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No effect of odor-induced memory reactivation during REM sleep on declarative memory stability.

Cordi MJ, Diekelmann S, Born J, Rasch B - Front Syst Neurosci (2014)

Bottom Line: In humans, experimentally inducing hippocampal memory reactivations during slow-wave sleep (but not during wakefulness) benefits consolidation and immediately stabilizes declarative memories against future interference.We show that odor-induced memory reactivation during REM sleep does not stabilize memories against future interference.We propose that the beneficial effect of reactivation during sleep on memory stability might be critically linked to processes characterizing SWS including, e.g., slow oscillatory activity, sleep spindles, or low cholinergic tone, which are required for a successful redistribution of memories from medial temporal lobe regions to neocortical long-term stores.

View Article: PubMed Central - PubMed

Affiliation: Division of Biopsychology, Institute of Psychology, University of Zurich Zurich, Switzerland.

ABSTRACT
Memory reactivations in hippocampal brain areas are critically involved in memory consolidation processes during sleep. In particular, specific firing patterns of hippocampal place cells observed during learning are replayed during subsequent sleep and rest in rodents. In humans, experimentally inducing hippocampal memory reactivations during slow-wave sleep (but not during wakefulness) benefits consolidation and immediately stabilizes declarative memories against future interference. Importantly, spontaneous hippocampal replay activity can also be observed during rapid eye movement (REM) sleep and some authors have suggested that replay during REM sleep is related to processes of memory consolidation. However, the functional role of reactivations during REM sleep for memory stability is still unclear. Here, we reactivated memories during REM sleep and examined its consequences for the stability of declarative memories. After 3 h of early, slow-wave sleep (SWS) rich sleep, 16 healthy young adults learned a 2-D object location task in the presence of a contextual odor. During subsequent REM sleep, participants were either re-exposed to the odor or to an odorless vehicle, in a counterbalanced within subject design. Reactivation was followed by an interference learning task to probe memory stability after awakening. We show that odor-induced memory reactivation during REM sleep does not stabilize memories against future interference. We propose that the beneficial effect of reactivation during sleep on memory stability might be critically linked to processes characterizing SWS including, e.g., slow oscillatory activity, sleep spindles, or low cholinergic tone, which are required for a successful redistribution of memories from medial temporal lobe regions to neocortical long-term stores.

No MeSH data available.


Experimental procedure. (A) Subjects slept for approximately 3 h before learning a 2-D object-location task while being exposed to an odor. During subsequent REM sleep, either the same odor or an odorless vehicle was presented for at least 20 min, in a counterbalanced order. After awakening, subjects learned an interfering 2-D object-location task without odor presentation. Retrieval of the original task was tested thereafter. (B) Reactivation in Diekelmann et al.'s study (2011), in contrast, occurred either during SWS or wakefulness.
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Figure 1: Experimental procedure. (A) Subjects slept for approximately 3 h before learning a 2-D object-location task while being exposed to an odor. During subsequent REM sleep, either the same odor or an odorless vehicle was presented for at least 20 min, in a counterbalanced order. After awakening, subjects learned an interfering 2-D object-location task without odor presentation. Retrieval of the original task was tested thereafter. (B) Reactivation in Diekelmann et al.'s study (2011), in contrast, occurred either during SWS or wakefulness.

Mentions: Subjects spent one adaptation night and two experimental sessions in the sleep laboratory. They were fully informed about the session flow. The experimental sessions were separated by at least 7 days. The sessions started at 9:00 p.m. with the attachment of electrodes for electroencephalographic (EEG), electromyographic (EMG) and electrooculographic (EOG) recordings. After filling out standard questionnaires and performing a reaction time test, subjects were allowed to sleep for at least 3 h from 10:30 p.m. on (see Figure 1). Fifteen minutes after awakening, at about 2:00 a.m., participants first performed a reaction time task and an odor detection test to ensure functionality of the olfactometer. Participants then learned the 2-D object-location task in the presence of the odor before they performed the odor detection test and the reaction time task again. Thereafter, participants returned to bed and olfactory stimulation (using a repeated 30-s on/30-s off pattern) was started as soon as polysomnographic recordings indicated stable REM sleep. We stimulated during tonic and phasic REM sleep phases. On one night, participants were re-exposed to the same odor that had been present during prior learning to induce memory reactivation. On the other night, an odorless vehicle stimulus was applied, in a counterbalanced order. Neither the subject nor the experimenter knew about the order of the stimulation. Stimulation was stopped as soon as arousals, awakenings or shifts into other sleep stages were detected. On average, stimulation duration during sleep was 29.77 ± 1.86 min (range 18–45.5 min) following Diekelmann et al.'s (2011) protocol. Post-experimental offline scoring confirmed that 92.55 ± 1.89% of odor stimulation and 92.29 ± 2.98% of placebo stimulation actually took place during REM sleep. Participants were awakened directly after the last reactivation in the REM sleep phase. Shortly after awakening, participants learned the interference 2-D object-location task. After a break of 20 min, recall of the card-pair locations of the original task, learned before sleep, was tested. Participants were asked to perform as well as possible in each of the memory tasks.


