Sound Asleep: Processing and Retention of Slow Oscillation Phase-Targeted Stimuli (original) (raw)
Related papers
The Journal of Neuroscience, 2016
Slow oscillations during slow-wave sleep (SWS) may facilitate memory consolidation by regulating interactions between hippocampal and cortical networks. Slow oscillations appear as high-amplitude, synchronized EEG activity, corresponding to upstates of neuronal depolarization and downstates of hyperpolarization. Memory reactivations occur spontaneously during SWS, and can also be induced by presenting learning-related cues associated with a prior learning episode during sleep. This technique, targeted memory reactivation (TMR), selectively enhances memory consolidation. Given that memory reactivation is thought to occur preferentially during the slow-oscillation upstate, we hypothesized that TMR stimulation effects would depend on the phase of the slow oscillation. Participants learned arbitrary spatial locations for objects that were each paired with a characteristic sound (eg, cat-meow). Then, during SWS periods of an afternoon nap, one-half of the sounds were presented at low intensity. When object location memory was subsequently tested, recall accuracy was significantly better for those objects cued during sleep. We report here for the first time that this memory benefit was predicted by slow-wave phase at the time of stimulation. For cued objects, location memories were categorized according to amount of forgetting from pre-to post-nap. Conditions of high versus low forgetting corresponded to stimulation timing at different slowoscillation phases, suggesting that learning-related stimuli were more likely to be processed and trigger memory reactivation when they occurred at the optimal phase of a slow oscillation. These findings provide insight into mechanisms of memory reactivation during sleep, supporting the idea that reactivation is most likely during cortical upstates.
Boosting slow oscillations during sleep potentiates memory
Nature
There is compelling evidence that sleep contributes to the longterm consolidation of new memories 1 . This function of sleep has been linked to slow (,1 Hz) potential oscillations, which predominantly arise from the prefrontal neocortex and characterize slow wave sleep 2-4 . However, oscillations in brain potentials are commonly considered to be mere epiphenomena that reflect synchronized activity arising from neuronal networks, which links the membrane and synaptic processes of these neurons in time 5 . Whether brain potentials and their extracellular equivalent have any physiological meaning per se is unclear, but can easily be investigated by inducing the extracellular oscillating potential fields of interest 6-8 . Here we show that inducing slow oscillationlike potential fields by transcranial application of oscillating potentials (0.75 Hz) during early nocturnal non-rapid-eye-movement sleep, that is, a period of emerging slow wave sleep, enhances the retention of hippocampus-dependent declarative memories in healthy humans. The slowly oscillating potential stimulation induced an immediate increase in slow wave sleep, endogenous cortical slow oscillations and slow spindle activity in the frontal cortex. Brain stimulation with oscillations at 5 Hz-another frequency band that normally predominates during rapid-eye-movement sleep-decreased slow oscillations and left declarative memory unchanged. Our findings indicate that endogenous slow potential oscillations have a causal role in the sleep-associated consolidation of memory, and that this role is enhanced by field effects in cortical extracellular space.
Auditory Closed-Loop Stimulation of the Sleep Slow Oscillation Enhances Memory
Neuron, 2013
Brain rhythms regulate information processing in different states to enable learning and memory formation. The <1 Hz sleep slow oscillation hallmarks slow-wave sleep and is critical to memory consolidation. Here we show in sleeping humans that auditory stimulation in phase with the ongoing rhythmic occurrence of slow oscillation up states profoundly enhances the slow oscillation rhythm, phasecoupled spindle activity, and, consequently, the consolidation of declarative memory. Stimulation out of phase with the ongoing slow oscillation rhythm remained ineffective. Closed-loop in-phase stimulation provides a straightforward tool to enhance sleep rhythms and their functional efficacy.
