Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory Consolidation
Sleep is critically important to consolidate information learned throughout the day. Slow-wave sleep (SWS) serves to consolidate declarative memories, a process previously modulated with open-loop non-invasive electrical stimulation, though not always effectively. These failures to replicate could b...
| Main Authors: | , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2018-11-01
|
| Series: | Frontiers in Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fnins.2018.00867/full |
| _version_ | 1811281708430917632 |
|---|---|
| author | Aaron P. Jones Aaron P. Jones Jaehoon Choe Natalie B. Bryant Natalie B. Bryant Charles S. H. Robinson Charles S. H. Robinson Charles S. H. Robinson Nicholas A. Ketz Steven W. Skorheim Angela Combs Angela Combs Melanie L. Lamphere Melanie L. Lamphere Bradley Robert Bradley Robert Hope A. Gill Hope A. Gill Melissa D. Heinrich Melissa D. Heinrich Michael D. Howard Vincent P. Clark Vincent P. Clark Vincent P. Clark Vincent P. Clark Praveen K. Pilly |
| author_facet | Aaron P. Jones Aaron P. Jones Jaehoon Choe Natalie B. Bryant Natalie B. Bryant Charles S. H. Robinson Charles S. H. Robinson Charles S. H. Robinson Nicholas A. Ketz Steven W. Skorheim Angela Combs Angela Combs Melanie L. Lamphere Melanie L. Lamphere Bradley Robert Bradley Robert Hope A. Gill Hope A. Gill Melissa D. Heinrich Melissa D. Heinrich Michael D. Howard Vincent P. Clark Vincent P. Clark Vincent P. Clark Vincent P. Clark Praveen K. Pilly |
| author_sort | Aaron P. Jones |
| collection | DOAJ |
| description | Sleep is critically important to consolidate information learned throughout the day. Slow-wave sleep (SWS) serves to consolidate declarative memories, a process previously modulated with open-loop non-invasive electrical stimulation, though not always effectively. These failures to replicate could be explained by the fact that stimulation has only been performed in open-loop, as opposed to closed-loop where phase and frequency of the endogenous slow-wave oscillations (SWOs) are matched for optimal timing. The current study investigated the effects of closed-loop transcranial Alternating Current Stimulation (tACS) targeting SWOs during sleep on memory consolidation. 21 participants took part in a three-night, counterbalanced, randomized, single-blind, within-subjects study, investigating performance changes (correct rate and F1 score) on images in a target detection task over 24 h. During sleep, 1.5 mA closed-loop tACS was delivered in phase over electrodes at F3 and F4 and 180° out of phase over electrodes at bilateral mastoids at the frequency (range 0.5–1.2 Hz) and phase of ongoing SWOs for a duration of 5 cycles in each discrete event throughout the night. Data were analyzed in a repeated measures ANOVA framework, and results show that verum stimulation improved post-sleep performance specifically on generalized versions of images used in training at both morning and afternoon tests compared to sham, suggesting the facilitation of schematization of information, but not of rote, veridical recall. We also found a surprising inverted U-shaped dose effect of sleep tACS, which is interpreted in terms of tACS-induced faciliatory and subsequent refractory dynamics of SWO power in scalp EEG. This is the first study showing a selective modulation of long-term memory generalization using a novel closed-loop tACS approach, which holds great potential for both healthy and neuropsychiatric populations. |
| first_indexed | 2024-04-13T01:38:26Z |
| format | Article |
| id | doaj.art-4959d746f7404eb9b3feb5e52fdc69de |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-13T01:38:26Z |
| publishDate | 2018-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-4959d746f7404eb9b3feb5e52fdc69de2022-12-22T03:08:15ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2018-11-011210.3389/fnins.2018.00867419204Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory ConsolidationAaron P. Jones0Aaron P. Jones1Jaehoon Choe2Natalie B. Bryant3Natalie B. Bryant4Charles S. H. Robinson5Charles S. H. Robinson6Charles S. H. Robinson7Nicholas A. Ketz8Steven W. Skorheim9Angela Combs10Angela Combs11Melanie L. Lamphere12Melanie L. Lamphere13Bradley Robert14Bradley Robert15Hope A. Gill16Hope A. Gill17Melissa D. Heinrich18Melissa D. Heinrich19Michael D. Howard20Vincent P. Clark21Vincent P. Clark22Vincent P. Clark23Vincent P. Clark24Praveen K. Pilly25Psychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesCenter for Human-Machine Collaboration, Information and Systems Sciences Laboratory, HRL Laboratories, LLC, Malibu, CA, United StatesPsychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesPsychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesThe Mind Research Network, Albuquerque, NM, United StatesCenter for Human-Machine Collaboration, Information and Systems Sciences Laboratory, HRL Laboratories, LLC, Malibu, CA, United StatesCenter for Human-Machine Collaboration, Information and Systems Sciences Laboratory, HRL Laboratories, LLC, Malibu, CA, United StatesPsychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesPsychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesPsychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesPsychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesPsychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesCenter for Human-Machine Collaboration, Information and Systems Sciences Laboratory, HRL Laboratories, LLC, Malibu, CA, United StatesPsychology Clinical Neuroscience Center, The University of New Mexico, Albuquerque, NM, United StatesDepartment of Psychology, The University of