No effect of odor-induced memory reactivation during REM sleep on declarative memory stability.

Cordi MJ, Diekelmann S, Born J, Rasch B - Front Syst Neurosci (2014)

Experimental procedure. (A) Subjects slept for approximately 3 h before learning a 2-D object-location task while being exposed to an odor. During subsequent REM sleep, either the same odor or an odorless vehicle was presented for at least 20 min, in a counterbalanced order. After awakening, subjects learned an interfering 2-D object-location task without odor presentation. Retrieval of the original task was tested thereafter. (B) Reactivation in Diekelmann et al.'s study (2011), in contrast, occurred either during SWS or wakefulness.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4150443&req=5

Figure 1: Experimental procedure. (A) Subjects slept for approximately 3 h before learning a 2-D object-location task while being exposed to an odor. During subsequent REM sleep, either the same odor or an odorless vehicle was presented for at least 20 min, in a counterbalanced order. After awakening, subjects learned an interfering 2-D object-location task without odor presentation. Retrieval of the original task was tested thereafter. (B) Reactivation in Diekelmann et al.'s study (2011), in contrast, occurred either during SWS or wakefulness.
Mentions: Subjects spent one adaptation night and two experimental sessions in the sleep laboratory. They were fully informed about the session flow. The experimental sessions were separated by at least 7 days. The sessions started at 9:00 p.m. with the attachment of electrodes for electroencephalographic (EEG), electromyographic (EMG) and electrooculographic (EOG) recordings. After filling out standard questionnaires and performing a reaction time test, subjects were allowed to sleep for at least 3 h from 10:30 p.m. on (see Figure 1). Fifteen minutes after awakening, at about 2:00 a.m., participants first performed a reaction time task and an odor detection test to ensure functionality of the olfactometer. Participants then learned the 2-D object-location task in the presence of the odor before they performed the odor detection test and the reaction time task again. Thereafter, participants returned to bed and olfactory stimulation (using a repeated 30-s on/30-s off pattern) was started as soon as polysomnographic recordings indicated stable REM sleep. We stimulated during tonic and phasic REM sleep phases. On one night, participants were re-exposed to the same odor that had been present during prior learning to induce memory reactivation. On the other night, an odorless vehicle stimulus was applied, in a counterbalanced order. Neither the subject nor the experimenter knew about the order of the stimulation. Stimulation was stopped as soon as arousals, awakenings or shifts into other sleep stages were detected. On average, stimulation duration during sleep was 29.77 ± 1.86 min (range 18–45.5 min) following Diekelmann et al.'s (2011) protocol. Post-experimental offline scoring confirmed that 92.55 ± 1.89% of odor stimulation and 92.29 ± 2.98% of placebo stimulation actually took place during REM sleep. Participants were awakened directly after the last reactivation in the REM sleep phase. Shortly after awakening, participants learned the interference 2-D object-location task. After a break of 20 min, recall of the card-pair locations of the original task, learned before sleep, was tested. Participants were asked to perform as well as possible in each of the memory tasks.

Bottom Line: In humans, experimentally inducing hippocampal memory reactivations during slow-wave sleep (but not during wakefulness) benefits consolidation and immediately stabilizes declarative memories against future interference.We show that odor-induced memory reactivation during REM sleep does not stabilize memories against future interference.We propose that the beneficial effect of reactivation during sleep on memory stability might be critically linked to processes characterizing SWS including, e.g., slow oscillatory activity, sleep spindles, or low cholinergic tone, which are required for a successful redistribution of memories from medial temporal lobe regions to neocortical long-term stores.

View Article: PubMed Central - PubMed

Affiliation: Division of Biopsychology, Institute of Psychology, University of Zurich Zurich, Switzerland.

ABSTRACT
Memory reactivations in hippocampal brain areas are critically involved in memory consolidation processes during sleep. In particular, specific firing patterns of hippocampal place cells observed during learning are replayed during subsequent sleep and rest in rodents. In humans, experimentally inducing hippocampal memory reactivations during slow-wave sleep (but not during wakefulness) benefits consolidation and immediately stabilizes declarative memories against future interference. Importantly, spontaneous hippocampal replay activity can also be observed during rapid eye movement (REM) sleep and some authors have suggested that replay during REM sleep is related to processes of memory consolidation. However, the functional role of reactivations during REM sleep for memory stability is still unclear. Here, we reactivated memories during REM sleep and examined its consequences for the stability of declarative memories. After 3 h of early, slow-wave sleep (SWS) rich sleep, 16 healthy young adults learned a 2-D object location task in the presence of a contextual odor. During subsequent REM sleep, participants were either re-exposed to the odor or to an odorless vehicle, in a counterbalanced within subject design. Reactivation was followed by an interference learning task to probe memory stability after awakening. We show that odor-induced memory reactivation during REM sleep does not stabilize memories against future interference. We propose that the beneficial effect of reactivation during sleep on memory stability might be critically linked to processes characterizing SWS including, e.g., slow oscillatory activity, sleep spindles, or low cholinergic tone, which are required for a successful redistribution of memories from medial temporal lobe regions to neocortical long-term stores.

No MeSH data available.