Entrainment of Prefrontal Beta Oscillations Induces an Endogenous Echo and Impairs Memory Formation

• Published in: Current biology Vol. 24; no. 8; pp. 904 - 909
• Main Authors: Hanslmayr, Simon, Matuschek, Jonas, Fellner, Marie-Christin
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 14.04.2014
• Subjects: Adult; Beta Rhythm - physiology; Biological Clocks - physiology; Electroencephalography; Female; Humans; Learning - physiology; Male; Memory - physiology; Models, Psychological; Prefrontal Cortex - physiology; Transcranial Magnetic Stimulation
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2014.03.007

Brain oscillations across all frequency bands play a key role for memory formation [1–4]. Specifically, desynchronization of local neuronal assemblies in the left inferior prefrontal cortex (PFC) in the beta frequency (∼18 Hz) has been shown to be central for encoding of verbal memories [5–8]. However, it remains elusive whether prefrontal beta desynchronization is causally relevant for memory formation and whether these endogenous beta oscillations can be entrained by external stimulation. By using combined EEG-TMS (transcranial magnetic stimulation), we here address these fundamental questions in human participants performing a word-list learning task. Confirming our predictions, memory encoding was selectively impaired when the left inferior frontal gyrus (IFG) was driven at beta (18.7 Hz) compared to stimulation at other frequencies (6.8 Hz and 10.7 Hz) and to ineffective sham stimulation (18.7 Hz). Furthermore, a sustained oscillatory “echo” in the left IFG, which outlasted the stimulation period by approximately 1.5 s, was observed solely after beta stimulation. The strength of this beta echo was related to memory impairment on a between-subjects level. These results show endogenous oscillatory entrainment effects and behavioral impairment selectively in beta frequency for stimulation of the left IFG, demonstrating an intimate causal relationship between prefrontal beta desynchronization and memory formation. [Display omitted] •Stimulating the left IFG at beta selectively impairs memory formation•Stimulating at other frequencies has no effect on memory•A sustained oscillatory echo in the left IFG is observed when stimulated at beta•Subjects with stronger entrainment show more memory impairment Decreases in beta oscillatory activity in the left prefrontal cortex have been suggested to be important for episodic memory formation. Hanslmayr et al. show that stimulating the left prefrontal cortex in the beta frequency specifically impairs memory encoding and induces long-lasting aftereffects in the stimulated frequency-entrainment echoes.