Phase-Amplitude Coupling and Phase Synchronization Between Medial Temporal, Frontal and Posterior Brain Regions Support Episodic Autobiographical Memory Recall

Nicolas Roehri; Lucie Bréchet; Martin Seeber; Alvaro Pascual-Leone; Christoph M Michel

doi:10.1007/s10548-022-00890-4

Phase-Amplitude Coupling and Phase Synchronization Between Medial Temporal, Frontal and Posterior Brain Regions Support Episodic Autobiographical Memory Recall

Brain Topogr. 2022 Mar;35(2):191-206. doi: 10.1007/s10548-022-00890-4. Epub 2022 Jan 26.

Authors

Nicolas Roehri^#¹, Lucie Bréchet^#^{2

3

4}, Martin Seeber¹, Alvaro Pascual-Leone^{3

4

5}, Christoph M Michel^{6

7}

Affiliations

¹ Functional Brain Mapping Laboratory, Department of Fundamental Neurosciences, Campus Biotech, University of Geneva, 9 chemin des Mines, 1211, Geneva, Switzerland.
² Center for Biomedical Imaging (CIBM), Lausanne and Geneva, 1015, Lausanne, Switzerland.
³ Hinda and Arthur Marcus Institute for Aging Research and Deanna and Sidney Wolk Center for Memory Health, Hebrew SeniorLife, Boston, MA, USA.
⁴ Department of Neurology, Harvard Medical School, Boston, MA, USA.
⁵ Guttmann Brain Health Institute, Institut Guttman de Neurorehabilitació, Barcelona, Spain.
⁶ Functional Brain Mapping Laboratory, Department of Fundamental Neurosciences, Campus Biotech, University of Geneva, 9 chemin des Mines, 1211, Geneva, Switzerland. christoph.michel@unige.ch.
⁷ Center for Biomedical Imaging (CIBM), Lausanne and Geneva, 1015, Lausanne, Switzerland. christoph.michel@unige.ch.

^# Contributed equally.

Abstract

Episodic autobiographical memory (EAM) is a complex cognitive function that emerges from the coordination of specific and distant brain regions. Specific brain rhythms, namely theta and gamma oscillations and their synchronization, are thought of as putative mechanisms enabling EAM. Yet, the mechanisms of inter-regional interaction in the EAM network remain unclear in humans at the whole brain level. To investigate this, we analyzed EEG recordings of participants instructed to retrieve autobiographical episodes. EEG recordings were projected in the source space, and time-courses of atlas-based brain regions-of-interest (ROIs) were derived. Directed phase synchrony in high theta (7-10 Hz) and gamma (30-80 Hz) bands and high theta-gamma phase-amplitude coupling were computed between each pair of ROIs. Using network-based statistics, a graph-theory method, we found statistically significant networks for each investigated mechanism. In the gamma band, two sub-networks were found, one between the posterior cingulate cortex (PCC) and the medial temporal lobe (MTL) and another within the medial frontal areas. In the high theta band, we found a PCC to ventromedial prefrontal cortex (vmPFC) network. In phase-amplitude coupling, we found the high theta phase of the left MTL biasing the gamma amplitude of posterior regions and the vmPFC. Other regions of the temporal lobe and the insula were also phase biasing the vmPFC. These findings suggest that EAM, rather than emerging from a single mechanism at a single frequency, involves precise spatio-temporal signatures mapping on distinct memory processes. We propose that the MTL orchestrates activity in vmPFC and PCC via precise phase-amplitude coupling, with vmPFC and PCC interaction via high theta phase synchrony and gamma synchronization contributing to bind information within the PCC-MTL sub-network or valuate the candidate memory within the medial frontal sub-network.

Keywords: EEG; Episodic autobiographical memory; Network; Phase synchronization; Phase-amplitude coupling.

Publication types

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

MeSH terms

Brain
Brain Mapping
Humans
Memory, Episodic*
Mental Recall
Prefrontal Cortex
Temporal Lobe
Theta Rhythm