Tobias Staudigl

Episodic memory formation is not a passive process but emerges from sequences of actions through which we engage with our environment. Yet, how these action sequences interact with the neural dynamics underlying human memory formation and retrieval remains poorly understood. Here, we investigated whether coordinated gaze shifts, one of the major exploratory actions in humans, structure the reactivation of memories. Participants learned multiple action sequences by pairing images with distinct real-world gaze shifts while we simultaneously recorded EEG and motion tracking data. During subsequent retrieval, the recalled gaze sequences acted as a direct behavioral readout of memory performance. Representational similarity analyses revealed that the reactivation of image memories was precisely timed to recalled gaze shifts within each sequence. Crucially, only correctly executed, but not incorrectly executed gaze shifts elicited significant reactivation of the corresponding image class, directly linking neural reactivation to retrieval success. These findings suggest that exploratory actions are fundamental components of episodic memories, not incidental accompaniments: self-initiated movements can serve as temporal anchors of memory reactivation that predict retrieval success. By investigating memory through natural behavior, our work provides an ecologically grounded perspective on human cognition, revealing that species-typical actions such as gaze shifts are essential to, rather than obstacles for, understanding memory’s neural basis.

Hippocampal ripples are considered a key mechanism of sleep-dependent memory consolidation. In humans, however, their direct investigation has relied on invasive recordings from patients with epilepsy, because EEG provides limited access to fast activity from deep medial temporal structures. Here, we tested whether source-resolved magnetoencephalography can reveal physiologically meaningful ripple-like activity during NREM sleep in healthy humans. These events showed hallmarks expected of sleep ripples: they were most prominent in medial temporal regions and embedded within slow oscillation (SO)–spindle dynamics, occurring preferentially during SO up-states and spindle centers. To test mnemonic relevance, we combined sleep MEG with targeted memory reactivation, in which learning cues were replayed during sleep. TMR improved memory performance, and later remembered cues preferentially recruited medial temporal ripple-like events alongside cortical spindles. Ripple-like events also coincided with enhanced item-specific reactivation during successful TMR. Together, these findings establish MEG as a non-invasive window onto hippocampo-cortical memory dynamics during sleep.

Natural states of consciousness are thought to be regulated by deep brain structures such as the thalamus. However, very little is known about the underlying electrophysiology in humans. Here, using a rare opportunity to directly record from the human thalamus, we identify a hitherto-unreported brain-state-specific oscillation of approximately 19-45 Hz. This oscillation is present only during rapid eye movement (REM) sleep and wakefulness, while being absent during non-REM sleep. The 19-45 Hz oscillation further distinguishes REM sleep microstates, co-occurring with bursts of eye movements, and is specific to the central thalamus, a structure implicated in causing global brain state transitions. The discovery of a distinct oscillatory signature in the central thalamus that distinguishes conscious states opens up avenues to further investigate thalamic contributions to states of consciousness in humans and potentially to refine interventions to treat disorders of consciousness.

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 reanalyzing an existing dataset where scalp electroencephalography and respiration recordings were acquired while participants ( N = 18, 15 females) performed an episodic memory task. Our results unveil that respiration influences retrieval-related power fluctuations in the α/β band and concomitant memory reactivation. Specifically, we found that both key neural signatures of successful remembering were comodulated 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.

Eye movements, such as saccades, allow us to gather information about the environment and, in this way, can shape memory. In non-human primates, saccades are associated with the activity of grid cells in the entorhinal cortex. Grid cells are essential for spatial navigation, but whether saccade-based grid-like signals play a role in human memory formation is currently unclear. Here, human participants undergo functional magnetic resonance imaging and continuous eye gaze monitoring while studying scene images. Recognition memory is probed immediately thereafter. Results reveal saccade-based grid-like codes in the left entorhinal cortex that are specific to later remembered trials during study, a finding that we replicate with an independent data set. The grid-related effects are time-locked to activation increases in the frontal eye fields. Unexpectedly, lower saccade-based grid-like codes are associated with better subsequent recognition memory performance. Our findings suggest an entorhinal map of visual space that is timed with neural activity in oculomotor regions, and negatively associated with subsequent memory. Grid-like codes, entorhinal cortex, saccades, frontal eye fields (FEF), memory, functional magnetic resonance imaging (fMRI)

