing. These processes were distributed across frontoparietal regions but showed systematic differences in anatomical focus, with WM-related activity concentrated in dorsolateral prefrontal cortex (PFC) and DM-related activity concentrated in ventrolateral PFC, while inferior parietal cortex preferentially tracked the behavioral significance of incoming stimuli and superior parietal cortex tracked the appearance of new information that may require updating ongoing processing. Together, these findings demonstrate that WM and DM processes are separable yet interleaved over time within distributed cortical networks, revealing coordinated but functionally distinct contributions to goal-directed behavior.

neuroscience↗

Visuospatial coding by theta oscillations in human hippocampus

The hippocampus has been proposed to support visual processing and perception, challenging longstanding accounts that emphasize navigation or declarative memory. A key prediction of visual-processing accounts is that the hippocampus should exhibit similar visuospatial coding properties to those of higher-order visual neocortical areas, such as sensitivity to the size of visual stimuli and contralateral visual field biases. We tested for these properties using intracranial EEG to measure hippocampal neural activity during a retinotopic mapping task. The hippocampus exhibited characteristic slow ([~]2 Hz) and fast ([~]8 Hz) theta oscillations throughout the task. Fast theta was responsive to the presence but not the amount of visual stimulation. In contrast, slow theta did not generally respond to stimulus presence but scaled with the size of the visual stimulus, consistent with larger receptive fields. Slow theta also showed a contralateral bias, an effect that was specific to the right hippocampus. None of these effects were attributable to microsaccades or performance of the concurrent vigilance task. These findings provide electrophysiological evidence for visual field coding by human hippocampus, supporting accounts of hippocampal function that emphasize its role atop the visual hierarchy. Visual processing of this kind may combine with self-motion, memory, and other signals to support the broader spatial and mnemonic functions with which hippocampal theta oscillations have long been associated.

neuroscience↗

Cycle-by-cycle respiration waveforms are coupled with the shape of neural oscillations

Beyond sustaining life, breathing is a vital physiological rhythm that shapes cognition, perception, emotional regulation, and mental health. Breathing has a direct effect on neuronal excitability and is coupled to neural oscillations across a variety of brain regions. Notably, both respiration and neural oscillations are asymmetric and not perfectly rhythmic: for example, every breath has a different shape and duration, and is interspersed with variable pauses. Here, we examined the coupling between breathing and the brain by quantifying the nonsinusoidal features of each breath and comparing it to the shape of each corresponding neural oscillation cycle. By leveraging invasive human brain recordings from 16 participants, we found respiration-neural waveform coupling on a breath-by-breath, cycle-by-cycle basis across limbic and cortical forebrain regions. For decades, the dominant perspective on cognition and mental health have focused on the brain, but recent work is highlighting the importance of brain-body interactions. Our results show that the coupling between breathing and neural activity is much richer than previously appreciated, and our approach opens new avenues for studying these peripheral-to-central nervous system interactions in a more robust, temporally precise manner.

neuroscience↗

Distributed theta networks support the control of working memory: Evidence from scalp and intracranial EEG

We combined scalp EEG and intracranial EEG (iEEG) to identify spectral and network-level signatures of executive control during a delayed match-to-sample task working memory task. To isolate executive processes, we contrasted test and sample phases, matched in perceptual input but differing in cognitive demand. Scalp EEG revealed increased frontal midline theta event-related spectral perturbations (ERSPs), dynamic increases and decreases in posterior theta-alpha ERSPs, and decreased central alpha-beta ERSPs during the test phase. These local spectral changes were accompanied by enhanced frontoposterior theta phase synchrony and network hub strength, predicting higher behavioral accuracy. Using a novel cross-modal scalp EEG-iEEG ERSP similarity approach, we localized the sources of scalp-derived frontal midline, posterior, and central control effects to medial frontal, parietal, temporal, and occipital regions. Our results integrate power and connectivity measures across scalp and iEEG, linking local spectral fluctuations to broader network organization. Together, they support a model in which executive control emerges from flexible, temporally precise coordination between medial frontal control hubs and posterior representational systems.

neuroscience↗

Targeting intracranial electrical stimulation to network regions defined within individuals causes network-level effects

Intracranial electrical stimulation (ES) is routinely used therapeutically, diagnostically, and to provide causal evidence in neuroscience studies. However, our understanding of the brain network-level effects of ES remains limited. We applied precision functional mapping (PFM), based on functional magnetic resonance imaging (fMRI), to define large-scale networks within individual epilepsy patients. We show that single-pulse electrical stimulation (SPES) and high-frequency electrical stimulation (HFES) are more likely to evoke within-network responses and elicit network-related behavioral effects, respectively, when applied near to a PFM-defined network region. Network-level effects were more likely when stimulating sites in white matter, in close proximity to the targeted network, and within a region predominantly occupied by the targeted network. Further, network-specific modulation may be achievable by applying lower current intensities at these sites. Our findings support that modulation of specific networks is achievable by targeting ES to a functional anatomic "sweet spot" that can be identified using PFM.

