scholarly journals Low acetylcholine during early sleep is important for motor memory consolidation

SLEEP ◽  
2019 ◽  
Vol 43 (6) ◽  
Author(s):  
Samsoon Inayat ◽  
Qandeel ◽  
Mojtaba Nazariahangarkolaee ◽  
Surjeet Singh ◽  
Bruce L McNaughton ◽  
...  

Abstract The synaptic homeostasis theory of sleep proposes that low neurotransmitter activity in sleep optimizes memory consolidation. We tested this theory by asking whether increasing acetylcholine levels during early sleep would weaken motor memory consolidation. We trained separate groups of adult mice on the rotarod walking task and the single pellet reaching task, and after training, administered physostigmine, an acetylcholinesterase inhibitor, to increase cholinergic tone in subsequent sleep. Post-sleep testing showed that physostigmine impaired motor skill acquisition of both tasks. Home-cage video monitoring and electrophysiology revealed that physostigmine disrupted sleep structure, delayed non-rapid-eye-movement sleep onset, and reduced slow-wave power in the hippocampus and cortex. Additional experiments showed that: (1) the impaired performance associated with physostigmine was not due to its effects on sleep structure, as 1 h of sleep deprivation after training did not impair rotarod performance, (2) a reduction in cholinergic tone by inactivation of cholinergic neurons during early sleep did not affect rotarod performance, and (3) stimulating or blocking muscarinic and nicotinic acetylcholine receptors did not impair rotarod performance. Taken together, the experiments suggest that the increased slow wave activity and inactivation of both muscarinic and nicotinic receptors during early sleep due to reduced acetylcholine contribute to motor memory consolidation.

2018 ◽  
Author(s):  
Samsoon Inayat ◽  
Qandeel ◽  
Mojtaba Nazariahangarkolaee ◽  
Surjeet Singh ◽  
Bruce L. McNaughton ◽  
...  

AbstractThe synaptic homeostasis theory of sleep proposes that low neurotransmitter activity in sleep is optimal for memory consolidation. We tested this theory by asking whether increasing acetylcholine levels during early sleep would disrupt motor memory consolidation. We trained separate groups of adult mice on the rotarod walking and skilled reaching for food tasks, and after training, administered physostigmine, an acetylcholinesterase inhibitor, to increase cholinergic tone in subsequent sleep. Post-sleep testing suggested that physostigmine impaired motor skill acquisition. Home-cage video monitoring and electrophysiology revealed that physostigmine disrupted sleep structure, delayed non-rapid-eye-movement sleep onset, and reduced slow-wave power in the hippocampus and cortex. The impaired motor performance with physostigmine, however, was not solely due to its effects on sleep structure, as one hour of sleep deprivation after training did not impair rotarod performance. A reduction in cholinergic tone by inactivation of cholinergic neurons during early sleep also affected rotarod performance. Administration of agonists and antagonists of muscarinic and nicotinic acetylcholine receptors revealed that activation of muscarinic receptors during early sleep impaired rotarod performance. The experiments suggest that the increased slow wave activity and inactivation of muscarinic receptors during early sleep due to reduced acetylcholine contribute to motor memory consolidation.


1987 ◽  
Vol 116 (1) ◽  
pp. 36-42 ◽  
Author(s):  
A. Steiger ◽  
T. Herth ◽  
F. Holsboer

Abstract. Sleep-electroencephalography, and the nocturnal secretion of cortisol and GH were investigated simultaneously in a sample of 25 male normal controls (27.1 ± 1.3 years) in order further to examine interaction between sleep structure and concurrent endocrine activity. Slow wave sleep activity was increased during the first part of the night, whereas cortisol concentration was low and GH output reached maximal levels. The second half of the night was characterized by a relative preponderance of REM-sleep, low GH-concentration, and an increase in cortisol. However, no distinct reciprocal interaction between cortisol and GH concentration was noted. In all subjects, a pronounced GH surge between 22.00 and 02.00 h was recorded which occurred independently of the presence of slow wave sleep. Six out of the 25 subjects showed nocturnal GH increases even before sleep onset. These data indicate that somatotropic cell activity during night is less dependent upon the sleeping state or specific conventially defined sleep stages than originally reported.