Neural activity and eye movements are two well-established predictors of memory performance in humans. Successful memory formation is typically associated with reduced alpha/beta power (i.e., the alpha/beta subsequent memory effect) and an increased number of eye movements. However, the functional relevance of these two memory correlates has primarily been investigated in isolation, leaving their coupling and combined contribution to memory formation largely unknown. Here, we address this gap through four experiments involving simultaneous eye-tracking and scalp or intracranial electroencephalography recordings while participants viewed scenes either freely or under varying levels of visual constraint. Across experiments and cohorts, we identified the degree of visual exploration, rather than subsequent memory performance, as the consistent and robust modulator of alpha/beta power reductions. Going beyond correlations, manipulating eye movements dissociated alpha/beta power reductions from memory. Combined with the finding that saccade parameters predicted the dynamics of alpha/beta activity, our results directly link alpha/beta activity to the oculomotor system. Moreover, we show that the accumulation of saccades over time accounted for the reduced alpha/beta power, resembling the pattern typically observed after stimulus onset. Our work demonstrates that neglecting eye movements results in an incomplete understanding of the alpha/beta subsequent memory effect. Together, the evidence points at alpha/beta activity directly reflecting eye movements, and only indirectly, memory formation. The current study thus bridges two lines of previous research and advocates for new perspectives on the specific interpretation of the alpha/beta subsequent memory effect and on the function of alpha/beta activity in general.

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 ⍺/β 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.

Natural states of consciousness are thought to be regulated by deep brain structures such as the thalamus. However, very little is known about the underlying electrophysiology in humans. Here, using a rare opportunity to directly record from the human thalamus, we identify a hitherto-unreported brain-state-specific oscillation of approximately 19-45 Hz. This oscillation is present only during Rapid Eye Movement (REM) sleep and wakefulness, while being absent during Non-REM sleep. The 19-45 oscillation further distinguishes REM sleep microstates, co-occurring with bursts of eye movements, and is specific to the Central Thalamus, a structure implicated in causing global brain state transitions. The discovery of a distinct oscillatory signature in the Central Thalamus that distinguishes conscious states opens up avenues to further investigate thalamic contributions to states of consciousness in humans and potentially to refine interventions to treat disorders of consciousness.

Memory consolidation relies in part on the reactivation of previous experiences during sleep. The precise interplay of sleep-related oscillations (slow oscillations, spindles and ripples) is thought to coordinate the information flow between relevant brain areas, with ripples mediating memory reactivation. However, in humans empirical evidence for a role of ripples in memory reactivation is lacking. Here, we investigated the relevance of sleep oscillations and specifically ripples for memory reactivation during human sleep using targeted memory reactivation. Intracranial electrophysiology in epilepsy patients and scalp EEG in healthy participants revealed that elevated levels of slow oscillation - spindle activity coincided with the read-out of experimentally induced memory reactivation. Importantly, spindle-locked ripples recorded intracranially from the medial temporal lobe were found to be correlated with the identification of memory reactivation during non-rapid eye movement sleep. Our findings establish ripples as key-oscillation for sleep-related memory reactivation in humans and emphasize the importance of the coordinated interplay of the cardinal sleep oscillations.

Information about heading direction is critical for navigation as it provides the means to orient ourselves in space. However, given that veridical head-direction signals require physical rotation of the head and most human neuroimaging experiments depend upon fixing the head in position, little is known about how the human brain is tuned to such heading signals. Here we adress this by asking 52 healthy participants undergoing simultaneous electroencephalography and motion tracking recordings (split into two experiments) and 10 patients undergoing simultaneous intracranial electroencephalography and motion tracking recordings to complete a series of orientation tasks in which they made physical head rotations to target positions. We then used a series of forward encoding models and linear mixed-effects models to isolate electrophysiological activity that was specifically tuned to heading direction. We identified a robust posterior central signature that predicts changes in veridical head orientation after regressing out confounds including sensory input and muscular activity. Both source localization and intracranial analysis implicated the medial temporal lobe as the origin of this effect. Subsequent analyses disentangled head-direction signatures from signals relating to head rotation and those reflecting location-specific effects. Lastly, when directly comparing head direction and eye-gaze-related tuning, we found that the brain maintains both codes while actively navigating, with stronger tuning to head direction in the medial temporal lobe. Together, these results reveal a taxonomy of population-level head-direction signals within the human brain that is reminiscent of those reported in the single units of rodents.