Targeted memory reactivation during sleep elicits neural signals related to learning content
2018
Reactivation of learning-related neural activity patterns is thought to drive memory stabilization. However, finding reliable, non-invasive, content-specific indicators of reactivation remains a central challenge. Here, we attempted to decode the content of reactivated memories in the electroencephalogram (EEG) during sleep. During encoding, human participants 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 righthand movements before bringing participants back for a final post-nap 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 reactivated the memories during sleep. Discrimination performance was significantly above chance and predicted subsequent memory, supporting the idea that reactivation leads to memory stabilization. Moreover, these lateralized signals increased with post-cue spindle power, demonstrating that reactivation 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 reactivation. .
Scientific Reports, 2019
slow-wave sleep (sWs) is known to contribute to memory consolidation, likely through the reactivation of previously encoded waking experiences. Contemporary studies demonstrate that when auditory or olfactory stimulation is administered during memory encoding and then reapplied during sWs, memory consolidation can be enhanced, an effect that is believed to rely on targeted memory reactivation (TMR) induced by the sensory stimulation. Here, we show that transcranial current stimulations (tCs) during sleep can also be used to induce tMR, resulting in the facilitation of high-level cognitive processes. Participants were exposed to repeating sequences in a realistic 3D immersive environment while being stimulated with particular tCs patterns. A subset of these tCs patterns was then reapplied during sleep stages N2 and SWS coupled to slow oscillations in a closed-loop manner. We found that in contrast to our initial hypothesis, performance for the sequences corresponding to the reapplied tCs patterns was no better than for other sequences that received stimulations only during wake or not at all. In contrast, we found that the more stimulations participants received overnight, the more likely they were to detect temporal regularities governing the learned sequences the following morning, with tCs-induced beta power modulations during sleep mediating this effect. Sleep plays an important role in consolidating recently encoded memories and facilitating a variety of cognitive skills 1. The consolidation process for declarative memories is thought to involve the coordinated transfer of memory traces from short-term fast-learning storage in the hippocampus to long-term slow-learning storage across the neocortex, occurring mostly during slow-wave sleep (SWS). Evidence from multi-site in vivo recordings in rodents during SWS 2,3 and fMRI recordings in humans during waking periods of rest 4,5 shows that the fidelity of the consolidation process, as manifested in stronger subsequent recall of the learned stimuli, may be related to the reactivations, or replay, of the spatiotemporal brain activity patterns that were elicited during learning at wake. Specifically, coordinated replay across the hippocampus and neocortex-as indexed by enhanced slow-wave (SW) oscillations 6 , increased spindle-SW phase-amplitude coupling 7,8 , and enhanced functional connectivity between hippocampal and cortical voxels 4,9 , among others-may allow for the consolidation of waking experiences in the neocortex 10 and result in the facilitation of subsequent memory recall performance during waking 11,12. Accordingly, over the last decade and a half, researchers have developed non-invasive methods to modulate both memory consolidation during sleep and its manifestations in brain oscillations using either sensory or electric
Napping to renew learning capacity: enhanced encoding after stimulation of sleep slow oscillations
European Journal of Neuroscience, 2013
As well as consolidating memory, sleep has been proposed to serve a second important function for memory, i.e. to free capacities for the learning of new information during succeeding wakefulness. The slow wave activity (SWA) that is a hallmark of slow wave sleep could be involved in both functions. Here, we aimed to demonstrate a causative role for SWA in enhancing the capacity for encoding of information during subsequent wakefulness, using transcranial slow oscillation stimulation (tSOS) oscillating at 0.75 Hz to induce SWA in healthy humans during an afternoon nap. Encoding following the nap was tested for hippocampusdependent declarative materials (pictures, word pairs, and word lists) and procedural skills (finger sequence tapping). As compared with a sham stimulation control condition, tSOS during the nap enhanced SWA and significantly improved subsequent encoding on all three declarative tasks (picture recognition, cued recall of word pairs, and free recall of word lists), whereas procedural finger sequence tapping skill was not affected. Our results indicate that sleep SWA enhances the capacity for encoding of declarative materials, possibly by down-scaling hippocampal synaptic networks that were potentiated towards saturation during the preceding period of wakefulness.
