Evidence supporting a time-limited hippocampal role in retrieving autobiographical memories

Abstract

The necessity of the human hippocampus for remote autobiographical recall remains fiercely debated. The standard model of consolidation predicts a time-limited role for the hippocampus, but the competing multiple trace/trace transformation theories posit indefinite involvement. Lesion evidence remains inconclusive, and the inferences one can draw from functional MRI (fMRI) have been limited by reliance on covert (silent) recall, which obscures dynamic, moment-to-moment content of retrieved memories. Here, we capitalized on advances in fMRI denoising to employ overtly spoken recall. Forty participants retrieved recent and remote memories, describing each for approximately 2 min. Details associated with each memory were identified and modeled in the fMRI time-series data using a variant of the Autobiographical Interview procedure, and activity associated with the recall of recent and remote memories was then compared. Posterior hippocampal regions exhibited temporally graded activity patterns (recent events > remote events), as did several regions of frontal and parietal cortex. Consistent with predictions of the standard model, recall-related hippocampal activity differed from a non-autobiographical control task only for recent, and not remote, events. Task-based connectivity between posterior hippocampal regions and others associated with mental scene construction also exhibited a temporal gradient, with greater connectivity accompanying the recall of recent events. These findings support predictions of the standard model of consolidation and demonstrate the potential benefits of overt recall in neuroimaging experiments.

A comparison of single and multi-echo processing of fMRI data during overt autobiographical recall

“…Consistent with a prior report using these data (Gilmore et al, 2021a), there was a single 2-way interaction of subregion and temporal distance, F(1,39) = 10.87, p = .002, reflecting different patterns of activity observed in anterior and posterior hippocampal subregions as a function of event recency (other 2-way interaction ps ≥ .138). However, and critically, this interaction must be qualified by a 3-way interaction among the factors of pipeline, subregion, and temporal distance, F(2,78) = 4.48, p = .041, (other 3-way interaction ps ≥ .305).…”

“…In this report, the practical benefits of ME-ICA processing are assessed using a recently acquired naturalistic dataset intended to study human memory function (Gilmore et al, 2021a).…”

“…At the same time, multi-echo acquisitions increase data processing complexity and may incur a cost to the temporal and spatial resolution of the acquired data. Here, we re-examine a multi-echo dataset (Gilmore et al, 2021a) analyzed using multi-echo ICA (ME-ICA) and focused on hippocampal activity during the overly spoken recall of recent and remote autobiographical memories. The goal of the present series of analyses was to determine if ME-ICA's theoretical denoising benefits might lead to a practical difference in the overall conclusions reached.…”

No consolidation without representation: Correspondence between neural and psychological representations in recent and remote memory

“…To date, all the neuroimaging studies on autobiographical memory had participants either answer true/false questions or mentally relive the events while being scanned, followed by production of narratives offline that were scored for details. Capitalizing on advances in fMRI denoising, Gilmore et al (2021) had participants narrate memories acquired on the day of scanning to those acquired months to years earlier while they were in the scanner. Compared to a control condition, they found a decline in posterior hippocampal activation over that period accompanied by a comparable decline in functional connectivity between the posterior hippocampus and neocortical regions implicated in memory.…”

Systems consolidation, transformation and reorganization: Multiple Trace Theory, Trace Transformation Theory and their Competitors

“…To date, all the neuroimaging studies on autobiographical memory had participants either answer true-false questions or mentally relive the events while being scanned, followed by extensive off-line narratives which were scored for details. Capitalizing on advances in fMRI denoising, Gilmore et al (2021) had participants narrate memories acquired on the day of scanning to those acquired 5-10 years earlier. Compared to a control condition, they found a decline in posterior hippocampal activation accompanied over that period accompanied by a comparable decline in functional connectivity between the hippocampus and neocortical regions implicated in memory.…”