Biology subjects

Staresina, B.

Publications and source records attributed to Staresina, B..

18 recordsLinked to original sources

bioRxiv2026

Sleep spindles enhance latent working memory representations

Working memory (WM) allows recently encountered information to be maintained over short periods, yet neural mechanisms supporting this short-term accessibility remain debated. Recent work suggests that WM representations can be maintained without persistent neural firing, in latent synaptic states often termed "activity-silent" memory. Such states can be reactivated by brief perturbations of cortical networks ("pinging"), providing a way to probe otherwise hidden representations. If such latent states rely on synaptic plasticity, they may be sensitive to sleep-dependent recalibration of cortical circuits. Here, we test whether sleep spindles, transient thalamo-cortical oscillations linked to synaptic plasticity, shape post-sleep accessibility of WM representations. Thirty participants performed a visual WM task before and after a daytime nap while high-density EEG was recorded. During the post-nap task, brief visual impulses were used to probe latent WM states, enabling multivariate decoding of memorised content. We show that longer spindle duration during prior NREM sleep predicts both improved post-sleep WM performance and higher-fidelity impulse-evoked decoding of item-specific representations, even when controlling for pre-sleep WM ability. These relationships were selective to spindles; slow-oscillation duration and other oscillatory metrics showed no corresponding effects. Together, our findings link sleep spindle dynamics to the neural readout of activity-silent WM and suggest that sleep-dependent synaptic recalibration optimises cortical circuits for subsequent, short-term information processing.

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bioRxiv2026

Hippocampal ripples evoke a stereotyped cortical response followed by spindle-mediated network synchronization.

Hippocampal sharp-wave ripples (SWRs) are thought to play a key role in systems memory consolidation by broadcasting reactivated memory content to distributed cortical networks while we sleep. Elucidating how this hippocampal-cortical dialogue unfolds at the brain-wide level is therefore essential to understanding how sleep transforms new experiences into lasting memories. Here we combined simultaneous hippocampal intracranial EEG and 21-channel scalp EEG during overnight sleep to characterize the large-scale cortical impact of hippocampal ripple events. We found that individual hippocampal ripples elicited a decodable, phase-locked cortical response at the scalp level. This cortical response was followed by increases in cortico-cortical synchronization and network density in the spindle-band. Mediation analyses revealed a sequential pathway in which ripple magnitude predicted large-scale cortical connectivity through this intermediate cortical response and subsequent spindle activity. These findings demonstrate that hippocampal ripples trigger a two-step cascade, i.e., an early stereotyped cortical response followed by spindle-mediated network synchronization, consistent with the view that SWRs co-activate distributed cortical nodes and potentiate the cortical-cortical connections that support memory consolidation. By demonstrating that ripple-related cortical responses are decodable noninvasively, our results moreover suggest a new strategy for inferring hippocampal ripple activity from scalp electrophysiology. Significance StatementHippocampal sharp-wave ripples are brief bursts of coordinated neural activity believed to support memory consolidation by coordinating communication between the hippocampus and the cortex during sleep. Although animal studies show that ripples influence widespread cortical activity, their large-scale cortical effects in humans have previously only been measurable through invasive brain recordings. By combining hippocampal intracranial recordings with scalp EEG, we show that hippocampal ripples evoke a cortical response decodable noninvasively, followed by widespread spindle-mediated synchronization across cortical networks. These findings reveal a temporally structured cascade linking hippocampal activity to large-scale cortical coordination during sleep and suggest that ripple-driven brain-wide responses can be monitored using non-invasive EEG recordings.

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bioRxiv2024

Characterizing neuronal and population responses to electrical stimulation in the human hippocampo-cortical network

Direct electrical stimulation (DES) can advance our understanding of the intricate dynamics of the human hippocampo-neocortical network, which underlies complex cognitive processes such as spatial cognition and memory. This knowledge can help Neurotechnology to more effectively interface with this network and improve its functions. Here, we investigated the effects of DES in seven epilepsy patients under medical supervision recording single neuron activity alongside local field potentials to investigate neural responses to single pulses at different levels of granularity. Our results demonstrate that (i) single neurons respond to local electrical stimulation with a stereotypical pattern of short-lived increased excitation, followed by sustained inhibition, (ii) that input into the hippocampus from neocortex takes [~]100 ms, and (iii) that output from the hippocampus to the neocortex is gated by theta phase. These results are vital to inform the optimal choice of parameters for future electrical stimulation studies targeting the human memory system.