neuroscience↗

Declarative Memory Through the Lens of Single-Trial Peaks in High-Frequency Power

Declarative memory depends on the coordination of local processing, indexed by high-frequency broadband (HFB) activity, with global network organization, indexed by theta oscillations. However, theta and HFB exhibit asynchronous timing, raising the question of how results of local processing are communicated throughout the network. Using intracranial EEG in patients performing a recognition memory task, we examined this coordination across the medial temporal lobe (MTL) and prefrontal cortex (PFC). HFB peak activity was earlier in the MTL than PFC. Anchoring analyses of theta phase clustering and connectivity to HFB peaks revealed strong phase clustering locked to HFB peaks in the PFC, as well as connectivity between the PFC and MTL that predicted individual memory performance. Graph analysis revealed specific connections amidst sparse network connectivity during memory success. This study demonstrates that transient brain states linked to internal physiological events support memory and refines our understanding of local and network-level process interactions. HighlightsO_LIMemory-linked theta activity is time-locked to internal brain events C_LIO_LINetwork connectivity changes dynamically during memory processing C_LIO_LISparse network connectivity supports successful memory C_LIO_LISpecific sequences of transient states may be critical for declarative memory C_LI

neuroscience↗

The development of aperiodic neural activity in the human brain

The neurophysiological mechanisms supporting brain maturation are fundamental to attention and memory capacity across the lifespan. Human brain regions develop at different rates, with many regions developing into the third and fourth decades of life. Here, in this preregistered study (https://osf.io/gsru7), we analyzed intracranial EEG (iEEG) recordings from widespread brain regions in a large developmental cohort. Using task-based (i.e., attention to-be-remembered visual stimuli) and task-free (resting-state) data from 101 children and adults (5.93 - 54.00 years, 63 males; n electrodes = 5691), we mapped aperiodic (1/[f]-like) activity, a proxy of neural noise, with steeper slopes indexing less noise and flatter slopes indexing more noise. We reveal that aperiodic slopes flatten with age into young adulthood in both association and sensorimotor cortices, challenging models of early sensorimotor development based on brain structure. In prefrontal cortex (PFC), attentional state modulated age effects, revealing steeper task-based than task-free slopes in adults and the opposite in children, consistent with the development of cognitive control. Age-related differences in task-based slopes also explained age-related gains in memory performance, linking the development of PFC cognitive control to the development of memory. Last, with additional structural imaging measures, we reveal that age-related differences in gray matter volume are similarly associated with aperiodic slopes in association and sensorimotor cortices. Our findings establish developmental trajectories of aperiodic activity in localized brain regions and illuminate the development of PFC control during adolescence in the development of attention and memory.

neuroscience↗

Human hippocampal responses to network stimulation vary with theta phase

Hippocampal-dependent memory is thought to be supported by distinct connectivity states, with strong input to the hippocampus benefitting encoding and weak input benefitting retrieval. Previous research in rodents suggests that the hippocampal theta oscillation orchestrates the transition between these states, with opposite phase angles predicting minimal versus maximal input. We investigated whether this phase dependence exists in humans using network-targeted intracranial stimulation. Intracranial local field potentials were recorded from individuals with epilepsy undergoing medically necessary stereotactic electroencephalographic recording. In each subject, biphasic bipolar direct electrical stimulation was delivered to lateral temporal sites with demonstrated connectivity to hippocampus. Lateral temporal stimulation evoked ipsilateral hippocampal potentials with distinct early and late components. Using evoked component amplitude to measure functional connectivity, we assessed whether the phase of hippocampal theta predicted relatively high versus low connectivity. We observed an increase in the continuous phase-amplitude relationship selective to the early and late components of the response evoked by lateral temporal stimulation. The maximal difference in these evoked component amplitudes occurred across 180 degrees of separation in the hippocampal theta rhythm; i.e., the greatest difference in component amplitude was observed when stimulation was delivered at theta peak versus trough. The pattern of theta phase dependence observed for hippocampus was not identified for control locations. These findings demonstrate that hippocampal receptivity to input varies with theta phase, suggesting that theta phase reflects connectivity states of human hippocampal networks. These findings confirm a putative mechanism by which neural oscillations modulate human hippocampal function.

neuroscience↗