Alpha rhythms reveal when, where and how memories are retrieved

SummaryOur memories for past experiences can range from vague recognition to full-blown recall of associated details. Neuroimaging research has tried to understand the brain mechanisms underlying qualitatively different memories for decades (Yonelinas, 2002). On the one hand, Electroencephalography (EEG) has shown that recall signals unfold a few hundred milliseconds after simple recognition and are hallmarked by sustained voltage deflections over left posterior sensors (Herron, 2007; Johansson & Mecklinger, 2003; Mecklinger, Rosburg, & Johansson, 2016; Rugg & Curran, 2007). However, sensor-based analyses only provide limited insights into the supporting brain networks. On the other hand, functional magnetic resonance imaging (fMRI) has revealed a ‘core recollection network’ centred on posterior parietal and medial temporal lobe (MTL) regions (Hayama, Vilberg, & Rugg, 2012; Johnson, Suzuki, & Rugg, 2013; King, de Chastelaine, Elward, Wang, & Rugg, 2015; Rugg, Johnson, & Uncapher, 2015; Rugg & Vilberg, 2013; Thakral, Benoit, & Schacter, 2017). However, due to the relatively poor time resolution of fMRI, the temporal dynamics of these regions during retrieval remain largely unknown. In order to overcome these modality-specific limitations, we here used Magnetoencephalography (MEG) in a verbal episodic memory paradigm assessing correct rejection (CR) of lures, item recognition (IR) of old words and associative recall (AR) of paired target words. We found that power decreases in the alpha frequency band (10-12 Hz) systematically track different mnemonic outcomes in both time and space: Over left posterior sensors, alpha power decreased in a stepwise fashion from 500 ms onward, first from CR to IR and then from IR to AR. When projecting alpha power into source space, the ‘core recollection network’ known from fMRI studies emerged, including posterior parietal cortex (PPC) and hippocampus. While PPC showed a linear change across conditions, hippocampal effects were specific to recall. Critically, the hippocampal recall effect emerged ∼200 ms before the PPC recall effect, suggesting a bottom-up recall signal from hippocampus to PPC. Our data thus link engagement of the core recollection network to the temporal dynamics of episodic memory and suggest that alpha rhythms constitute a fundamental oscillatory mechanism revealing when, where and how our memories are retrieved.HighlightsAlpha rhythms distinguish between different retrieval outcomesAlpha power time courses track item recognition and associative recallSource alpha power decreases track the fMRI core recollection networkHippocampal recall signal precedes parietal signal