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Negative Results, Cognition and Behavior

Closed-loop acoustic stimulation enhances sleep oscillations but not memory performance

Simon Henin, Helen Borges, Anita Shankar, Cansu Sarac, Lucia Melloni, Daniel Friedman, Adeen Flinker, Lucas C Parra, Gyorgy Buzsaki, Orrin Devinsky and Anli Liu
eNeuro 11 October 2019, ENEURO.0306-19.2019; DOI: https://doi.org/10.1523/ENEURO.0306-19.2019
Simon Henin
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
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Helen Borges
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
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Anita Shankar
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
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Cansu Sarac
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
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Lucia Melloni
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
2NYU Langone Health, stth, New York, NY 10017
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Daniel Friedman
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
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Adeen Flinker
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
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Lucas C Parra
3Max Planck Institute for Empirical Aesthetics, Grüneburgweg 14, 60322 Frankfurt am Main, Germany
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Gyorgy Buzsaki
4Department of Biomedical Engineering, City College of New York, 160 Convent Ave, New York, NY 10031
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Orrin Devinsky
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
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Anli Liu
1NYU Comprehensive Epilepsy Center, th, New York, NY 10016, USA
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ABSTRACT

Slow-oscillations and spindle activity during non-REM sleep have been implicated in memory consolidation. Closed-loop acoustic stimulation has previously been shown to enhance slow oscillations and spindle activity during sleep and improve verbal associative memory. We assessed the effect of closed-loop acoustic stimulation during a daytime nap on a virtual reality spatial navigation task in 12 healthy human subjects in a randomized within-subject crossover design. We show robust enhancement of slow-spindle activity during sleep. However, no effects on behavioral performance were observed when comparing real versus sham stimulation. To explore whether memory enhancement effects were task-specific and dependent on nocturnal sleep, in a second experiment with 19 healthy subjects, we aimed to replicate a previous study which used closed-loop acoustic stimulation to enhance memory for word pairs. Methods were as close as possible to the original study, except we used a double-blind protocol, in which both subject and experimenter were unaware of the test condition. Again, we successfully enhanced slow-spindle power, but again did not strengthen associative memory performance with stimulation. We conclude that enhancement of slow-spindle oscillations may be insufficient to enhance memory performance in spatial navigation or verbal association tasks, and provide possible explanations for lack of behavioral replication.

SIGNIFICANCE STATEMENT Prior studies have demonstrated that a closed-loop acoustic pulse paradigm during sleep can enhance verbal memory performance. This technique has widespread scientific and clinical appeal due to its non-invasive nature and ease of application. We tested with a rigorous double-blind design whether this technique could enhance key sleep rhythms associated sleep-dependent memory performance. We discovered that we could reliably enhance slow and spindle rhythms, but did not improve memory performance in the stimulation condition compared to sham condition. Our findings suggest that enhancing slow-spindle rhythms is insufficient to enhance sleep-dependent learning.

  • Acoustic Stimulation
  • Declarative Memory
  • Memory
  • Oscillations
  • Sleep
  • Spindles

Footnotes

  • Authors report no conflict of interest.

  • This project was funded by NIH R01MH107396, NIH K23NS104252, the Zimin Foundation, and NYU Finding a Cure for Epilepsy and Seizures (FACES).

  • Correspondence: anli.liu{at}nyulangone.org; simon.henin{at}nyulangone.org

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Closed-loop acoustic stimulation enhances sleep oscillations but not memory performance
Simon Henin, Helen Borges, Anita Shankar, Cansu Sarac, Lucia Melloni, Daniel Friedman, Adeen Flinker, Lucas C Parra, Gyorgy Buzsaki, Orrin Devinsky, Anli Liu
eNeuro 11 October 2019, ENEURO.0306-19.2019; DOI: 10.1523/ENEURO.0306-19.2019

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Closed-loop acoustic stimulation enhances sleep oscillations but not memory performance
Simon Henin, Helen Borges, Anita Shankar, Cansu Sarac, Lucia Melloni, Daniel Friedman, Adeen Flinker, Lucas C Parra, Gyorgy Buzsaki, Orrin Devinsky, Anli Liu
eNeuro 11 October 2019, ENEURO.0306-19.2019; DOI: 10.1523/ENEURO.0306-19.2019
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Keywords

  • acoustic stimulation
  • declarative memory
  • memory
  • oscillations
  • sleep
  • spindles

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