When the brain, but not the person, remembers: Cortical reinstatement is modulated by retrieval goal in developmental amnesia

Abstract

Developmental amnesia (DA) is associated with early hippocampal damage and subsequent episodic amnesia emerging in childhood alongside age-appropriate development of semantic knowledge. We employed fMRI to assess whether patients with DA show evidence of ‘cortical reinstatement’, a neural correlate of episodic memory, despite their amnesia. At study, 23 participants (5 patients) were presented with words overlaid on a scene or a scrambled image for later recognition. Scene reinstatement was indexed by scene memory effects (greater activity for previously presented words paired with a scene rather than scrambled images) that overlapped with scene perception effects. Patients with DA demonstrated scene reinstatement effects in the parahippocampal and retrosplenial cortex that were equivalent to those shown by healthy controls. Behaviourally, however, patients with DA showed markedly impaired scene memory. The data indicate that reinstatement can occur despite hippocampal damage, but that cortical reinstatement is insufficient to support accurate memory performance. Furthermore, scene reinstatement effects were diminished during a retrieval task in which scene information was not relevant for accurate responding, indicating that strategic mnemonic processes operate normally in DA. The data suggest that cortical reinstatement of trial-specific contextual information is decoupled from the experience of recollection in the presence of severe hippocampal atrophy.

Brain Mechanisms Underlying the Subjective Experience of Remembering

“…Importantly, cortical reactivation has been shown to be mediated by retrievalrelated activity in the hippocampus (Horner et al 2015;Ritchey et al 2013;Treder et al 2021), and its relation to the subjective experience of recollection depends on the integrity of the hippocampus (Elward et al 2021). The features of memory are reactivated in a cohesive manner, with the hippocampus supporting incidental reactivation of non-target associations that have been integrated in memory, consistent with a pattern completion account (Horner et al 2015) (Figure 1C).…”

Using Recognition Testing to Support Semantic Learning in Developmental Amnesia

“…Reactivation and consolidation are thought to be crucially dependent on the hippocampal complex which is severely compromised in patients with DA. However, recent research from our laboratory indicates that patients with DA can reactivate prior events in memory even when that information is unavailable to recall (Elward et al, 2021). This is consistent with several other accounts that have demonstrated that hippocampal processes may not be strictly necessary for reinstatement of a prior event in memory (Gagnon et al, 2018; Thakral et al, 2017).…”

Effects of age on neural reinstatement during memory retrieval

“…This is a potentially important issue given that it is widely held that the hippocampus (and, therefore, hippocampally driven neural reinstatement) plays a much more important role in recollection-driven than familiarity-driven memory judgments (Eichenbaum et al, 2007). It is worth noting, however, that reinstatement effects have sometimes been reported in the absence of behavioral evidence of successful recollection (Elward, et al, 2021;Johnson et al, 2009;Thakral, et al, 2017;Wang, et al, 2016). These findings suggest that while reinstatement might be necessary for recollection, it is not sufficient.…”