scholarly journals Odor-evoked category reactivation in human ventromedial prefrontal cortex during sleep promotes memory consolidation

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Laura K Shanahan ◽  
Eva Gjorgieva ◽  
Ken A Paller ◽  
Thorsten Kahnt ◽  
Jay A Gottfried

Slow-wave sleep is an optimal opportunity for memory consolidation: when encoding occurs in the presence of a sensory cue, delivery of that cue during sleep enhances retrieval of associated memories. Recent studies suggest that cues might promote consolidation by inducing neural reinstatement of cue-associated content during sleep, but direct evidence for such mechanisms is scant, and the relevant brain areas supporting these processes are poorly understood. Here, we address these gaps by combining a novel olfactory cueing paradigm with an object-location memory task and simultaneous EEG-fMRI recording in human subjects. Using pattern analysis of fMRI ensemble activity, we find that presentation of odor cues during sleep promotes reactivation of category-level information in ventromedial prefrontal cortex that significantly correlates with post-sleep memory performance. In identifying the potential mechanisms by which odor cues selectively modulate memory in the sleeping brain, these findings bring unique insights into elucidating how and what we remember.

2019 ◽  
Author(s):  
Matthias Grieder ◽  
Yosuke Morishima ◽  
Stephanie Winkelbeiner ◽  
Sarah M Mueller ◽  
Kristoffer Feher ◽  
...  

Background: Sleep is crucial for sound memory functioning in humans. In particular, the slow waves that occur predominantly during slow wave sleep (SWS) are associated with hippocampus-dependent declarative memory consolidation. Making use of this association, boosting SWS to improve memory performance would be appealing for both healthy and memory-impaired populations. Transcranial direct current stimulation (tDCS) is a non-invasive brain stimulation that modulates the brain’s excitability and has shown promising results in improving memory performance. However, owing to differing stimulation protocols and contradictory findings, there is insufficient evidence for the efficacy of tDCS-modulated hippocampal excitability on SWS and sleep-dependent memory consolidation.Hypotheses: We aimed to enhance sleep-dependent memory consolidation and augment slow wave amplitudes.Methods: We applied bi-temporal anodal tDCS to the left and right lateral temporal lobes of 31 healthy participants in a double-blind, sham-controlled, randomized crossover study. State-dependent tDCS was administered during slow wave sleep only. A pair-associate episodic memory task was used to assess sleep-dependent memory consolidation with face-occupation stimuli with baseline retrieval before sleep and delayed retrieval after sleep.Results: Sleep-dependent memory consolidation was increased by tDCS only in participants who showed above-average performance (i.e. high performers) in baseline memory retrieval. Moreover, tDCS increased the slow wave amplitudes compared to sham.Conclusions: When targeting a specialized brain mechanism such as memory consolidation with tDCS during slow wave sleep, only those who were high performers at baseline achieved a memory boost.


2019 ◽  
Author(s):  
Becky Crowley ◽  
Amir-Homayoun Javadi

Consistent with the context-dependent memory literature, previous research suggests that when the same frequency of neural oscillations is reinstated between memory encoding and retrieval, engram reactivation is facilitated, and thus declarative memory recall is enhanced. Importantly, engram reactivation is also fundamental for the redistribution process that underlies sleep-dependent memory consolidation. Therefore, the current study investigated whether reinstating frequency-specific oscillatory activity between encoding and sleep would facilitate the engram reactivation implicated in sleep-dependent memory consolidation, and thus enhance post-sleep declarative memory performance. Transcranial alternating current stimulation (tACS) was administered to the left dorsolateral prefrontal cortex (DLPFC) of human participants during a declarative memory task. Participants received 60 Hz of stimulation during encoding, and 60 Hz, 90 Hz, or sham stimulation during post-learning slow-wave sleep (SWS) or rapid eye-movement (REM) sleep. In immediate and delayed free recall sessions, declarative memory performance was significantly enhanced if participants had received the same frequency of stimulation during encoding and SWS compared to any other stimulation condition. This finding supports a novel theoretical proposal, which assumes that an intrinsic neurobiological mechanism for coordinating frequency-specific oscillatory activity, during SWS, underlies sleep-dependent declarative memory consolidation.


