Neural mechanisms of reactivation-induced updating that enhance and distort memory

We remember a considerable number of personal experiences because we are frequently reminded of them, a process known as memory reactivation. Although memory reactivation helps to stabilize and update memories, reactivation may also introduce distortions if novel information becomes incorporated with memory. Here we used functional magnetic resonance imaging (fMRI) to investigate the neural mechanisms mediating reactivation-induced updating in memory for events experienced during a museum tour. During scanning, participants were shown target photographs to reactivate memories from the museum tour followed by a novel lure photograph from an alternate tour. Later, participants were presented with target and lure photographs and asked to determine whether the photographs showed a stop they visited during the tour. We used a subsequent memory analysis to examine neural recruitment during reactivation that was associated with later true and false memories. We predicted that the quality of reactivation, as determined by online ratings of subjective recollection, would increase subsequent true memories but also facilitate incorporation of the lure photograph, thereby increasing subsequent false memories. The fMRI results revealed that the quality of reactivation modulated subsequent true and false memories via recruitment of left posterior parahippocampal, bilateral retrosplenial, and bilateral posterior inferior parietal cortices. However, the timing of neural recruitment and the way in which memories were reactivated contributed to differences in whether memory reactivation led to distortions or not. These data reveal the neural mechanisms recruited during memory reactivation that modify how memories will be subsequently retrieved, supporting the flexible and dynamic aspects of memory

Episodic memory reconsolidation and strengthening

Episodic memories are not always accurate, subject to false recollection due to the process of memory reconsolidation (Loftus, 2005). Memory reactivation places memory to a labile state and can lead to two phenomena: memory updating/reconsolidation with possibility of having inaccurate memories (Hupbach et al. 2007) and memory strengthening. By replicating Hupbach et al. (2007, 2008) study, Study 1 aimed to investigate the impact of music upon memory reconsolidation whereas Study 2 explored whether exposure to original learning context is sufficient to trigger reconsolidation. Study 1 found out that reconsolidation process may not be as reliable as suggested in existing reconsolidation studies. Study 2 discovered dissociation between updating of list memory and resistance to the memory-weakening effect of interference, suggesting reactivation-induced reconsolidation can maintain or even strengthen memories. Study 3 tested directly the capacity of memory reactivation to facilitate memory strengthening. An idea of implementing 6 hours interval in between Day 2 sessions was suggested, aimed to determine whether or not the learning effect is mediated by reconsolidation processes. The common effects of retrieval-relearning, relearning-retrieval, relearning-relearning, retrieval-6 hours-relearning, relearning-6 hours-retrieval to strengthen episodic memory may reflect different underlying processes, one or more of which might be related to memory reconsolidation

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

Are latent working memory items retrieved from long-term memory?

Switching one’s focus of attention between to-be-remembered items in working memory (WM) is critical for cognition, but the mechanisms by which this is accomplished are unclear. A long-term memory (LTM) account suggests that switching attention away from an item, and passively retaining and reactivating such “latent” items back into the focus of attention involves episodic LTM retrieval processes, even for delays of only a few seconds. We tested this hypothesis using a two-item, double-retrocue WM task that requires participants to switch attention away from and reactivate items followed by subsequent LTM tests for reactivated items from the initial WM task (vs. continuously retained or untested control items). We compared performance on these tests between older adults (a population with LTM deficits) and young adults with either full (Experiment 1) or divided (Experiment 2) attention during the WM delay periods. The effects of reactivating latent items, as well as ageing and divided attention, had significant effects on WM performance, but did not interact with or systematically affect subsequent LTM for reactivated versus control items on item-, location-, or associative-recognition memory judgements made with either high or low confidence. Experiment 3 confirmed that these effects did not depend on whether or not young participants were warned about the subsequent LTM tests before performing the WM task. These dissociations between WM and LTM are inconsistent with the LTM account of latent WM; they are more consistent with the dynamic processing model of WM (Current Directions in Psychological Science)

