Biology subjects

Staresina, B. P.

Publications and source records attributed to Staresina, B. P..

At least 19 recordsLinked to original sources

bioRxiv2026

The human hippocampus retroactively binds experiences across time

Creating memories requires linking events across seconds and minutes, but canonical mechanisms of associative plasticity operate over much shorter timescales. This poses a fundamental problem: how can the brain bind information that arrives at different times? Computational model and animal studies implicate the hippocampus in associating events across time, but when the hippocampus becomes engaged and how it interacts with representations of preceding events are unknown. Here we show, using intracranial recordings in humans forming image-word associations across a ~2-s temporal gap, that hippocampal high-frequency activity predicts later memory when the second event arrives, but not during the initial image or intervening delay. At this moment, neurons tuned to the preceding image reinstate stimulus-specific firing despite its sensory absence. Across trials, hippocampal high-frequency activity was selectively coupled to this reinstatement during successful encoding and increased before spiking of image-tuned neurons. These findings reveal a retroactive mode of hippocampal binding, whereby representations of preceding events are recruited when new information arrives. This mechanism provides a neural solution for binding experiences across the temporal discontinuities that characterize everyday life.

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bioRxiv2026

Sleep ripples drive single-neuron reactivation for human memory consolidation

Sleep transforms fragile experiences into lasting memories, but the neuronal basis of this process in humans has remained elusive. In rodents, hippocampal ripples orchestrate the replay of place cell sequences, establishing a cellular mechanism for consolidation - though with limited generalizability to human memory. In humans, neuroimaging has revealed large-scale offline reactivation, but these coarse signals leave open whether individual neurons are reactivated and how ripples might mediate this process. Here, we bridge this gap by directly recording 1,466 medial temporal lobe (MTL) neurons and intracranial electroencephalography during learning, post-learning wakefulness, and sleep. We show that ripples robustly drive neuronal firing, with sleep ripples eliciting stronger activation than wake ripples. Critically, neurons tuned to items that were later remembered fired more strongly during ripples than those coding for forgotten items, and this memory-linked reactivation was selectively observed during sleep. Finally, ripple-associated neuronal MTL bursts were detectable across widespread cortical activity, pointing to a mechanism for systems-level consolidation. Together, these findings provide the first direct evidence that ripple-driven single-neuron reactivation supports human episodic memory consolidation and reveal why sleep -- compared to wakefulness -- offers a privileged window for stabilizing memories.

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bioRxiv2025

Sleep strengthens successor representations of learned sequences

Experiences reshape our internal representations of the world. However, the neural and cognitive dynamics of this process are largely unknown. Here, we investigated how sequence learning reorganizes neural representations and how sleep-dependent consolidation contributes to this transformation. Using high-density electroencephalography and multivariate decoding, we found that learning temporal sequences of visual information led to the incorporation of successor representations during a subsequent perceptual task, despite temporal information being task-irrelevant. Importantly, individuals with better sequence memory performance exhibited stronger successor incorporation during the perceptual task. Representational similarity analyses comparing neural patterns with different layers of a deep neural network revealed a learning-induced shift in representational format, from low-level visual features to higher-level abstract properties. Critically, both the strength and transformation of successor representations correlated with the proportion of slow-wave sleep during a post-learning nap. These findings support the idea that sequence learning induces lasting changes in visual representational geometry and that sleep strengthens these changes, providing mechanistic insights into how the brain updates internal models after exposure to environmental regularities.

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bioRxiv2025

Respiration shapes the neural dynamics of successful remembering in humans.

Respiration has been shown to impact memory retrieval, yet the neural dynamics underlying this effect remain unclear. Here, we investigated how respiration shapes both behavioral and neural expressions of memory retrieval by re-analyzing an existing dataset where scalp electroencephalography and respiration recordings were acquired while participants (N = 18) performed an episodic memory task. Our results unveil that respiration influences retrieval-related power fluctuations in the /{beta} band and concomitant memory reactivation. Specifically, we found that both key neural signatures of successful remembering were co-modulated during exhalation, with the strength of the interaction between respiration and reactivation processes being associated with memory performance. Together, these findings suggest that respiration may act as a scaffold for episodic memory retrieval in humans by coordinating the neural conditions that support effective remembering. Significance statementRecent evidence suggests that respiration may shape neural dynamics underlying various cognitive processes. In this study, we identify respiration as a potential pacemaker for memory retrieval by showing that key neural signatures of effective remembering--namely, decreases in /{beta} power and the reactivation of previously encoded neural representations--are tightly synchronized with the respiratory cycle. Notably, the strength of this respiration-brain coupling is associated with individual memory performance, underscoring the critical role and functional significance of brain-body interactions in supporting cognitive functions.