New Mexico, Albuquerque, NM, United StatesThe Mind Research Network, Albuquerque, NM, United StatesDepartment of Neuroscience, University of New Mexico School of Medicine, Albuquerque, NM, United StatesCenter for Human-Machine Collaboration, Information and Systems Sciences Laboratory, HRL Laboratories, LLC, Malibu, CA, United StatesSleep is critically important to consolidate information learned throughout the day. Slow-wave sleep (SWS) serves to consolidate declarative memories, a process previously modulated with open-loop non-invasive electrical stimulation, though not always effectively. These failures to replicate could be explained by the fact that stimulation has only been performed in open-loop, as opposed to closed-loop where phase and frequency of the endogenous slow-wave oscillations (SWOs) are matched for optimal timing. The current study investigated the effects of closed-loop transcranial Alternating Current Stimulation (tACS) targeting SWOs during sleep on memory consolidation. 21 participants took part in a three-night, counterbalanced, randomized, single-blind, within-subjects study, investigating performance changes (correct rate and F1 score) on images in a target detection task over 24 h. During sleep, 1.5 mA closed-loop tACS was delivered in phase over electrodes at F3 and F4 and 180° out of phase over electrodes at bilateral mastoids at the frequency (range 0.5–1.2 Hz) and phase of ongoing SWOs for a duration of 5 cycles in each discrete event throughout the night. Data were analyzed in a repeated measures ANOVA framework, and results show that verum stimulation improved post-sleep performance specifically on generalized versions of images used in training at both morning and afternoon tests compared to sham, suggesting the facilitation of schematization of information, but not of rote, veridical recall. We also found a surprising inverted U-shaped dose effect of sleep tACS, which is interpreted in terms of tACS-induced faciliatory and subsequent refractory dynamics of SWO power in scalp EEG. This is the first study showing a selective modulation of long-term memory generalization using a novel closed-loop tACS approach, which holds great potential for both healthy and neuropsychiatric populations.https://www.frontiersin.org/article/10.3389/fnins.2018.00867/fullmemory consolidationclosed-looptACSsleeptDCSlearning and memory |
| spellingShingle | Aaron P. Jones Aaron P. Jones Jaehoon Choe Natalie B. Bryant Natalie B. Bryant Charles S. H. Robinson Charles S. H. Robinson Charles S. H. Robinson Nicholas A. Ketz Steven W. Skorheim Angela Combs Angela Combs Melanie L. Lamphere Melanie L. Lamphere Bradley Robert Bradley Robert Hope A. Gill Hope A. Gill Melissa D. Heinrich Melissa D. Heinrich Michael D. Howard Vincent P. Clark Vincent P. Clark Vincent P. Clark Vincent P. Clark Praveen K. Pilly Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory Consolidation Frontiers in Neuroscience memory consolidation closed-loop tACS sleep tDCS learning and memory |
| title | Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory Consolidation |
| title_full | Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory Consolidation |
| title_fullStr | Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory Consolidation |
| title_full_unstemmed | Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory Consolidation |
| title_short | Dose-Dependent Effects of Closed-Loop tACS Delivered During Slow-Wave Oscillations on Memory Consolidation |
| title_sort | dose dependent effects of closed loop tacs delivered during slow wave oscillations on memory consolidation |
| topic | memory consolidation closed-loop tACS sleep tDCS learning and memory |
| url | https://www.frontiersin.org/article/10.3389/fnins.2018.00867/full |
| work_keys_str_mv | AT aaronpjones dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT aaronpjones dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT jaehoonchoe dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT nataliebbryant dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT nataliebbryant dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT charlesshrobinson dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT charlesshrobinson dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT charlesshrobinson dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT nicholasaketz dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT stevenwskorheim dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT angelacombs dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT angelacombs dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT melaniellamphere dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT melaniellamphere dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT bradleyrobert dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT bradleyrobert dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT hopeagill dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT hopeagill dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT melissadheinrich dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT melissadheinrich dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT michaeldhoward dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT vincentpclark dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT vincentpclark dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT vincentpclark dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT vincentpclark dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation AT praveenkpilly dosedependenteffectsofclosedlooptacsdeliveredduringslowwaveoscillationsonmemoryconsolidation |