Neural oscillations and a nascent corticohippocampal theory of reference

The ability to use words to refer to the world is vital to the communicative power of human language. In particular, the anaphoric use of words to refer to previously mentioned concepts (antecedents) allows dialogue to be coherent and meaningful. Psycholinguistic theory posits that anaphor comprehension involves reactivating a memory representation of the antecedent. Whereas this implies the involvement of recognition memory, or the mnemonic sub-routines by which people distinguish old from new, the neural processes for reference resolution are largely unknown. Here, we report time-frequency analysis of four EEG experiments to reveal the increased coupling of functional neural systems associated with referentially coherent expressions compared to referentially problematic expressions. Despite varying in modality, language, and type of referential expression, all experiments showed larger gamma-band power for referentially coherent expressions compared to referentially problematic expressions. Beamformer analysis in high-density Experiment 4 localised the gamma-band increase to posterior parietal cortex around 400-600 ms after anaphor-onset and to frontaltemporal cortex around 500-1000 ms. We argue that the observed gamma-band power increases reflect successful referential binding and resolution, which links incoming information to antecedents through an interaction between the brain’s recognition memory networks and frontal-temporal language network. We integrate these findings with previous results from patient and neuroimaging studies, and we outline a nascent cortico-hippocampal theory of reference

Episodic memory retrieval functionally relies on very rapid reactivation of sensory information

Episodic memory retrieval is assumed to rely on the rapid reactivation of sensory information that was present during encoding, a process termed “ecphory.” We investigated the functional relevance of this scarcely understood process in two experiments in human participants. We presented stimuli to the left or right of fixation at encoding, followed by an episodic memory test with centrally presented retrieval cues. This allowed us to track the reactivation of lateralized sensory memory traces during retrieval. Successful episodic retrieval led to a very early (∼100–200 ms) reactivation of lateralized alpha/beta (10–25 Hz) electroencephalographic (EEG) power decreases in the visual cortex contralateral to the visual field at encoding. Applying rhythmic transcranial magnetic stimulation to interfere with early retrieval processing in the visual cortex led to decreased episodic memory performance specifically for items encoded in the visual field contralateral to the site of stimulation. These results demonstrate, for the first time, that episodic memory functionally relies on very rapid reactivation of sensory information

Virtual enactment effect on memory in young and aged populations: a systematic review

Background: Spatial cognition is a critical aspect of episodic memory, as it provides the scaffold for events and enables successful retrieval. Virtual enactment (sensorimotor and cognitive interaction) by means of input devices within virtual environments provides an excellent opportunity to enhance encoding and to support memory retrieval with useful traces in the brain compared to passive observation. Methods: We conducted a systematic review with Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines concerning the virtual enactment effect on spatial and episodic memory in young and aged populations. We aim at giving guidelines for virtual enactment studies, especially in the context of aging, where spatial and episodic memory decline. Results: Our findings reveal a positive effect on spatial and episodic memory in the young population and promising outcomes in aging. Several cognitive factors (e.g., executive function, decision-making, and visual components) mediate memory performances. Findings should be taken into account for future interventions in aging. Conclusions: The present review sheds light on the key role of the sensorimotor and cognitive systems for memory rehabilitation by means of a more ecological tool such as virtual reality and stresses the importance of the body for cognition, endorsing the view of an embodied mind

Reconsolidation of appetitive memory and sleep: functional connectomics and plasticity