Reverberation, storage, and postsynaptic propagation of memories during sleep
Learning & Memory, 2004
In mammals and birds, long episodes of nondreaming sleep (“slow-wave” sleep, SW) are followed by short episodes of dreaming sleep (“rapid-eye-movement” sleep, REM). Both SW and REM sleep have been shown to be important for the consolidation of newly acquired memories, but the underlying mechanisms remain elusive. Here we review electrophysiological and molecular data suggesting that SW and REM sleep play distinct and complementary roles on memory consolidation: While postacquisition neuronal reverberation depends mainly on SW sleep episodes, transcriptional events able to promote long-lasting memory storage are only triggered during ensuing REM sleep. We also discuss evidence that the wake-sleep cycle promotes a postsynaptic propagation of memory traces away from the neural sites responsible for initial encoding. Taken together, our results suggest that basic molecular and cellular mechanisms underlie the reverberation, storage, and propagation of memory traces during sleep. We prop...
Memory stabilization with targeted reactivation during human slow-wave sleep
Proceedings of the National Academy of Sciences, 2012
It is believed that neural representations of recent experiences become reactivated during sleep, and that this process serves to stabilize associated memories in long-term memory. Here, we initiated this reactivation process for specific memories during slow-wave sleep. Participants studied 50 object-location associations with object-related sounds presented concurrently. For half of the associations, the related sounds were re-presented during subsequent slow-wave sleep while participants underwent functional MRI. Compared with control sounds, related sounds were associated with increased activation of right parahippocampal cortex. Postsleep memory accuracy was positively correlated with sound-related activation during sleep in various brain regions, including the thalamus, bilateral medial temporal lobe, and cerebellum. In addition, postsleep memory accuracy was also positively correlated with pre-to postsleep changes in parahippocampal-medial prefrontal connectivity during retrieval of reactivated associations. Our results suggest that the brain is differentially activated by studied and unstudied sounds during deep sleep and that the thalamus and medial temporal lobe are involved in establishing the mnemonic consequences of externally triggered reactivation of associative memories. consolidation | neuroimaging | EEG-functional MRI | replay
Oscillating circuitries in the sleeping brain
Nature Reviews Neuroscience, 2019
Since the first recordings of electrical activity in the brain 1,2 , scalp electroencephalography (EEG) has been commonly used to measure the differences in generalized brain activity between wakefulness and sleep. The classical descriptions of sleep-related brain activity, which were derived from low spatial resolution EEG, led to the distinction between rapid eye movement (REM, also termed paradoxical) sleep and non-REM (NREM) sleep (Fig. 1a). However, the multifaceted organization of sleep-related brain activity in space and time has only been appreciated in the past decade. Theta and gamma rhythms are the hallmarks of REM sleep as recorded by scalp EEG or intracranial local field potentials (LFPs, Fig. 1a), whereas the predominant oscillations during NREM sleep are slow oscillations, delta waves, spindles and sharp wave-ripples (SWRs). These typical sleeprelated oscillations result from the synchronous activity of neural circuits restricted to the thalamus, neocortex or hippocampus. Their amplitudes correlate with the level of synchronization of underlying neuronal firing, and strongly depend on the intrinsic properties of ion channels, transporters and receptors expressed at the cell membrane, cell morphology, and extrinsic influences from synaptic inputs and background neural activity (that is, noise). At the network level, neural circuit oscillations m i g ht a l s o r e s ult f r o m m o n os y n aptic i n t er a c tions b e t we en fast excitatory and inhibitory neurons, feedback loops (for example, recurrent thalamocortical resonance) and slower forms of neuromodulation. Advances in multichannel surface and intracranial electrophysiological recordings in humans and rodents, together with functional imaging of brain activity across sleep states, have revealed a complex landscape of regionspecific activity. For example, 21-channel EEG recordings in humans showed a marked increase of oscillatory activity in the theta band concomitant with a decrease in the alpha band at the onset of NREM sleep; this increase