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bioRxiv2024

Hippocampal ripples during offline periods predict human motor sequence learning

High-frequency bursts in the hippocampus, known as ripples (80-120 Hz in humans), have been shown to support episodic memory processes. However, converging recent evidence in rodent models as well as human neuroimaging suggests that the hippocampus may be involved in a wider range of memory domains, including motor sequence learning (MSL). Nevertheless, no direct link between hippocampal ripples and MSL has yet been established. Here, we recorded intracranial electroencephalography from the hippocampus in 20 epilepsy patients during a MSL task in which participants showed steady improvement across nine 30-second training blocks interspersed with 30-second rest ( offline) periods. We first demonstrate that ripple rates strongly increase during rest periods relative to training blocks. Importantly, ripple rates during rest periods tracked learning behaviour, both across blocks and across participants. These results suggest that hippocampal ripples during offline periods play a functional role in motor sequence learning and that the hippocampus may be involved in offline learning beyond episodic memory.

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bioRxiv2023

How coupled slow oscillations, spindles and ripples control neuronal processing and communication during human sleep

Learning and plasticity rely on fine-tuned regulation of neuronal circuits during offline periods. An unresolved puzzle is how the sleeping brain - in the absence of external stimulation or conscious effort - controls neuronal firing rates (FRs) and communication within and across circuits, supporting synaptic and systems consolidation. Using intracranial Electroencephalography (iEEG) combined with multiunit activity (MUA) recordings from the human hippocampus and surrounding medial temporal lobe (MTL) areas, we here show that governed by slow oscillation (SO) up-states, sleep spindles set a timeframe for ripples to occur. This sequential coupling leads to a stepwise increase in (i) neuronal FRs, (ii) short-latency cross-correlations among local neuronal assemblies and (iii) cross-regional MTL interactions. Triggered by SOs and spindles, ripples thus establish optimal conditions for spike-timing dependent plasticity and systems consolidation. These results unveil how the coordinated coupling of specific sleep rhythms orchestrates neuronal processing and communication during human sleep.

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bioRxiv2021

Post-encoding reactivation promotes one-shot learning of episodes in humans

Prior animal and human work have shown that post-encoding reinstatement plays an important role in organizing the temporal sequence of unfolding episodes in memory. Here, we investigated whether post-encoding reinstatement serves to promote the encoding of one-shot episodic learning beyond the temporal structure in humans. In experiment 1, participants encoded sequences of pictures depicting unique and meaningful episodic-like events. We used representational similarity analysis on scalp electroencephalography recordings during encoding and found evidence of rapid picture elicited EEG patterns reinstatement at episodic offset (around 500ms post-episode). Memory reinstatement was not observed between successive elements within an episode and the degree of memory reinstatement at episodic offset predicted later recall for that episode. In experiment 2, participants encoded a shuffled version of the picture sequences from experiment 1, rendering each episode meaningless to the participant but temporally structured as in experiment 1, and we found no evidence of memory reinstatement at episodic offset. These results suggest that post-encoding memory reinstatement is akin to the rapid formation of unique and meaningful episodes that unfold over time.

