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Auditory stimulation during REM sleep modulates REM electrophysiology and cognitive performance.

ABSTRACT: REM sleep is critical for memory, emotion, and cognition. Manipulating brain activity during REM could improve our understanding of its function and benefits. Earlier studies have suggested that auditory stimulation in REM might modulate REM time and reduce rapid eye movement density. Building on this, we studied the cognitive effects and electroencephalographic responses related to such stimulation. We used acoustic stimulation locked to eye movements during REM and compared two overnight conditions (stimulation and no-stimulation). We evaluated the impact of this stimulation on REM sleep duration and electrophysiology, as well as two REM-sensitive memory tasks: visual discrimination and mirror tracing. Our results show that this auditory stimulation in REM decreases the rapid eye movements that characterize REM sleep and improves performance on the visual task but is detrimental to the mirror tracing task. We also observed increased beta-band activity and decreased theta-band activity following stimulation. Interestingly, these spectral changes were associated with changes in behavioural performance. These results show that acoustic stimulation can modulate REM sleep and suggest that different memory processes underpin its divergent impacts on cognitive performance.

SUBMITTER: Navarrete M

PROVIDER: S-EPMC10873307 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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Auditory stimulation during REM sleep modulates REM electrophysiology and cognitive performance.

Navarrete Miguel M Greco Viviana V Rakowska Martyna M Bellesi Michele M Lewis Penelope A PA

Communications biology 20240216 1

REM sleep is critical for memory, emotion, and cognition. Manipulating brain activity during REM could improve our understanding of its function and benefits. Earlier studies have suggested that auditory stimulation in REM might modulate REM time and reduce rapid eye movement density. Building on this, we studied the cognitive effects and electroencephalographic responses related to such stimulation. We used acoustic stimulation locked to eye movements during REM and compared two overnight condi ...[more]

PMID: 38365955

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Project description:We previously demonstrated that seizure occurrences at different zeitgeber times alter sleep and circadian rhythm differently. On the other hand, the synchronized delta wave of electroencephalogram (EEG) during non-rapid eye movement (NREM) sleep facilitates seizure, while the desynchronized EEG of rapid eye movement (REM) sleep suppresses it. We also elucidated that unilateral deep brain stimulation (DBS) of the anterior nucleus of thalamus (ANT) suppresses seizure recurrence. In the present study, we intraperitoneally injected pentylenetetrazol (PTZ, 40 mg/kg) for 14 consecutive days (PTZ kindling) to induce spontaneous seizure in rats, and a 30-min (delivered 10 min before each PTZ injection) or a 3-h DBS of unilateral ANT (delivered 1 h before each PTZ injection) was applied to suppress seizure. The frequency of DBS stimulation was 200 Hz and the electrical current consisted of biphasic square pulses with 50-?A intensity, 100-?s pulse width, and 4.1-ms stimulation interval. Our results found that PTZ-induced spontaneous seizure did not cause a significant change in the quantity of NREM sleep but suppressed the amount of REM sleep. Unilateral ANT DBS prolonged the onset latency of ictal seizure, decreased the spontaneous seizure duration, and increased the survival rate but did not change the amplitude of epileptiform EEGs during ictal period. Unilateral ANT DBS did not significantly alter NREM sleep but increased the amount of REM sleep. An analysis of the spectrograms of fast Fourier transform indicated that the intensities of all frequencies were enhanced during the PTZ-induced ictal period and the subsequent spontaneous seizure. Thirty minutes of unilateral ANT DBS suppressed the augmentation of low-frequency (<10 Hz) intensities during the spontaneous seizure induced by PTZ kindling. We further found that consecutive injections of PTZ progressively increased the enhancement of the delta powers during NREM sleep, whereas unilateral ANT DBS inhibited this progressive enhancement. It was also noticed that 30 min of ANT DBS exhibited a better efficacy in epilepsy suppression than 3 h of ANT DBS. These results elucidated that unilateral ANT DBS enhanced the seizure threshold by increasing the amount of REM sleep and decreasing the progressive enhancement of delta power during NREM sleep to suppress spontaneous seizure recurrences in PTZ kindling-induced epileptic rats.

Project description:IntroductionMaintaining cognitive performance during sleep deprivation is of vital importance in many professions, especially in high-risk professions like the military. It has long been known that sleep deprivation diminishes cognitive performance. To mitigate the negative effects on cognitive performance during crucial military tasks, new interventions are necessary. Non-invasive cervical transcutaneous vagus nerve stimulation (ctVNS) has gained traction as a method to boost alertness and cognitive functioning.MethodsWe investigated the effects of a 2 × 2 minute ctVNS stimulation protocol on three cognitive tasks applied during conditions of sleep-deprivation: a psychomotor vigilance task (PVT), a multitasking task (SynWin), and an inhibitory control task (stop-signal task; SST). In addition, participants also performed a close-quarter-battle (CQB) test in virtual reality (VR) to examine if potential effects of ctVNS translate to operational military contexts. A total of 35 military operators from Special Operations Forces (SOF) and SOF support units participated. They were randomly assigned to an active stimulation group or sham group. Before stimulation at 19:00 h, participants performed baseline tests. Participants stayed awake through the night and performed the cognitive tasks every 3 h. The last round of cognitive tasks was followed by the VR test.ResultsThough sleep deprivation was successfully induced, as evident from a decline in performance on all three cognitive tasks (effect of session: p < 0.001 SynWin; p < 0.001 PVT; p < 0.001 SST; Linear Mixed Model), no significant effects of ctVNS were found on cognitive task performance, as well as on the military operational VR task. However, the influence of stimulation intensity on SynWin performance showed a trend, indicating that higher stimulation intensities could have a negative impact on cognitive performance.DiscussionA 2 × 2 minute stimulation protocol may not be sufficient to elicit beneficial effects on cognitive-and operational military performance. Moreover, correct stimulation intensity may be critical to induce effects on cognitive performance, as stimulation effects may follow an inverted-u dose-response curve. Stimulation intensities in the current study are higher compared to a similar study that reported beneficial effects of ctVNS, which may explain this null finding. Further research is recommended to optimize stimulation protocols and investigate robustness of effects.

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Auditory stimulation during REM sleep modulates REM electrophysiology and cognitive performance.

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Auditory stimulation during REM sleep modulates REM electrophysiology and cognitive performance.

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