vmPFC drives hippocampal processing during autobiographical memory recall regardless of remoteness

Abstract

Our ability to recall past experiences, autobiographical memories (AMs), is crucial to cognition, endowing us with a sense of self and underwriting our capacity for autonomy.Traditional views assume that the hippocampus orchestrates event recall, whereas recent accounts propose that the ventromedial prefrontal cortex (vmPFC) instigates and coordinates hippocampal-dependent processes. Here we sought to characterise the dynamic interplay between hippocampus and vmPFC during AM recall to adjudicate between these perspectives.Leveraging the high temporal resolution of magnetoencephalography, we found that the hippocampus and the vmPFC showed the greatest power changes during AM retrieval.Moreover, responses in the vmPFC preceded activity in the hippocampus during initiation of AM recall, except during retrieval of the most recent AMs. The vmPFC drove hippocampal activity during recall initiation and also as AMs unfolded over subsequent seconds, and this effect was evident regardless of AM age. These results re-cast the positions of the hippocampus and the vmPFC in the AM retrieval hierarchy, with implications for theoretical accounts of memory processing and systems-level consolidation.

Reminders activate the prefrontal‐medial temporal cortex and attenuate forgetting of event memory

“…PLS does not assume a particular shape to the HRF, so the results are not biased by assuming a similar shape to the HRF across regions. Despite the sluggish HRF, our finding on the time course of prefrontal cortex preceding the hippocampus during reminder processing was motivated by, and is consistent with, these previous studies investigating how prefrontal-hippocampal networks dynamically interact to support retrieval (Barry et al, 2019;Fuentemilla et al, 2014;McCormick et al, 2020;St. Jacques, Conway, et al, 2011;St.…”

“…St. Jacques, Conway, et al (2011) and St. Jacques, Kragel, & Rubin (2011) found that the medial prefrontal cortex is strongly engaged during both early memory construction and the subsequent elaboration phase, whereas the medial temporal lobe comes online more strongly during the elaboration phase. A comparable pattern of results was obtained by McCormick et al (2020) using MEG that affords greater temporal resolution than fMRI. In their study on retrieval of autobiographical memories acquired between 1 month to 5 years ago, vmPFC activation reached a peak at about 125 ms after initiation of retrieval, which preceded that of the hippocampus by 65 ms, for all but the most recent memories.…”

“…(Moscovitch, 1989(Moscovitch, , 1992Burgess & Shallice, 1996;Moscovitch & Winocur, 2002;Gilboa, Winocur, et al, 2006;Gilboa, Alain, et al, 2006), Examining retrieval data from confabulation patients with vmPFC lesions, Moscovitch and Melo (1997) noted that the most prominent deficit in retrieving old autobiographical and historical memories to verbal cues was failure to recover any memory at all, indicative of the crucial role that vmPFC played in initiating retrieval and guiding search (see also Schnider, 2013;Gilboa & Moscovitch, 2017;Gilboa & Marlatte, 2017; see also work on frontal involvement in "retrieval mode", Tulving, 1983;Lepage, Ghaffar, Nyberg, & Tulving, 2000;Tarder-Stoll, Jayakumar, Dimsdale-Zucker, Günseli, & Aly, 2020). The data from the current study, and from that of McCormick et al (2020) suggest that the temporal sequence of PFC-hippocampal activations can vary by the age of the memory and by reminders, but the underlying factors that influence it have yet to be determined.…”

“…Several studies seeking to identify how the prefrontalhippocampal networks dynamically interact to support retrieval have found that vPFC activity often precedes hippocampal activity during episodic memory retrieval, although it remains unclear what each region functionally contributes to the retrieval process (Barry et al, 2019;Fuentemilla, Barnes, Düzel, & Levine, 2014;McCormick et al, 2020). To investigate the temporal pattern of activity supporting cued reminders and retrieval of complex event memory, we asked if viewing a partial screenshot reminder of a previously encoded film clip activates, in a time-dependent manner, memory for the perceptual elements of the event.…”

“…The dramatic decline in recollection of the perceptual/peripheral details was accompanied by a decline in posterior hippocampal activity, but continued activation of anterior hippocampus after 7 days. When the week‐old memories for the film clips were recalled with a high degree of vividness, however, robust anterior and posterior hippocampal activity was observed, suggesting that the hippocampus continues to support the retrieval of perceptually detailed memory over time (Barry, Barnes, Clark, & Maguire, 2019; Bonnici et al, 2012; McCormick, Barry, Jafarian, Barnes, & Maguire, 2020; Sekeres, Winocur, & Moscovitch, 2018; Sheldon & Levine, 2018).…”