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bioRxiv2021

Fronto-medial theta coordinates posterior maintenance of working memory content

How does the human brain manage multiple bits of information to guide goal-directed behaviour? Successful working memory (WM) functioning has consistently been linked to oscillatory power in the theta frequency band (4-8 Hz) over fronto-medial cortex (fronto-medial theta, FMT). Specifically, FMT is thought to reflect the mechanism of an executive sub-system that coordinates maintenance of memory contents in posterior regions. However, direct evidence for the role of FMT in controlling specific WM content is lacking. Here we collected high-density Electroencephalography (EEG) data whilst participants engaged in load-varying WM tasks and then used multivariate decoding methods to examine WM content during the maintenance period. Higher WM load elicited a focal increase in FMT. Importantly, decoding of WM content was driven by posterior/parietal sites, which in turn showed load-induced functional theta coupling with fronto-medial cortex. Finally, we observed a significant slowing of FMT frequency with increasing WM load, consistent with the hypothesised broadening of a theta duty cycle to accommodate additional WM items. Together these findings demonstrate that frontal theta orchestrates posterior maintenance of WM content. Moreover, the observed frequency slowing elucidates the function of FMT oscillations by specifically supporting phase-coding accounts of WM. Significance StatementHow does the brain juggle the maintenance of multiple items in working memory (WM)? Here we show that increased WM demands increase theta power (4-8 Hz) in fronto-medial cortex. Interestingly, using a machine learning approach, we found that the content held in WM could be read out not from frontal, but from posterior areas. These areas were in turn functionally coupled with fronto-medial cortex, consistent with the idea that frontal cortex orchestrates WM representations in posterior regions. Finally, we observed that holding an additional item in WM leads to significant slowing of the frontal theta rhythm, supporting computational models that postulate longer duty cycles to accommodate additional WM demands.

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bioRxiv2021

Oscillations support co-firing of neurons in the service of human memory formation

Theta and gamma oscillations in the medial temporal lobe are suggested to play a critical role for human memory formation via establishing synchrony in neural assemblies. Arguably, such synchrony facilitates efficient information transfer between neurons and enhances synaptic plasticity, both of which benefit episodic memory formation. However, to date little evidence exists from humans that would provide direct evidence for such a specific role of theta and gamma oscillations for episodic memory formation. Here we investigate how oscillations shape the temporal structure of neural firing during memory formation in the medial temporal lobe. We measured neural firing and local field potentials in human epilepsy patients via micro-wire electrode recordings to analyze how brain oscillations promote co-incidences of firing between neurons during successful and unsuccessful encoding of episodic memories. The results show that phase-coupling of neurons to faster theta and gamma oscillations correlates with co-firing at short latencies ([~]20-30 ms) and occurs during successful memory formation. Phase-coupling at slower oscillations in these same frequency bands, in contrast, correlates with longer co-firing latencies and occurs during memory failure. Thus, our findings provide evidence which implicate neural oscillations into the synchronization of neural firing in the medial temporal lobe during the encoding of episodic memories.

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bioRxiv2020

Theta rhythmicity governs the timing of behavioral and hippocampal responses in humans specifically during memory-dependent tasks

1.Memory formation and reinstatement are thought to lock to the hippocampal theta rhythm, predicting that encoding and retrieval processes appear rhythmic themselves. Here, we show that rhythmicity can be observed in behavioral responses from memory tasks, where participants indicate, using button presses, the timing of encoding or retrieval of cue-object associative memories. We found no evidence for rhythmicity in button presses for visual tasks using the same stimuli, or for questions about already retrieved objects. The oscillations for correctly remembered trials center in the slow theta frequency range (1-5 Hz), while responses from later forgotten trials do not lock to the behavioral oscillation. Using intracranial EEG recordings, we show that the memory task induces temporally extended phase consistency in hippocampal local field potentials at slow theta frequencies, but only for correctly remembered trials, providing a mechanistic underpinning for the theta oscillations found in behavioral responses.

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bioRxiv2020

Disentangling the roles of neocortical alpha/beta and hippocampal theta/gamma activity in human episodic memory

To form an episodic memory, we must first process a vast amount of sensory information about a to-be-encoded event and then bind these sensory representations together to form a coherent memory. While these two cognitive capabilities are thought to have two distinct neural origins, with neocortical alpha/beta oscillations supporting information representation and hippocampal theta-gamma phase-amplitude coupling supporting mnemonic binding, evidence for a dissociation between these two neural markers is conspicuously absent. To address this, seventeen human participants completed a sequence-learning task that first involved processing information about three stimuli, and then binding these stimuli together into a coherent memory trace, all the while undergoing MEG recordings. We found that decreases in neocortical alpha/beta power during sequence perception, but not mnemonic binding, correlated with enhanced memory performance. Hippocampal theta/gamma phase-amplitude coupling, however, showed the opposite pattern; increases during mnemonic binding (but not sequence perception) correlated with enhanced memory performance. These results demonstrate that memory-related decreases in neocortical alpha/beta power and memory-related increases in hippocampal theta/gamma phase-amplitude coupling arise at distinct stages of the memory formation process. We speculate that this temporal dissociation reflects a functional dissociation in which neocortical alpha/beta oscillations could support the processing of incoming information relevant to the memory, while hippocampal theta-gamma phase-amplitude coupling could support the binding of this information into a coherent memory trace.

