Distinct frequencies balance segregation with interaction between different memory types within a prefrontal circuit

Martina Bracco; Tuomas P Mutanen; Domenica Veniero; Gregor Thut; Edwin M Robertson

doi:10.1016/j.cub.2023.05.027

Distinct frequencies balance segregation with interaction between different memory types within a prefrontal circuit

Curr Biol. 2023 Jun 19;33(12):2548-2556.e6. doi: 10.1016/j.cub.2023.05.027. Epub 2023 Jun 2.

Authors

Martina Bracco¹, Tuomas P Mutanen², Domenica Veniero³, Gregor Thut⁴, Edwin M Robertson⁵

Affiliations

¹ Sorbonne Université, Institut du Cerveau, Paris Brain Institute, ICM, Inserm, CNRS, APHP, Hôpital de la Pitié Salpêtrière, 47 Bd de l'Hôpital, 75013 Paris, France.
² Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, P.O. box 12200, FI-00076 Aalto, Finland.
³ School of Psychology, University of Nottingham, Nottingham NG7 2RD, UK.
⁴ Institute of Neuroscience and Psychology, Centre for Cognitive Neuroimaging, University of Glasgow, Glasgow G12 8QB, UK.
⁵ Institute of Neuroscience and Psychology, Centre for Cognitive Neuroimaging, University of Glasgow, Glasgow G12 8QB, UK. Electronic address: edwin.robertson@glasgow.ac.uk.

PMID: 37269827
DOI: 10.1016/j.cub.2023.05.027

Abstract

Once formed, the fate of memory is uncertain. Subsequent offline interactions between even different memory types (actions versus words) modify retention.¹^,²^,³^,⁴^,⁵^,⁶ These interactions may occur due to different oscillations functionally linking together different memory types within a circuit.⁷^,⁸^,⁹^,¹⁰^,¹¹^,¹²^,¹³ With memory processing driving the circuit, it may become less susceptible to external influences.¹⁴ We tested this prediction by perturbing the human brain with single pulses of transcranial magnetic stimulation (TMS) and simultaneously measuring the brain activity changes with electroencephalography (EEG¹⁵^,¹⁶^,¹⁷). Stimulation was applied over brain areas that contribute to memory processing (dorsolateral prefrontal cortex, DLPFC; primary motor cortex, M1) at baseline and offline, after memory formation, when memory interactions are known to occur.¹^,⁴^,⁶^,¹⁰^,¹⁸ The EEG response decreased offline (compared with baseline) within the alpha/beta frequency bands when stimulation was applied to the DLPFC, but not to M1. This decrease exclusively followed memory tasks that interact, revealing that it was due specifically to the interaction, not task performance. It remained even when the order of the memory tasks was changed and so was present, regardless of how the memory interaction was produced. Finally, the decrease within alpha power (but not beta) was correlated with impairment in motor memory, whereas the decrease in beta power (but not alpha) was correlated with impairment in word-list memory. Thus, different memory types are linked to different frequency bands within a DLPFC circuit, and the power of these bands shapes the balance between interaction and segregation between these memories.

Keywords: EEG; TMS; declarative memory; memory interactions; offline processsing; procedural memory; sequence learning.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Brain
Electroencephalography*
Humans
Memory / physiology
Prefrontal Cortex* / physiology
Transcranial Magnetic Stimulation