Retrieval dynamics in episodic memory – from computations to representations

Understanding how our experiences are retrieved from long-term memory is fundamental in cognitive neuroscience. In this doctoral thesis I explore two essential questions regarding the temporal dynamics of episodic memory retrieval. First, I investigate how rapidly distinct components of a visual object representation (i.e., perceptual and conceptual aspects) are reactivated during retrieval, and how this temporal sequence evolves compared to visual encoding. Findings from a series of behavioural, scalp electroencephalography (EEG) and intracranial EEG experiments, using reaction times and time- resolved decoding analyses, suggest that retrieval is a hierarchical, multi- layered process that follows the reverse order compared to encoding, prioritizing semantic information over perceptual details. Second, I explore whether memories are reactivated following a specific oscillatory rhythm. Computational models, based on studies in rodents, suggest that encoding and retrieval processes occur at opposing phases of hippocampal theta oscillations. Evidence for such phase modulation in humans is still sparse. The present findings suggest that in humans, neural signatures of memory retrieval fluctuate with, and are time-locked to, the phase of theta oscillations. Altogether, this doctoral thesis supports the view that retrieval is an oscillatory process and the elements that form our memories are retrieved following a biased and sequential order

An optimal oscillatory phase for pattern reactivation during memory retrieval

Computational models and in vivo studies in rodents suggest that the hippocampal system oscillates between states that are optimal for encoding and states that are optimal for retrieval. Here, we show that in humans, neural signatures of memory reactivation are modulated by the phase of a theta oscillation. Electroencephalography (EEG) was recorded while participants were cued to recall previously learned word-object associations, and time-resolved pattern classifiers were trained to detect neural reactivation of the target objects. Classifier fidelity rhythmically fluctuated at 7 or 8 Hz and was modulated by theta phase across the entire recall period. The phase of optimal classification was shifted approximately 180° between encoding and retrieval. Inspired by animal work, we then computed “classifier-locked averages” to analyze how ongoing theta oscillations behaved around the time points at which the classifier indicated memory retrieval. We found strong theta (7 or 8 Hz) phase consistency approximately 300 ms before the time points of maximal neural memory reactivation. Our findings provide important evidence that the neural signatures of memory retrieval fluctuate and are time locked to the phase of an ongoing theta oscillation

Evidence that neural information flow is reversed between object perception and object reconstruction from memory

Little is known about how the reconstruction of a memory unfolds in time in the human brain. Here, the authors provide evidence that the process of reconstructing the memory of an object involves a reversal of the information flow involved in the actual perception of that object

EEG and fMRI evidence for 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 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. Participants 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 increased activation for AM compared to non-AM in the brain networks underlying 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 AM reactivation in empathy

Theta rhythmicity governs human behavior and hippocampal signals during memory-dependent tasks.

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 and recall of cue-object associative memories. We find 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). 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 significantly more for remembered than forgotten trials, providing a potential mechanistic underpinning for the theta oscillations found in behavioral responses

Theta rhythmicity governs human behavior and hippocampal signals during memory-dependent tasks.

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 and recall of cue-object associative memories. We find 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). 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 significantly more for remembered than forgotten trials, providing a potential mechanistic underpinning for the theta oscillations found in behavioral responses