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bioRxiv2020

Sharp-wave ripples in human amygdala and their coordination with hippocampus

Cooperative interactions between the amygdala and hippocampus are widely regarded as critical for overnight emotional processing of waking experiences, but direct support from the human brain for such a dialog is absent. Using intracranial recordings in four pre-surgical epilepsy patients (two male, two female), we discovered ripples within human amygdala during non-rapid eye movement (NREM) sleep. Like hippocampal ripples, amygdala ripples are strongly associated with sharp waves, are linked to sleep spindles, and tend to co-occur with their hippocampal counterparts. Moreover, sharp waves and ripples are temporally linked across the two brain structures, with amygdala ripples occurring during hippocampal sharp waves and vice versa. Combined with further evidence of interregional sharp wave and spindle synchronization, these findings offer a potential physiological substrate for the NREM-sleep-dependent consolidation and regulation of emotional experiences.

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bioRxiv2019

Phase-based coordination of hippocampal and neocortical oscillations during human sleep

During sleep, new memories undergo a gradual transfer from the hippocampus (HPC) to the neocortex (NC). Precisely timed neural oscillations interacting within and between these brain structures are thought to mediate this sleep-dependent memory consolidation, but exactly which sleep oscillations instantiate the HPC-NC dialog, and via what mechanisms, remains elusive. Employing invasive electroencephalography in ten neurosurgical patients across a full night of sleep, we identified three broad classes of phase-based HPC-NC communication. First, we observed interregional phase synchrony for non-rapid eye movement (NREM) spindles, N2 and rapid eye movement (REM) theta, and N3 beta activity. Second, and most intriguingly, we found asymmetrical N3 cross-frequency phase-amplitude coupling between HPC SOs and NC activity spanning the delta to high-gamma/ripple bands, but not in the opposite direction. Lastly, N2 theta and NREM spindle synchrony were themselves modulated by HPC SOs. These novel forms of phase-based interregional communication emphasize the role of HPC SOs in the HPC-NC dialog, and may offer a physiological basis for the sleep-dependent reorganization of mnemonic content.

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bioRxiv2019

Autobiographical memory reactivation in empathy

Empathy relies on the ability to mirror and to explicitly infer others inner states. Theoretical accounts suggest that memories play a role in empathy but direct evidence of a reactivation of autobiographical memories (AM) in empathy is yet to be shown. We addressed this question in two experiments. In experiment 1, electrophysiological activity (EEG) was recorded from 28 participants who performed an empathy task in which targets for empathy were depicted in contexts for which participants either did or did not have an AM, followed by a task that explicitly required memory retrieval of the AM and non-AM contexts. The retrieval task was implemented to extract the neural fingerprints of AM and non-AM contexts, which were then used to probe data from the empathy task. An EEG pattern classifier was trained and tested across tasks and showed evidence for AM reactivation when participants were preparing their judgement in the empathy task. Participants self-reported higher empathy for people depicted in situations they had experienced themselves as compared to situations they had not experienced. A second independent fMRI experiment replicated this behavioural finding and showed the predicted activation in the brain networks underlying both AM retrieval and empathy: precuneus, posterior parietal cortex, superior and inferior parietal lobule and superior frontal gyrus. Together, our study reports behavioural, electrophysiological and fMRI evidence that robustly supports the involvement of AM reactivation in empathy.