Introduzione: La dipendenza da cibo \ue8 un disturbo comportamentale caratterizzato da modelli maladattativi di consumo alimentare, in cui alimenti ricchi in zuccheri, sale e/o grassi possono indurre una dipendenza tale da essere paragonata ai disturbi relativi all\u2019abuso di sostanze. Alla base di questo processo vi \ue8 l\u2019associazione tra questi cibi altamente palatabili e la sensazione piacevole e rinforzante indotta dal loro consumo, che pu\uf2 essere codificata in una nuova memoria maladattativa sottostante il disturbo di dipendenza. Infatti, le nuove informazioni che riceviamo quotidianamente dall\u2019esterno vengono processate dal nostro cervello tramite un primo stadio di codifica e un secondo stadio di consolidamento, durante il quale vengono stabilizzate in una nuova memoria e integrate nella rete cerebrale di conoscenze preesistenti. Tuttavia, dopo il suo consolidamento, una memoria pu\uf2 essere destabilizzata e riportata ad uno stato di labilit\ue0 che ne permette la modifica e l\u2019eventuale integrazione con nuove informazioni. Infine, un nuovo processo di stabilizzazione chiamato riconsolidamento \ue8 necessario affinch\ue9 la traccia mnemonica aggiornata sia nuovamente stabilizzata. Da recenti studi, \ue8 noto come il sonno sia rilevante sia per il consolidamento che per il riconsolidamento della memoria. Tuttavia, mentre \ue8 chiaro come il consolidamento che avviene durante il sonno permetta la stabilizzazione a lungo termine delle tracce mnemoniche, non \ue8 ancora stato del tutto chiarito il ruolo del sonno nel processo di riconsolidamento. Scopo: Date queste premesse, e nota l\u2019importanza dell\u2019interazione tra amigdala basolaterale (BLA) e ippocampo nel riconsolidamento delle memorie appetitive, gli obiettivi della presente tesi erano: i) valutare come l\u2019amigdala BLA e ippocampo interagiscono in termini di potenziali locali durante la riattivazione della memoria strumentale effettuata o durante la fase di attivit\ue0 o durante la fase di inattivit\ue0 del ciclo circadiano dei roditori; ii) valutare come il richiamo della memoria effettuato durante la fase attiva o quella inattiva possa influenzare il successivo processo di riconsolidamento, e iii) trovare, in-vivo, un marker di riattivazione della memoria appetitiva. Metodi: Sono stati utilizzati 32 ratti maschi, ceppo Sprague Dawley, a cui sono stati impiantati due elettrodi profondi: uno in BLA e uno in ippocampo, per la registrazione dei potenziali locali. I ratti sono stati sottoposti ad un protocollo comportamentale in gabbia operante di auto-somministrazione di saccarosio, composto da quattro stadi: addestramento (i), in cui i ratti imparavano l\u2019associazione tra la pressione di una leva e l\u2019emissione di un pellet di saccarosio; astinenza (ii), durante la quale i soggetti non venivano esposti al contesto di addestramento; riattivazione o non riattivazione (iii) della memoria strumentale in gabbia operante, svolta o durante la fase di attivit\ue0, o durante la fase di inattivit\ue0; test di ricaduta (iv). I potenziali locali sono stati analizzati per lo stadio (iii) in modo da ottenere la potenza delle oscillazioni theta e gamma per i due elettrodi profondi; tali frequenze sono state scelte in quanto rilevanti per i processi mnemonici. Infatti, il richiamo della memoria \ue8 correlato alla sincronizzazione delle onde theta (4-12 Hz) tra BLA e altre aree cerebrali quali l\u2019area CA1 dell\u2019ippocampo, ed \ue8 inoltre correlato alle basse gamma (30-60 Hz) nell\u2019ippocampo. Infine, l\u2019accoppiamento tra le onde theta e gamma nell\u2019ippocampo \ue8 un noto metodo di comunicazione tra sotto-aree ippocampali nel corso dei processi di memoria. Risultati: I risultati hanno mostrato la presenza di una correlazione inversa tra la potenza delle basse gamma nell\u2019area CA1 ippocampale e il tasso di risposta durante lo stadio di richiamo della memoria nella fase di attivit\ue0, indipendentemente dal fatto che i soggetti stessero o meno premendo la leva. Le basse gamma potrebbero quindi rappresentare un marker di correlazione per il richiamo della memoria appetitiva. Inoltre, la potenza di basse e alte gamma ippocampali aumenta durante le epoche di pressione di leva quando il richiamo della memoria viene effettuato nella fase di inattivit\ue0, suggerendo che le onde gamma potrebbero essere dei marker correlazionali specifici per la componente strumentale del richiamo della memoria effettuato durante la fase di inattivit\ue0. Conclusioni e