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bioRxiv2025

Slow wave sleep supports the reorganisation of episodic memory networks

Models of memory consolidation propose that newly acquired memory traces undergo reorganisation during sleep. To test this idea, we recorded high-density electroencephalography (EEG) during an evening session of word-image learning followed by immediate (pre-sleep) and delayed (post-sleep) recall. Polysomnography was employed throughout the intervening night, capturing time spent in different sleep stages. Using source-reconstructed time-frequency analysis, we first replicated the effect of alpha power decreases for successful relative to unsuccessful recall, emerging between 700 and 1500 ms after cue onset and spanning medial and lateral temporal lobe regions as well as posterior parietal cortex. Directly contrasting successful post-sleep vs. pre-sleep recall revealed a shift of alpha power decrease from parietal towards anterior temporal lobe (ATL) after sleep. Critically, time spent in slow wave sleep (SWS) during the intervening night not only predicted the extent of memory retention, but also correlated with the shift to ATL recall effects. Finally, brain-wide functional connectivity profiles during successful recall pointed to a marked overnight reorganisation of memory networks, with the extent of reorganisation again predicted by time spent in SWS. Together, these findings link SWS to the consolidation and functional reorganisation of episodic memory networks.

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bioRxiv2025

Human sleep spindles track experimentally excited brain circuits

Spindles are hallmark oscillations during non-rapid-eye-movement (NREM) sleep. Together with slow oscillations (SOs), they are thought to play a mechanistic role in the consolidation of learned information. The quantity and spatial distribution of spindles has been linked to brain activity during learning before sleep and to memory performance after sleep. If spindles are drawn to cortical areas excited through pre-sleep learning tasks, this begs the question whether the spatial distribution of spindles is flexible, and whether their regional expression can also be manipulated with experimental brain stimulation. We used excitatory transcranial direct current stimulation (tDCS) to stimulate the left and right motor cortex in a repeated-measures experimental design. After stimulation, we recorded high-density electroencephalography (EEG) during sleep to test how local stimulation modulated the regional expression of sleep spindles. Indeed, we show that excitatory tDCS of local cortical sites before sleep biases the expression of spindles to the excited locations during subsequent sleep. No effects of localised tDCS excitation were seen for SOs. These results demonstrate that the spatial topography of sleep spindles is neither hard-wired nor random, with spindles being flexibly directed to exogenously excited cortical circuits. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=108 SRC="FIGDIR/small/631687v2_ufig1.gif" ALT="Figure 1"> View larger version (21K): org.highwire.dtl.DTLVardef@fb33c1org.highwire.dtl.DTLVardef@2f291org.highwire.dtl.DTLVardef@1831f08org.highwire.dtl.DTLVardef@16a7f6a_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical AbstractC_FLOATNO C_FIG Statement of SignificanceSpindles are signatures of NREM sleep linked to memory consolidation, intelligence, and neurological disorders. Recent work shows the spatial distribution of spindles mirrors cortical activation patterns during learning. If spindles are preferentially expressed at cortical sites engaged during prior waking, the question arises whether spindles can be directed by inducing excitation exogenously with non-invasive brain stimulation. Here, we applied anodal-tDCS to either left or right motor areas before a nap. Indeed, we found that spindle (and not SO) rates are greater at cortical sites excited by tDCS. This result suggests the spatial distribution of spindles is flexible and is sensitive to experimental excitatory stimulation. This has implications for targeted rehabilitation of specific cortical areas and for developing sleep-based brain-computer interfaces.

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bioRxiv2023

Respiration shapes sleep-oscillations and memory reactivation in humans.