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bioRxiv2019

Sleep spindles mediate hippocampal-neocortical coupling during sharp-wave ripples

Sleep is pivotal for the consolidation of memories [1]. According to two-stage accounts, experiences are temporarily stored in the hippocampus and gradually translocated to neocortical sites during non-rapid-eye-movement (NREM) sleep [2,3]. Mechanistically, information transfer is thought to rely on interactions between thalamocortical spindles and hippocampal ripples. In particular, spindles may open precisely-timed communication channels, across which reactivation patterns may travel between the hippocampus and cortical target sites when ripples occur. To test this hypothesis, we first derived time-frequency representations (TFRs) in hippocampus (HIPP) and at scalp electrode Cz (neocortex, NC) time-locked to individual hippocampal ripple events. Compared to matched ripple-free intervals, results revealed a concurrent increase in spindle power both in HIPP and NC. As revealed by coherence analysis, hippocampal-neocortical coupling was indeed enhanced in the spindle band around ripples. Finally, we examined the directionality of spindle coupling and observed a strong driving effect from NC to HIPP. Specifically, [~]250 ms prior to the HIPP ripple, NC spindles emerge and entrain HIPP spindles. Both regions then remain synchronised until [~]500 ms after the ripple. Consistent with recent rodent work, these findings suggest that active consolidation is initiated by neocortex and draws on neocortical-hippocampal-neocortical reactivation loops [4], with a role of sleep spindles in mediating this process.

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bioRxiv2019

Alpha rhythms reveal when, where and how memories are retrieved

Our memories for past experiences can range from vague recognition to full-blown recall of associated details. Neuroimaging research has tried to understand the brain mechanisms underlying qualitatively different memories for decades (Yonelinas, 2002). On the one hand, Electroencephalography (EEG) has shown that recall signals unfold a few hundred milliseconds after simple recognition and are hallmarked by sustained voltage deflections over left posterior sensors (Herron, 2007; Johansson & Mecklinger, 2003; Mecklinger, Rosburg, & Johansson, 2016; Rugg & Curran, 2007). However, sensor-based analyses only provide limited insights into the supporting brain networks. On the other hand, functional magnetic resonance imaging (fMRI) has revealed a core recollection network centred on posterior parietal and medial temporal lobe (MTL) regions (Hayama, Vilberg, & Rugg, 2012; Johnson, Suzuki, & Rugg, 2013; King, de Chastelaine, Elward, Wang, & Rugg, 2015; Rugg, Johnson, & Uncapher, 2015; Rugg & Vilberg, 2013; Thakral, Benoit, & Schacter, 2017). However, due to the relatively poor time resolution of fMRI, the temporal dynamics of these regions during retrieval remain largely unknown. In order to overcome these modality-specific limitations, we here used Magnetoencephalography (MEG) in a verbal episodic memory paradigm assessing correct rejection (CR) of lures, item recognition (IR) of old words and associative recall (AR) of paired target words. We found that power decreases in the alpha frequency band (10-12 Hz) systematically track different mnemonic outcomes in both time and space: Over left posterior sensors, alpha power decreased in a stepwise fashion from 500 ms onward, first from CR to IR and then from IR to AR. When projecting alpha power into source space, the core recollection network known from fMRI studies emerged, including posterior parietal cortex (PPC) and hippocampus. While PPC showed a linear change across conditions, hippocampal effects were specific to recall. Critically, the hippocampal recall effect emerged [~]200 ms before the PPC recall effect, suggesting a bottom-up recall signal from hippocampus to PPC. Our data thus link engagement of the core recollection network to the temporal dynamics of episodic memory and suggest that alpha rhythms constitute a fundamental oscillatory mechanism revealing when, where and how our memories are retrieved.\n\nHighlightsO_LIAlpha rhythms distinguish between different retrieval outcomes\nC_LIO_LIAlpha power time courses track item recognition and associative recall\nC_LIO_LISource alpha power decreases track the fMRI core recollection network\nC_LIO_LIHippocampal recall signal precedes parietal signal\nC_LI

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bioRxiv2018

Hippocampal synchrony and neocortical desynchrony cooperate to encode and retrieve episodic memories