2021 ◽  
Vol 11 (4) ◽  
pp. 410
Author(s):  
Simon Ruch ◽  
Kristoffer Fehér ◽  
Stephanie Homan ◽  
Yosuke Morishima ◽  
Sarah Maria Mueller ◽  
...  

Slow-wave sleep (SWS) has been shown to promote long-term consolidation of episodic memories in hippocampo–neocortical networks. Previous research has aimed to modulate cortical sleep slow-waves and spindles to facilitate episodic memory consolidation. Here, we instead aimed to modulate hippocampal activity during slow-wave sleep using transcranial direct current stimulation in 18 healthy humans. A pair-associate episodic memory task was used to evaluate sleep-dependent memory consolidation with face–occupation stimuli. Pre- and post-nap retrieval was assessed as a measure of memory performance. Anodal stimulation with 2 mA was applied bilaterally over the lateral temporal cortex, motivated by its particularly extensive connections to the hippocampus. The participants slept in a magnetic resonance (MR)-simulator during the recordings to test the feasibility for a future MR-study. We used a sham-controlled, double-blind, counterbalanced randomized, within-subject crossover design. We show that stimulation vs. sham significantly increased slow-wave density and the temporal coupling of fast spindles and slow-waves. While retention of episodic memories across sleep was not affected across the entire sample of participants, it was impaired in participants with below-average pre-sleep memory performance. Hence, bi-temporal anodal direct current stimulation applied during sleep enhanced sleep parameters that are typically involved in memory consolidation, but it failed to improve memory consolidation and even tended to impair consolidation in poor learners. These findings suggest that artificially enhancing memory-related sleep parameters to improve memory consolidation can actually backfire in those participants who are in most need of memory improvement.


2000 ◽  
Vol 12 (2) ◽  
pp. 267-280 ◽  
Author(s):  
Tetsuya Iidaka ◽  
Nicole D. Anderson ◽  
Shitij Kapur ◽  
Roberto Cabez ◽  
Fergus I. M. Craik

The effects of divided attention (DA) on episodic memory encoding and retrieval were investigated in 12 normal young subjects by positron emission tomography (PET). Cerebral blood flow was measured while subjects were concurrently performing a memory task (encoding and retrieval of visually presented word pairs) and an auditory tone-discrimination task. The PET data were analyzed using multivariate Partial Least Squares (PLS), and the results revealed three sets of neural correlates related to specific task contrasts. Brain activity, relatively greater under conditions of full attention (FA) than DA, was identified in the occipital-temporal, medial, and ventral-frontal areas, whereas areas showing relatively more activity under DA than FA were found in the cerebellum, temporo-parietal, left anterior-cingulate gyrus, and bilateral dorsolateral-prefrontal areas. Regions more active during encoding than during retrieval were located in the hippocampus, temporal and the prefrontal cortex of the left hemisphere, and regions more active during retrieval than during encoding included areas in the medial and right-prefrontal cortex, basal ganglia, thalamus, and cuneus. DA at encoding was associated with specific decreases in rCBF in the left-prefrontal areas, whereas DA at retrieval was associated with decreased rCBF in a relatively small region in the right-prefrontal cortex. These different patterns of activity are related to the behavioral results, which showed a substantial decrease in memory performance when the DA task was performed at encoding, but no change in memory levels when the DA task was performed at retrieval.


SLEEP ◽  
2020 ◽  
Vol 43 (Supplement_1) ◽  
pp. A34-A34
Author(s):  
E M Wernette ◽  
K M Fenn