2016 ◽  
Vol 2016 ◽  
pp. 1-11 ◽  
Author(s):  
Richard Thomas ◽  
Mikkel Malling Beck ◽  
Rune Rasmussen Lind ◽  
Line Korsgaard Johnsen ◽  
Svend Sparre Geertsen ◽  
...  

High intensity aerobic exercise amplifies offline gains in procedural memory acquired during motor practice. This effect seems to be evident when exercise is placed immediately after acquisition, during the first stages of memory consolidation, but the importance of temporal proximity of the exercise bout used to stimulate improvements in procedural memory is unknown. The effects of three different temporal placements of high intensity exercise were investigated following visuomotor skill acquisition on the retention of motor memory in 48 young (24.0 ± 2.5 yrs), healthy male subjects randomly assigned to one of four groups either performing a high intensity (90% Maximal Power Output) exercise bout at 20 min (EX90), 1 h (EX90+1), 2 h (EX90+2) after acquisition or rested (CON). Retention tests were performed at 1 d (R1) and 7 d (R7). At R1 changes in performance scores after acquisition were greater for EX90 than CON (p<0.001) and EX90+2 (p=0.001). At R7 changes in performance scores for EX90, EX90+1, and EX90+2 were higher than CON (p<0.001,p=0.008, andp=0.008, resp.). Changes for EX90 at R7 were greater than EX90+2 (p=0.049). Exercise-induced improvements in procedural memory diminish as the temporal proximity of exercise from acquisition is increased. Timing of exercise following motor practice is important for motor memory consolidation.


2014 ◽  
Vol 26 (12) ◽  
pp. 2716-2734 ◽  
Author(s):  
Ella Gabitov ◽  
David Manor ◽  
Avi Karni

An almost universally accepted tacit expectation is that learning and memory consolidation processes must be reflected in the average brain activity in brain areas relevant to task performance. Motor cortex (M1) plasticity has been implicated in motor skill acquisition and its consolidation. Nevertheless, no consistent pattern of changes in the average signal, related to motor learning or motor memory consolidation following a single session of training, has emerged from imaging studies. Here we show that the pattern and magnitude of short-term brain activity modulations in response to task repetition, in M1, may provide a robust signature for effective motor memory consolidation processes. We studied participants during the paced performance of a finger-to-thumb opposition sequence (FOS), intensively trained a day earlier, and a similarly constructed untrained FOS. In addition to within-session “on-line” gains, most participants expressed delayed, consolidation-phase gains in the performance of the trained FOS. The execution of the trained FOS induced repetition enhancements in the contralateral M1 and bilaterally in the medial-temporal lobes, offsetting novelty-related repetition suppression effects. Moreover, the M1 modulations were positively correlated with the magnitude of each participant's overnight delayed gains but not with absolute performance levels. Our results suggest that short-term enhancements of brain signals upon task repetition reflect the effectiveness of overnight motor memory consolidation. We propose that procedural memory consolidation processes may affect the excitation–inhibition balance within cortical representations of the trained movements; this new balance is better reflected in repetition effects than in the average level of evoked neural activity.


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.


2014 ◽  
Vol 62 (1) ◽  
pp. 89-99 ◽  
Author(s):  
Carla D. Cash ◽  
Sarah E. Allen ◽  
Amy L. Simmons ◽  
Robert A. Duke

This study was designed to investigate the extent to which the presentation of an auditory model prior to learning a novel melody affects performance during active practice and the overnight consolidation of procedural memory. During evening training sessions, 32 nonpianist musicians practiced a 13-note keyboard melody with their left (nondominant) hand in twelve 30-s practice intervals separated by 30-s rest intervals. Participants were instructed to play the sequence “as quickly, accurately, and evenly as possible.” Approximately half the participants, prior to the first practice interval, listened to 10 repetitions of the target melody played at 552 tones per minute (half note = 138). All participants were tested on the target melody the following morning, approximately 12 hr after training, in three 30-s blocks separated by 30-s rest intervals. Performance was measured in terms of the mean number of correct key presses per 30-s block (CKP/B). Consistent with previous research, participants made considerable improvements in CKP/B during the evening training sessions and between the end of training and the morning test sessions. Learners who listened to the model made significantly larger gains in performance during training and between the end of training and test than did those who did not hear the model.


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