Episodic memories hinge upon our ability to process a wide range of multisensory information and bind this information into a coherent, memorable representation. On a neural level, these two processes are thought to be supported by neocortical alpha/beta desynchronisation and hippocampal theta/gamma synchronisation, respectively. Intuitively, these two processes should couple to successfully create and retrieve episodic memories, yet this hypothesis has not been tested empirically. We address this by analysing human intracranial EEG data recorded during two associative memory tasks. We find that neocortical alpha/beta (8-20Hz) power decreases reliably precede and predict hippocampal \"fast\" gamma (60-80Hz) power increases during episodic memory formation; during episodic memory retrieval however, hippocampal \"slow\" gamma (40-50Hz) power increases reliably precede and predict later neocortical alpha/beta power decreases. We speculate that this coupling reflects the flow of information from neocortex to hippocampus during memory formation, and hippocampal pattern completion inducing information reinstatement in the neocortex during memory retrieval.\n\nSignificance StatementEpisodic memories detail our personally-experienced past. The formation and retrieval of these memories has long been thought to be supported by a division of labour between the neocortex and the hippocampus, where the former processes event-related information and the latter binds this information together. However, it remains unclear how the two regions interact. We uncover directional coupling between these regions, with power decreases in the neocortex that precede and predict power increases in the hippocampus during memory formation. Fascinatingly, this process reverses during memory retrieval, with hippocampal power increases preceding and predicting neocortical power decreases. These results suggest a bidirectional flow of information between the neocortex and hippocampus is fundamental to the formation and retrieval of episodic memories.

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bioRxiv2017

Data-driven re-referencing of intracranial EEG based on independent component analysis (ICA)

Intracranial recordings from patients implanted with depth electrodes are a valuable source of information in cognitive neuroscience. They allow for the unique opportunity to record brain activity with a high spatial and temporal resolution. To extract the local signal of interest in stereotactic EEG (S-EEG) data, a common pre-processing choice is to re-reference the data with a bipolar montage.\n\nWith bipolar reference, each channel is subtracted from its neighbour in order to reduce commonalities between channels and isolate activity that is spatially confined. We here challenge the assumption that bipolar reference can effectively perform this task. We argue that in order to extract local activity, the distribution of the signal source of interest, as well as the distribution of interfering distant signals and noise sources need to be considered. Those can have a variable spatial extent and are modulated by electrode spacing, location and anatomical characteristics. Those factors are not accounted for by a fixed referencing scheme and bipolar reference can therefore not only decrease the signal to noise ratio (SNR) of the data, but also lead to mislocalization of activity and consequently to misinterpretation of results.\n\nWe promote the perspective of regarding referencing as a spatial filtering operation with fixed coefficients. As an alternative, we propose to use Independent Component Analysis (ICA), to derive filter coefficients that reflect the statistical dependencies of the data at hand. We argue that ICA performs the same task that bipolar referencing pursues, namely undoing the linear superposition of activity and can therefore be used to identify activity that is local. We first describe and demonstrate this procedure on human S-EEG recordings. In a simulation with real data, we then quantitatively show that ICA outperforms the bipolar referencing operation in sensitivity and importantly in specificity when it comes to revealing local time series from the superposition of neighbouring channels.

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bioRxiv2017

Theta Phase Synchronization Between The Human Hippocampus And The Prefrontal Cortex Supports Learning Of Unexpected Information

Events that violate predictions are thought to not only modulate activity within the hippocampus and prefrontal cortex, but also to enhance communication between the two regions. Several studies in rodents have shown that synchronized theta oscillations facilitate communication between the prefrontal cortex and hippocampus during salient events, but it remains unclear whether similar oscillatory mechanisms support interactions between the two regions in humans. Here, we had the rare opportunity to conduct simultaneous electrophysiological recordings from the human hippocampus and prefrontal cortex from two patients undergoing presurgical evaluation for pharmaco-resistant epilepsy. Recordings were conducted during a task that involved encoding of contextually expected and unexpected visual stimuli. Across both patients, hippocampal-prefrontal theta phase synchronization was significantly higher during encoding of unexpected study items, compared to contextually expected study items. In contrast, we did not find increased theta synchronization between the prefrontal cortex and rhinal cortex. Our findings are consistent with the idea that theta oscillations orchestrate communication between the hippocampus and prefrontal cortex during the processing of contextually salient information.

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