The beneficial effect of sleep on memory consolidation relies on the precise interplay of slow oscillations (SOs) and spindles. However, whether these rhythms are orchestrated by an underlying pacemaker has remained elusive. Here, we tested whether respiration, which has been shown to impact brain rhythms and cognition during wake, shapes memory reactivation by modulating sleep-related oscillations and their interplay in humans. We recorded scalp EEG and respiration throughout an experiment in which participants acquired associative memories before taking a nap. Our results reveal that respiration strongly modulates the emergence of sleep oscillations. Specifically, SOs, spindles as well as their interplay (i.e., coupled SO_spindle complexes) systematically increase towards inhalation peaks. Moreover, the strength of respiration-SO_spindle coupling is linked to the extent of memory reactivation during SO_spindles. Our results identify respiration as a potential pacemaker for memory consolidation in humans and highlight the critical role of brain-body interactions during sleep.

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bioRxiv2022

Ripple-locked coactivity of stimulus-specific neurons supports human associative memory

Associative memory is the ability to encode and retrieve relations between different stimuli. To better understand its neural basis, we investigated whether associative memory involves precisely timed spiking of neurons in the medial temporal lobes that exhibit stimulus-specific tuning. Using single-neuron recordings from epilepsy patients performing an associative object-location memory task, we identified the object- and place-specific neurons that encoded the separate elements of each memory. When patients encoded and retrieved particular memories, the relevant object- and place-specific neurons activated synchronously during hippocampal ripples. This ripple-locked coactivity of stimulus-specific neurons emerged over time as the patients associative learning progressed. Our results suggest a cellular account of associative memory, in which hippocampal ripples coordinate the activity of specialized cellular populations to facilitate links between stimuli.

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bioRxiv2021

Sleep spindles track cortical learning patterns for memory consolidation

Memory consolidation, the transformation of labile memory traces into stable long-term representations, is facilitated by post-learning sleep. Computational and biophysical models suggest that sleep spindles may play a key mechanistic role for consolidation, igniting structural changes at cortical sites involved in prior learning. Here we tested the resulting prediction that spindles are most pronounced over learning-related cortical areas and that the extent of this learning-spindle overlap predicts behavioural measures of memory consolidation. Using high-density scalp Electroencephalography (EEG) and Polysomnography (PSG) in healthy volunteers, we first identified cortical areas engaged during a temporospatial associative memory task (power decreases in the alpha/beta frequency range, 6-20 Hz). Critically, we found that participant-specific topographies (i.e., spatial distributions) of post-learning sleep spindle amplitude correlated with participant-specific learning topographies. Importantly, the extent to which spindles tracked learning patterns further predicted memory consolidation across participants. Our results provide empirical evidence for a role of post-learning sleep spindles in tracking learning networks, thereby facilitating memory consolidation.

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bioRxiv2021

Hippocampal neurons code individual memory episodes in humans

The hippocampus is an essential hub for episodic memory processing. However, how human hippocampal single neurons code multi-element associations remains unknown. Some argue that each hippocampal neuron codes for an invariant element within an episode. Instead, others have proposed that hippocampal neurons bind together all elements present in a discrete episodic memory. Here, we provide evidence for the latter. We show that individual neurons, which we term Episode Specific Neurons (ESNs), code discrete episodic memories using either a rate code or a temporal firing code. We find evidence for these neurons exclusively in the hippocampus. Importantly, these ESNs do not reflect the coding of a particular element in the episode (i.e., concept or time). Instead, they code for the conjunction of the different elements that make up the episode. One-Sentence SummaryIndividual neurons in the hippocampus code for discrete episodic memories.

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bioRxiv2021

Stress diminishes outcome but enhances response representations during instrumental learning

Stress may shift behavioural control from a goal-directed system that encodes action-outcome relationships to a habit system that learns stimulus-response associations. Although this shift to habits is highly relevant for stress-related psychopathologies, limitations of existing behavioural paradigms hindered previous research to answer the fundamental question of whether the stress-induced bias to habits is due to impaired goal-directed or enhanced habitual processing (or both). Here, we leveraged EEG-based multivariate pattern analysis to decode neural outcome representations, crucial for goal-directed control, and response representations, essential for habitual responding, during instrumental learning. We show that stress reduces outcome representations but enhances response representations, both of which were directly associated with a behavioural index of habitual responding. Further, changes in outcome and response representations were uncorrelated, suggesting that these may reflect distinct processes. Our findings indicate that habit behaviour under stress is the result of both enhanced habitual and diminished goal-directed processing.

