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

Shanahan, Laura K.; Gjorgieva, Eva; Paller, Ken A.; Kahnt, Thorsten; Gottfried, Jay A.

doi:10.7554/elife.39681

Cited by 63 publications

(67 citation statements)

References 49 publications

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“…That is, it is unclear how the dominant trisynaptic circuit within the hippocampus could exhibit patterns of activity that could support item-specific reinstatement as measured by fMRI. Further, previous findings are mixed [29], with some fMRI studies failing to find evidence for item- [4,5] or category-level [30] reinstatement within the hippocampus and other studies finding evidence for item-level [31] or category-level [32] reinstatement. We used left and right hippocampus as ROIs for the same reinstatement analysis described above, and found no evidence of significant reinstatement for either control-stimulation (p's > 0.063) or HNT-stimulation sessions (p's > 0.183), and no difference in reinstatement between stimulation sessions (p's > 0.110).…”

Section: Effects Of Stimulation On Reinstatementmentioning

confidence: 99%

Enhanced reinstatement of naturalistic event memories due to hippocampal-network-targeted stimulation

Hebscher¹,

Kragel²,

Kahnt³

et al. 2020

Preprint

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Episodic memory involves the reinstatement of distributed patterns of brain activity present when events were initially experienced. The hippocampus is thought to coordinate reinstatement via its interactions with a network of brain regions, but this hypothesis has not been causally tested in humans. The current study directly tested the involvement of the hippocampal network in reinstatement using network-targeted noninvasive stimulation. We measured reinstatement of multi-voxel patterns of fMRI activity during encoding and retrieval of naturalistic video clips depicting everyday activities. Reinstatement of video-specific activity patterns was robust in posterior-parietal and occipital areas previously implicated in event reinstatement. Theta-burst stimulation targeting the hippocampal network increased video-specific reinstatement of fMRI activity patterns in occipital cortex and improved memory accuracy relative to stimulation of a control out-of-network location. Furthermore, stimulation targeting the hippocampal network influenced the trial-by-trial relationship between hippocampal activity during encoding and later reinstatement in occipital cortex. These findings implicate the hippocampal network in the reinstatement of spatially distributed patterns of event-specific activity, and identify a role for the hippocampus in encoding complex naturalistic events that later undergo cortical reinstatement.

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Section: Effects Of Stimulation On Reinstatementmentioning

confidence: 99%

Enhanced reinstatement of naturalistic event memories due to hippocampal-network-targeted stimulation

Hebscher¹,

Kragel²,

Kahnt³

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

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“…Additionally, they found that the presence of sleep spindles, brief (0.5-3 s) bursts of 11-16 Hz oscillatory brain activity during NREM sleep that frequently correlate with memory retention (Antony and Paller, 2017) overlapped with time intervals when this decoding was possible. Similarly, Shanahan et al (2018) showed decoding of TMR-evoked category information using fMRI. Finally, multivariate features from EEG activity after TMR cues could be used to successfully decode different parts of a procedural memory sequence (Belal et al, 2018).…”

Section: Introductionmentioning

confidence: 97%

Targeted Memory Reactivation during Sleep Elicits Neural Signals Related to Learning Content

et al. 2019

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Retrieval of learning-related neural activity patterns is thought to drive memory stabilization. However, finding reliable, noninvasive, content-specific indicators of memory retrieval remains a central challenge. Here, we attempted to decode the content of retrieved memories in the EEG during sleep. During encoding, male and female human subjects learned to associate spatial locations of visual objects with left-or right-hand movements, and each object was accompanied by an inherently related sound. During subsequent slow-wave sleep within an afternoon nap, we presented half of the sound cues that were associated (during wake) with left-and right-hand movements before bringing subjects back for a final postnap test. We trained a classifier on sleep EEG data (focusing on lateralized EEG features that discriminated left-vs right-sided trials during wake) to predict learning content when we cued the memories during sleep. Discrimination performance was significantly above chance and predicted subsequent memory, supporting the idea that retrieval leads to memory stabilization. Moreover, these lateralized signals increased with postcue sleep spindle power, demonstrating that retrieval has a strong relationship with spindles. These results show that lateralized activity related to individual memories can be decoded from sleep EEG, providing an effective indicator of offline retrieval.

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“…This can be achieved by presenting sounds or smells that were previously linked to items learned in wake during subsequent sleep. TMR has been shown to trigger memory reactivation (Belal et al, 2018; Schreiner et al, 2018; Shanahan et al, 2018) and to influence memory performance after sleep, for example by improving episodic (Rasch et al, 2007; Rudoy et al, 2009; Cellini and Cappuzo, 2018) and procedural skill consolidation (Antony et al, 2012; Schönauer et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Targeted memory reactivation of a serial reaction time task in SWS, but not REM, preferentially benefits the non-dominant hand

Acm

Mea

Belal

et al. 2020

Preprint

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Targeted memory reactivation (TMR) is a technique by which sounds paired with learned information can be used to cue neural reactivation of that information during sleep. While TMR in slow-wave sleep (SWS) has been shown to strengthen procedural memories, it is unclear whether TMR in rapid eye movement (REM) sleep, a state strongly associated with motor consolidation, provides equivalent benefit. Furthermore, it is unclear whether this technique influences dominant and non-dominant hands equally. We applied TMR of a two-handed serial reaction time task (SRTT) during either SWS or REM in thirty-two human right handed adults (sixteen female) to examine the impact of stimulation in each sleep stage on right (dominant) and left hands. While TMR in SWS led to strong benefits in reaction times and sequence-specific skill, equivalent cueing in REM led to no benefit at all, suggesting that reactivation in this sleep stage is not important for the SRTT. Event-related potentials elicited by TMR cues for left and right hand movements differed significantly in REM, but not SWS, showing that these cues are at least processed in REM. Interestingly, TMR benefits were apparent only in the non-dominant hand, potentially due to the weaker performance measured in this hand at the outset. Overall, these findings suggest that memory replay in SWS, but not REM, is important for consolidation of the SRTT, and TMR-cued consolidation is stronger in the non-dominant hand.Significance statementTargeted memory reactivation (TMR) in sleep leads to memory consolidation, but many aspects of this process remain to be understood. We used TMR of a bimanual serial reaction time task to show that behavioural benefit is only observed after stimulation in SWS, even though electrophysiology shows that the TMR cues are processed in REM. Importantly, TMR selectively benefitted the non-dominant hand. These findings suggest that TMR in REM does not benefit this serial reaction time task, and that TMR in SWS preferentially consolidates weaker memory traces relating to the non-dominant hand.

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

Cited by 63 publications

References 49 publications

Enhanced reinstatement of naturalistic event memories due to hippocampal-network-targeted stimulation

Enhanced reinstatement of naturalistic event memories due to hippocampal-network-targeted stimulation

Targeted Memory Reactivation during Sleep Elicits Neural Signals Related to Learning Content

Targeted memory reactivation of a serial reaction time task in SWS, but not REM, preferentially benefits the non-dominant hand

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