limitazioni: Per concludere, i risultati hanno mostrato l\u2019importanza delle frequenze basse gamma nel richiamo delle memorie appetitive, tuttavia non hanno mostrato alcuna differenza a livello delle onde theta, n\ue9 a livello della BLA. Di conseguenza, si conclude che il protocollo utilizzato nella presente tesi non ha mostrato una sensibilit\ue0 sufficientemente elevata nell\u2019evidenziare i cambiamenti ipotizzati a livello dei potenziali locali. Lo svolgimento di ulteriori esperimenti che andranno a determinare misure di connettomica quali coerenza e accoppiamento, sia intra- che inter- area, aiuter\ue0 a determinare se e come le due aree comunicano tra di loro.Introduction: Food addiction is a behavioural disorder in which individuals develop maladaptive patterns of food consumption. Particularly, food containing processed sugars, salt, fat etc. can be addictive, and refined food consumption behaviours may meet the criteria for substance use disorders. For these characteristics, food addiction can also be considered a memory disorder. Memories in the brain are processed as follows: new information is encoded and then long-term consolidated through a process allowing its integration into already existing knowledge networks. After a memory has been consolidated, it can be destabilized and brought back to a labile state, requiring a new re-stabilization process called reconsolidation. Memory consolidation is known to require sleep. In fact, sleep allows new memory traces to long-term stabilize. Sleep also seems to influence memory reconsolidation; however, its involvement in this process is not yet clear. Aim: Given these premises, the goals of the project were: to evaluate how basolateral amygdala (BLA) and hippocampus interact in terms of local field potentials (LFPs) when appetitive instrumental memory is retrieved either during active or inactive phase of rats circadian rhythm; to evaluate how retrieving the memory in the activity vs inactivity phase influences following memory reconsolidation; and to find an in vivo electrophysiological marker of appetitive memory retrieval. In fact, it has been shown that BLA and dorsal hippocampus interaction is crucial for appetitive memory reconsolidation. Methods: Thirty-two male Sprague Dawley rats were implanted with in-depth electrodes for LFPs recordings in BLA and dorsal hippocampal CA1 and subject to a behavioural protocol apt to induce appetitive memory retrieval. The behavioural procedure consisted of four stages: training (i), in which animals learned lever pressing \u2013 sucrose reward association; abstinence (ii), during which subjects were not exposed to the training context; memory retrieval or no retrieval (iii): instrumental memory reactivation or no reactivation, performed either during active or inactive phase; and relapse test (iv), during which sucrose-seeking behaviour was analysed. Theta and gamma oscillations powers were analysed during stage (iii). In fact, they are known to be involved in memory processes. Memory retrieval has been shown to correlate with theta (4-12 Hz) synchronization between BLA and other brain areas (such as hippocampal CA1) and with low gamma (30-60 Hz) in hippocampus. Particularly, theta-gamma cross-frequency coupling has been shown to be used as a mean of communication between hippocampal sub-areas during memory processing. Results: Results showed an inverse correlation between hippocampal CA1 low gamma power and reactivation rate of responding (either when rats were lever pressing or not) when reactivation was performed during the active phase. This suggests that low gamma may be a correlational marker of instrumental sucrose memory retrieval, independent of whether rats were lever-pressing or not. Moreover, hippocampal CA1 gamma bands increased when lever pressing during instrumental memory reactivation while in the inactive phase, suggesting that both low and high gamma bands may be correlational markers to actual instrumental responding retrieval during the inactive phase. Conclusions and limitations: In conclusion, results showed that low gamma is relevant in sucrose appetitive memory retrieval. However, no difference was observed in the theta frequency band, nor at the level of BLA. Therefore, the current protocol did not have the sensitivity to detect predicted changes in LFPs. Further experiments would help investigating if and how the two areas interact, by determining connectomics measures such as coherence and coupling within and between areas