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bioRxiv2020

Endogenous memory reactivation during sleep in humans is clocked by slow oscillation-spindle complexes.

Sleep is thought to support memory consolidation via reactivation of prior experiences, with particular electrophysiological sleep signatures (slow oscillations (SOs) and sleep spindles) gating the information flow between relevant brain areas. However, empirical evidence for a role of endogenous memory reactivation (i.e., without experimentally delivered memory cues) for consolidation in humans is lacking. Here, we devised a paradigm in which participants acquired associative memories before taking a nap. Multivariate decoding was then used to capture endogenous memory reactivation during non-rapid eye movement (NREM) sleep in surface EEG recordings. Our results reveal reactivation of learning material during SO-spindle complexes, with the precision of SO-spindle coupling predicting reactivation strength. Critically, reactivation strength (i.e. classifier evidence in favor of the previously studied stimulus category) in turn predicts the level of consolidation across participants. These results elucidate the memory function of sleep in humans and emphasize the importance of SOs and spindles in clocking endogenous consolidation processes.

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bioRxiv2020

Auditory beat stimulation modulates memory-related single-neuron activity in the human medial temporal lobe

Auditory beats are composed of two sine waves using nearby frequencies, which can either be applied as a superposed signal to both ears or to each ear separately. In the first case, the beat sensation results from hearing an amplitude-modulated signal (monaural beat). In the second case, it is generated by phase-sensitive neurons in the brain stem (binaural beat). We investigated the effects of monaural and binaural 5 Hz beat stimulation on neural activity and memory performance in neurosurgical patients performing an associative recognition task. Previously, we had reported that these beat stimulation conditions modulated memory performance in opposite directions. Here, we analyzed data from a patient subgroup, in which microwires were implanted in the amygdala, hippocampus, entorhinal cortex and parahippocampal cortex. We identified neurons responding with firing rate changes to binaural versus monaural 5 Hz beat stimulation. In these neurons, we correlated the differences in firing rates for binaural versus monaural beats to the memory-related differences for remembered versus forgotten items and associations. In the left hemisphere for these neurons, we detected statistically significant negative correlations between firing rate differences for binaural versus monaural beats and remembered versus forgotten items/associations. Importantly, such negative correlations were also observed between beat stimulation-related firing rate differences in the baseline window and memory-related firing rate differences in the poststimulus windows. In line with concepts of homeostatic plasticity, we interpret our findings as indicating that beat stimulation is linked to memory performance via shifting baseline firing levels.

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bioRxiv2020

The hippocampus as the switchboard between perception and memory

Adaptive memory recall requires a rapid and flexible switch from external perceptual reminders to internal mnemonic representations. However, owing to the limited temporal or spatial resolution of brain imaging modalities used in isolation, the hippocampal-cortical dynamics supporting this process remain unknown. We thus employed an object-scene cued recall paradigm across two studies, including intracranial Electroencephalography (iEEG) and high-density scalp EEG. First, a sustained increase in hippocampal high gamma power (60-110 Hz) emerged 500 ms after cue onset and distinguished successful vs. unsuccessful recall. This increase in gamma power for successful recall was followed by a decrease in hippocampal alpha power (8-12 Hz). Intriguingly, the hippocampal gamma power increase marked the moment at which extrahippocampal activation patterns shifted from perceptual cue towards mnemonic target representations. In parallel, source-localised EEG alpha power revealed that the recall signal progresses from hippocampus to posterior parietal cortex and then to medial prefrontal cortex. Together, these results identify the hippocampus as the switchboard between perception and memory and elucidate the ensuing hippocampal-cortical dynamics supporting the recall process. SignificanceHow do we adaptively switch from perceiving the external world to retrieving goal-relevant internal memories? To tackle this question, we used - in a cued-recall paradigm - direct intracranial recordings from the human hippocampus complemented by high-density scalp Electroencephalography (EEG). We found that a hippocampal signal ~500 ms after a perceptual cue marks the conversion from external (perceptual) to internal (mnemonic) representations. This sets in motion a recall cascade involving posterior parietal and medial prefrontal cortex, revealed via source-localised and time-resolved EEG alpha power. Together, these results unveil the hippocampal-cortical dynamics supporting rapid and flexible memory recall.

