Elsevier

NeuroImage

Volume 85, Part 2, 15 January 2014, Pages 730-737
NeuroImage

Theta oscillations orchestrate medial temporal lobe and neocortex in remembering autobiographical memories

https://doi.org/10.1016/j.neuroimage.2013.08.029Get rights and content

Highlights

  • Personal audio recordings from the past trigger autobiographic memories

  • Medial temporal lobe and neocortex are orchestrated in theta during recollection

  • Medial temporal lobe theta synchrony with precuneus and medial prefrontal cortex

  • The amount of theta synchrony predicts the vividness of autobiographical memories

Abstract

Remembering autobiographical events can be associated with detailed visual imagery. The medial temporal lobe (MTL), precuneus and prefrontal cortex are held to jointly enable such vivid retrieval, but how these regions are orchestrated remains unclear. An influential prediction from animal physiology is that neural oscillations in theta frequency may be important. In this experiment, participants prospectively collected audio recordings describing personal autobiographical episodes or semantic knowledge over 2 to 7 months. These were replayed as memory retrieval cues while recording brain activity with magnetoencephalography (MEG). We identified a peak of theta power within a left MTL region of interest during both autobiographical and General Semantic retrieval. This MTL region was selectively phase-synchronized with theta oscillations in precuneus and medial prefrontal cortex, and this synchrony was higher during autobiographical as compared to General Semantic knowledge retrieval. Higher synchrony also predicted more detailed visual imagery during retrieval. Thus, theta phase-synchrony orchestrates in humans the MTL with a distributed neocortical memory network when vividly remembering autobiographical experiences.

Introduction

Humans have the ability to vividly recollect previous autobiographical experiences. Neuroimaging studies have shown that a distributed network of brain regions is associated with the retrieval of autobiographical memories (AM), comprising prefrontal, medial (including the hippocampus) temporal lobe (MTL), and posterior regions, such as precuneus and posterior cingulate cortex (Cabeza and St, 2007, Maguire, 2001, Svoboda et al., 2006). The sense of recollection brought by the act of recalling unique personal memory episodes is thought to be mediated by the effective coordination of this set of regions (Maguire, 2001). In fact, influential models of memory organization hold that recollecting personal episodes require the coordination of neocortical areas and the MTL, thereby implementing reinstatement of retrieved information in distributed neocortical assemblies (Marr, 1971, McClelland et al., 1995, Rolls, 2000, Treves and Rolls, 1994). Yet, little is known about the mechanisms governing such neural interactions.

A putative mechanism by which functional neural integration could take place is through brain oscillations. Oscillatory rhythms are thought to coordinate the precise timing of neurons in large-scale neural networks and thereby influence representation and long-term coding of information (Buzsaki and Draguhn, 2004, Huxter et al., 2003, Lisman and Otmakhova, 2001, Steriade, 2000). A special emphasis has been given to theta (4–8 Hz) oscillations in learning and memory tasks in animal (Huxter et al., 2003, O'Keefe and Recce, 1993) and human research (Caplan et al., 2003, Ekstrom et al., 2005, Guderian and Duzel, 2005, Kahana et al., 1999, Osipova et al., 2006, Raghavachari et al., 2001; see for a recent review Duzel et al., 2010). These findings support the view that cortical theta oscillations are crucial to memory-related processes, consistent with computational models of memory postulating that theta mediates a dynamic MTL–neocortical orchestration, allowing a functional implementation of cortical reinstatement during recollection.

Formal assessment of this prediction is hampered by the methodological complexity of testing AM. The typical retrospective sampling of AMs for laboratory assessment lacks experimental control over prior rehearsal, personal significance, emotionality, and retrieval effort. Prospective collection of autobiographical stimuli enhances experimental control and can provide highly specific retrieval cues, akin to revisiting a particular scene where a unique or important event occurred (Conway et al., 2002, Heisz et al., in press). Such cues promote vivid recollection of everyday episodes (Brewer, 1988, Sheldon and Levine, 2013), engaging episodic memory and its accompanying state of autonoetic consciousness (Wheeler et al., 1997).

Furthermore, despite evidence from animal and human intracranial recordings (e.g., Anderson et al., 2010, Colgin, 2011, Foster et al., 2013, Watrous et al., 2013) and human functional neuroimaging studies (Tambini et al., 2010), investigating the neurophysiological mechanisms sustaining MTL–neocortical interactions in memory has been affected by limited access to simultaneous acquisition of distributed neural activity together with anatomically targeted recordings. However, a number of recent studies (Cornwell et al., 2010, Guitart-Masip et al., 2013, Kaplan et al., 2012, Poch et al., 2011, Riggs et al., 2009) have shown that it is possible to record simultaneously and non-invasively from the MTL and cortex using whole-head magnetoencephalography (MEG), and that such sensitivity might be incremented when using a realistic anatomical and electrophysiological model of deep brain activity (Attal and Schwartz, 2013). In fact, it has been observed that there could be zero-phase lag correlation between hippocampal activity and MEG (Buzsaki et al., 2012). It should be noted that, albeit some initial available empirical evidence that theta emanating from the MTL (specifically from the hippocampus) could be observed in correspondence with MEG activity (Dalal et al., in press), it is possible that not all hippocampal activity patterns can be measured from the scalp. One reason for this could be that some circuits within the hippocampus form closed loops (see Nunez and Silberstein (2000) for a theoretical discussion on this topic).

Here, we investigated whether and how MTL–neocortical orchestration takes place during the retrieval of unique episodic elements of AM through the recording of MEG data during stimulation with prospectively collected AM cues. We sought to test the hypothesis that neocortical activity linked to the retrieval of AMs was coordinated by dynamic interactions with the MTL through the phase of the ongoing theta.

Section snippets

Participants

Eight healthy adults (3 males; mean age = 30; STD = 5.34; mean education = 18 years; STD = 2.5 years) participated in the study. None of the participants reported a history of neurological, psychiatric or any other serious medical problems. All participants gave written informed consent for the study, which was approved by the hospital research ethics board.

Collection of autobiographical stimuli

Participants collected stimuli prospectively over 2–7 months using a portable digital recorder (ICD-BP100 V-O-R; Sony) following the methods specified

Personal Episodic and General Semantic subjective ratings

Personal Episodic was more effective at evoking vivid recollections than General Semantic condition (Table 1). This effect was confirmed statistically with a repeated measures analysis of variance (ANOVA) with memory type (Personal Episodic and General Semantic) and subjective rating as within factors. The ANOVA showed a significant main effect of condition (F(1,7) = 169.2, MSE = 502.76, p < 0.0001) and a significant interaction memory type × subjective rating (F(3,21) = 3.16, MSE = 0.82, p = 0.048),

Discussion

We found that the MTL region was selectively phase synchronized in theta frequency with the precuneus and mPFC during richly detailed autobiographical recollection evoked by prospectively recorded audio cues from remote everyday events. In a subsequent whole-brain analysis, higher synchrony in similar precuneus and mPFC regions predicted the degree of visual imagery achieved during retrieval, a core property accompanying the recollection of autobiographical memories (Greenberg and Rubin, 2003).

Acknowledgments

Sabitha Kanagasabai and Tim Bardouille are thanked for technical assistance and Marc Guitart-Masip for his advice in the phase lag index analysis. This study was supported by funding from the Canadian Institutes of Health Research, grant # MGP-62963 to BL and the National Institute of Child Health and Human Development, National Institutes of Health, grant # HD42385-01 to B.L. LF was supported with a Spanish Government grant (PSI2010-15024) and the Ramon y Cajal program (RYC-2009-05471). The

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