Perturbation of theta-gamma coupling at the temporal lobe hinders verbal declarative memory

Gabriel Amador de Lara, Ivan Alekseichuk, Zsolt Turi, Albert Lehr, Andrea Antal, Walter Paulus

Research output: Contribution to journalArticlepeer-review

39 Scopus citations


Background: Phase-amplitude cross-frequency coupling (PAC) is characterized by the modulation of the power of a fast brain oscillation (e.g., gamma) by the phase of a slow rhythm (e.g., theta). PAC in different sub- and neocortical regions is known to underlie effective neural communication and correlates with successful long-term memory formation. Objective/Hypothesis: The present work aims to extend earlier observational data, by probing the functional role of theta-gamma PAC in the left temporal cortex in humans during verbal long-term memory encoding. Methods: In three double-blinded, placebo-controlled experiments (n = 72), we employed cross-frequency transcranial alternating current stimulation (tACS) to externally modulate ongoing PAC during a verbal-associative learning task. Three types of cross-frequency tACS protocols were used: bursts of high gamma tACS were coupled to the peak or trough of the theta tACS cycle, and a control condition where gamma tACS was continuously superimposed at theta tACS cycles. Results: Gamma bursts coupled to the trough of theta tACS induced robust behavioral impairment in memory performance (p < .01), whereas gamma burst coupled to the peak or continuously superimposed with theta tACS had no significant behavioral effects. Conclusions: Our results demonstrate direct evidence regarding the importance of theta-gamma coupling in verbal long-term memory formation.

Original languageEnglish (US)
Pages (from-to)509-517
Number of pages9
JournalBrain Stimulation
Issue number3
StatePublished - May 2018

Bibliographical note

Funding Information:
We thank Christine Crozier for language editing of the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft ( PA 419/15-1 ) awarded to WP.

Publisher Copyright:
© 2017 Elsevier Inc.


  • Long-term memory
  • Phase-amplitude cross-frequency coupling
  • TACS
  • Temporal lobe
  • Verbal episodic memory

PubMed: MeSH publication types

  • Journal Article
  • Research Support, Non-U.S. Gov't
  • Controlled Clinical Trial


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