Abstract Introduction Slow wave sleep (SWS) strengthens declarative memory for information studied for a later test. However, research on the effect of sleep on information that is not intentionally remembered is scare. Previous research from our lab suggests sleep consolidates some, but not all, information that has been encoded incidentally, meaning that it has been acted on but not intentionally remembered. It remains unclear what determines which information benefits from sleep-dependent consolidation processes and what aspects of sleep are related to these mnemonic benefits. In two experiments, we test the hypothesis that sleep consolidates strong but not weak memory traces following incidental encoding, and assess the relationship between memory performance and objective sleep characteristics. Methods In Experiment 1, participants rated words one (weak traces) or three times (strong traces) in a deep or shallow incidental encoding task. Participants either rated words on a scale from ‘concrete’ to ‘abstract’ (deep) or counted the vowels in the words (shallow). Following a 12-hour period containing sleep or wakefulness, participants took a surprise memory test. In Experiment 2, participants rated words one or three times in the deep encoding task, received an 8-hour sleep opportunity with polysomnography, and took the surprise memory test. Results In Experiment 1, participants remembered words better after sleep than wake regardless of whether words were encoded one or three times, but only after deep encoding. Sleep did not consolidate information following shallow encoding. Experiment 2 is ongoing, but we predict that the amount of SWS will correlate positively with memory. Conclusion Results thus far suggest sleep may have consolidated information based on the strength of memory traces. Because deep encoding results in stronger memory traces than shallow encoding, this work is broadly consistent with theories of memory consolidation that predict sleep is more beneficial for strong memory traces than weak, such as the synaptic downscaling hypothesis. Support N/A


2017 ◽  
Author(s):  
Mohsen Naji ◽  
Giri P. Krishnan ◽  
Elizabeth A McDevitt ◽  
Maxim Bazhenov ◽  
Sara C. Mednick

AbstractWhile anatomical pathways between forebrain cognitive and brainstem autonomic nervous centers are well defined, autonomic–central interactions during sleep and their contribution to waking performance are not understood. Here, we analyzed simultaneous central activity via electroencephalography (EEG) and autonomic heart beat-to-beat intervals (RR intervals) from electrocardiography (ECG) during wake and daytime sleep. We identified bursts of ECG activity that lasted 4-5 seconds and predominated in non-rapid-eye-movement sleep (NREM). Using event-based analysis of NREM sleep, we found an increase in delta (0.5-4Hz) and sigma (12-15Hz) power and an elevated density of slow oscillations (0.5-1Hz) about 5 secs prior to peak of the heart rate burst, as well as a surge in vagal activity, assessed by high-frequency (HF) component of RR intervals. Using regression framework, we show that these Autonomic/Central Events (ACE) positively predicted post-nap improvement in a declarative memory task after controlling for the effects of spindles and slow oscillations from sleep periods without ACE. No such relation was found between memory performance and a control nap. Additionally, NREM ACE negatively correlated with REM sleep and learning in a non-declarative memory task. These results provide the first evidence that coordinated autonomic and central events play a significant role in declarative memory consolidation.


2020 ◽  
Vol 375 (1799) ◽  
pp. 20190227 ◽  
Author(s):  
Masami Tatsuno ◽  
Soroush Malek ◽  
LeAnna Kalvi ◽  
Adrian Ponce-Alvarez ◽  
Karim Ali ◽  
...  

Interaction between hippocampal sharp-wave ripples (SWRs) and UP states, possibly by coordinated reactivation of memory traces, is conjectured to play an important role in memory consolidation. Recently, it was reported that SWRs were differentiated into multiple subtypes. However, whether cortical UP states can also be classified into subtypes is not known. Here, we analysed neural ensemble activity from the medial prefrontal cortex from rats trained to run a spatial sequence-memory task. Application of the hidden Markov model (HMM) with three states to epochs of UP–DOWN oscillations identified DOWN states and two subtypes of UP state (UP-1 and UP-2). The two UP subtypes were distinguished by differences in duration, with UP-1 having a longer duration than UP-2, as well as differences in the speed of population vector (PV) decorrelation, with UP-1 decorrelating more slowly than UP-2. Reactivation of recent memory sequences predominantly occurred in UP-2. Short-duration reactivating UP states were dominated by UP-2 whereas long-duration ones exhibit transitions from UP-1 to UP-2. Thus, recent memory reactivation, if it occurred within long-duration UP states, typically was preceded by a period of slow PV evolution not related to recent experience, and which we speculate may be related to previously encoded information. If that is the case, then the transition from UP-1 to UP-2 subtypes may help gradual integration of recent experience with pre-existing cortical memories by interleaving the two in the same UP state. This article is part of the Theo Murphy meeting issue ‘Memory reactivation: replaying events past, present and future'.


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