Dynamic internal states shape memory retrieval

Abstract

Why do we sometimes easily retrieve memories, but other times appear to forget them? We often look to our external environment for retrieval cues, but another way to optimize memory retrieval is to be in a mental state, or mode, that prioritizes access to our internal representation of the world. Such a ‘retrieval mode’ was proposed by Endel Tulving (1983), who considered it a neurocognitive state in which one keeps the goal of memory retrieval in mind. Building on Tulving’s proposal, we review converging evidence from multiple lines of research that emphasize the importance of internal states in the instantiation of retrieval modes that optimize successful remembering. We identify three key factors that contribute to a retrieval mode by modulating either the likelihood or the content of retrieval: (1) an intention to remember or forget (either in the present or the future), (2) attentional selection of goal-relevant memories and suppression of distractors, and (3) fluctuating levels of acetylcholine in the hippocampus. We discuss empirical evidence that these internal states individually influence memory retrieval and propose how they may interact synergistically. Characterizing these dynamic internal factors is an important key for unlocking our understanding of the organization and accessibility of our memories.

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

“…These findings are consistent with earlier models of PFChippocampal activations during retrieval which posited that frontal cortex guided memory search to enable hippocampally-mediated recovery of memory. (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.…”

Prediction Errors Disrupt Hippocampal Representations and Update Episodic Memories

“…Past studies have suggested that either cholinergic (27–29, 35–37, 60) or dopaminergic (16, 24, 61) modulation could regulate hippocampal function after prediction errors, such as by enhancing plasticity and switching between processing modes. However, mixed evidence supporting both hypotheses has left the question unresolved (25, 26, 31, 33, 34). Here, we investigated whether activation of the basal forebrain or the VTA could explain the relationship between hippocampal activation after prediction error and subsequent memory.…”

“…Past studies have suggested that either cholinergic (27-29, 41-43, 52) or dopaminergic (16,24,53) modulation could regulate hippocampal processing after prediction errors. However, mixed evidence supporting both hypotheses has left the question unresolved (25,26,31,37,40).…”

“…Several models have proposed that acetylcholine from the medial septum (within the basal forebrain) regulates the balance between input and output pathways in the hippocampus (27)(28)(29)(41)(42)(43)(44), thus allowing stored memories to be compared with perceptual input (31,44,45). After prediction errors, acetylcholine release could change hippocampal processing and enhance encoding or memory updating (26,29,40,43,45). On the other hand, dopamine released from the ventral tegmental area (VTA), if transmitted to the hippocampus, could also modulate hippocampal plasticity after prediction errors.…”

“…Neuromodulation may be a critical factor that regulates hippocampal processing and enables memory updating. Currently, there is mixed evidence supporting two hypotheses: acetylcholine and/or dopamine could act upon the hippocampus to regulate processing after surprising events (24–27, 29, 31, 33, 34). Several models have proposed that acetylcholine from the medial septum (within the basal forebrain) regulates the balance between input and output pathways in the hippocampus (27–29, 35–38), thus allowing stored memories to be compared with perceptual input (31, 38, 39).…”