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bioRxiv2020

A neural code of egocentric spatial information in human medial temporal lobe

Spatial navigation relies on neural systems that encode information about places, distances, and directions in relation to the external world or relative to the navigating organism. Since the proposal of cognitive maps, the neuroscience of navigation has focused on allocentric (world-referenced) neural representations including place, grid, and head-direction cells. Here, using single-neuron recordings during virtual navigation, we identify "anchor cells" in the human brain as a neural code for egocentric (self-centered) spatial maps: Anchor cells represent egocentric directions towards "anchor points" located in the environmental center or periphery. Anchor cells were abundant in parahippocampal cortex, supported full vectorial representations of egocentric space, and were integrated into a neural memory network. Neurons encoding allocentric direction complemented anchor-cell activity, potentially assisting anchor cells in transforming percepts into allocentric representations. Anchor cells may facilitate egocentric navigation strategies, may support route planning from egocentric viewpoints, and may underlie the first-person perspective in episodic memories.

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bioRxiv2019

Content tuning in the medial temporal lobe cortex: Voxels that perceive, retrieve

How do we recall vivid details from our past based only on sparse cues? Research suggests that the phenomenological reinstatement of past experiences is accompanied by neural reinstatement of the original percept. This process critically depends on the medial temporal lobe (MTL). Within the MTL, perirhinal cortex (PRC) and parahippocampal cortex (PHC) are thought to support encoding and recall of objects and scenes, respectively, with the hippocampus (HC) serving as a content-independent hub. If the fidelity of recall indeed arises from neural reinstatement of perceptual activity, then successful recall should preferentially draw upon those neural populations within content-sensitive MTL cortex that are tuned to the same content during perception. We tested this hypothesis by having eighteen human participants undergo functional magnetic resonance imaging (fMRI) while they encoded and recalled objects and scenes paired with words. Critically, recall was cued with the words only. While HC distinguished successful from unsuccessful recall of both objects and scenes, PRC and PHC were preferentially engaged during successful vs. unsuccessful object and scene recall, respectively. Importantly, within PRC and PHC, this content-sensitive recall was predicted by content tuning during perception: Across PRC voxels, we observed a positive linear relationship between object tuning during perception and successful object recall, while across PHC voxels, we observed a positive linear relationship between scene tuning during perception and successful scene recall. Our results thus highlight content-based roles of MTL cortical regions for episodic memory and reveal a direct mapping between content-specific tuning during perception and successful recall.

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bioRxiv2019

Heterogeneous profiles of coupled sleep oscillations in human hippocampus

Cross-frequency coupling of sleep oscillations is thought to mediate memory consolidation. While the hippocampus is deemed central to this process, detailed knowledge of which oscillatory rhythms interact in the sleeping human hippocampus is lacking. Combining intracranial hippocampal and non-invasive electroencephalography from twelve neurosurgical patients, we characterized spectral power and coupling during non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. Hippocampal coupling was extensive, with the majority of channels expressing spectral interactions. NREM consistently showed delta-ripple coupling, but ripples were also modulated by slow oscillations (SOs) and sleep spindles. SO-delta and SO-theta coupling, as well as interactions between delta/theta and spindle/beta frequencies also occurred. During REM, limited interactions between delta/theta and beta frequencies emerged. Moreover, oscillatory organization differed substantially between i) hippocampus and scalp, ii) sites along the anterior-posterior hippocampal axis, and iii) individuals. Overall, these results extend and refine our understanding of hippocampal sleep oscillations.

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bioRxiv2018

Speed of time-compressed forward replay flexibly changes in human episodic memory

Remembering information from continuous past episodes is a complex task. On the one hand, we must be able to recall events in a highly accurate way that often includes exact timing; on the other hand, we can ignore irrelevant details and skip to events of interest. We here track continuous episodes, consisting of different sub-events, as they are recalled from memory. In behavioral and MEG data, we show that memory replay is temporally compressed and proceeds in a forward direction. Neural replay is characterized by the reinstatement of temporal patterns from encoding. These fragments of activity reappear on a compressed timescale. Herein, the replay of sub-events takes longer than the transition from one sub-event to another. This identifies episodic memory replay as a dynamic process in which participants replay fragments of fine-grained temporal patterns and are able to skip flexibly across sub-events.

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