Preston P. Thakral

A role for the left angular gyrus in episodic simulation and memory

Functional magnetic resonance imaging (fMRI) studies indicate that episodic simulation (i.e., imagining specific future experiences) and episodic memory (i.e., remembering specific past experiences) are associated with enhanced activity in a common set of neural regions referred to as the core network. This network comprises the hippocampus, medial prefrontal cortex, and left angular gyrus, among other regions. Because fMRI data are correlational, it is unknown whether activity increases in core network regions are critical for episodic simulation and episodic memory. In the current study, we used MRI-guided transcranial magnetic stimulation (TMS) to assess whether temporary disruption of the left angular gyrus would impair both episodic simulation and memory (16 participants, 10 females). Relative to TMS to a control site (vertex), disruption of the left angular gyrus significantly reduced the number of internal (i.e., episodic) details produced during the simulation and memory tasks, with a concomitant increase in external detail production (i.e., semantic, repetitive, or off-topic information), reflected by a significant detail by TMS site interaction. Difficulty in the simulation and memory tasks also increased after TMS to the left angular gyrus relative to the vertex. In contrast, performance in a nonepisodic control task did not differ statistically as a function of TMS site (i.e., number of free associates produced or difficulty in performing the free associate task). Together, these results are the first to demonstrate that the left angular gyrus is critical for both episodic simulation and episodic memory. SIGNIFICANCE STATEMENT Humans have the ability to imagine future episodes (i.e., episodic simulation) and remember episodes from the past (i.e., episodic memory). A wealth of neuroimaging studies have revealed that these abilities are associated with enhanced activity in a core network of neural regions, including the hippocampus, medial prefrontal cortex, and left angular gyrus. However, neuroimaging data are correlational and do not tell us whether core regions support critical processes for simulation and memory. In the current study, we used transcranial magnetic stimulation and demonstrated that temporary disruption of the left angular gyrus leads to impairments in simulation and memory. The present study provides the first causal evidence to indicate that this region is critical for these fundamental abilities.

Imagining the future: The core episodic simulation network dissociates as a function of timecourse and the amount of simulated information

Neuroimaging data indicate that episodic memory (i.e., remembering specific past experiences) and episodic simulation (i.e., imagining specific future experiences) are associated with enhanced activity in a common set of neural regions, often referred to as the core network. This network comprises the hippocampus, parahippocampal cortex, lateral and medial parietal cortex, lateral temporal cortex, and medial prefrontal cortex. Evidence for a core network has been taken as support for the idea that episodic memory and episodic simulation are supported by common processes. Much remains to be learned about how specific core network regions contribute to specific aspects of episodic simulation. Prior neuroimaging studies of episodic memory indicate that certain regions within the core network are differentially sensitive to the amount of information recollected (e.g., the left lateral parietal cortex). In addition, certain core network regions dissociate as a function of their timecourse of engagement during episodic memory (e.g., transient activity in the posterior hippocampus and sustained activity in the left lateral parietal cortex). In the current study, we assessed whether similar dissociations could be observed during episodic simulation. We found that the left lateral parietal cortex modulates as a function of the amount of simulated details. Of particular interest, while the hippocampus was insensitive to the amount of simulated details, we observed a temporal dissociation within the hippocampus: transient activity occurred in relatively posterior portions of the hippocampus and sustained activity occurred in anterior portions. Because the posterior hippocampal and lateral parietal findings parallel those observed during episodic memory, the present results add to the evidence that episodic memory and episodic simulation are supported by common processes. Critically, the present study also provides evidence that regions within the core network support dissociable processes.

An attention account of neural priming.

ABSTRACT Repetition priming of familiar stimuli (e.g., objects) produces a decrease in visual cortical activity for repeated versus novel items, which has been attributed to more fluent processing for repeated items. By contrast, priming of unfamiliar stimuli (e.g., abstract shapes) produces an increase in visual cortical activity. The mechanism for priming-related increases in activity for repeated unfamiliar stimuli is unknown. We hypothesised that such increases in activity may reflect attentional allocation to these items. We tested this hypothesis using a priming-spatial attention paradigm. During Phase 1 of Experiment 1, participants viewed unfamiliar abstract shapes and familiar objects. During Phase 2, participants identified target letters (S or H). Each target letter was preceded by a non-informative shape or object cue that was repeated (from Phase 1) or novel in the same (valid) or opposite (invalid) hemifield. In Experiment 2, we manipulated shape familiarity by presenting shapes once or six times during Phase 1. For both experiments, at valid locations, target identification accuracy was higher following repeated versus novel unfamiliar item cues and lower following repeated versus novel familiar item cues. These findings support our hypothesis that priming-related increases in visual cortical activity for repeated unfamiliar items may, in part, reflect attentional allocation.

Characterizing the role of the hippocampus during episodic simulation and encoding

The hippocampus has been consistently associated with episodic simulation (i.e., the mental construction of a possible future episode). In a recent study, we identified an anterior‐posterior temporal dissociation within the hippocampus during simulation. Specifically, transient simulation‐related activity occurred in relatively posterior portions of the hippocampus and sustained activity occurred in anterior portions. In line with previous theoretical proposals of hippocampal function during simulation, the posterior hippocampal activity was interpreted as reflecting a transient retrieval process for the episodic details necessary to construct an episode. In contrast, the sustained anterior hippocampal activity was interpreted as reflecting the continual recruitment of encoding and/or relational processing associated with a simulation. In the present study, we provide a direct test of these interpretations by conducting a subsequent memory analysis of our previously published data to assess whether successful encoding during episodic simulation is associated with the anterior hippocampus. Analyses revealed a subsequent memory effect (i.e., later remembered > later forgotten simulations) in the anterior hippocampus. The subsequent memory effect was transient and not sustained. Taken together, the current findings provide further support for a component process model of hippocampal function during simulation. That is, unique regions of the hippocampus support dissociable processes during simulation, which include the transient retrieval of episodic information, the sustained binding of such information into a coherent episode, and the transient encoding of that episode for later retrieval.

Increased hippocampus to ventromedial prefrontal connectivity during the construction of episodic future events

Both the hippocampus and ventromedial prefrontal cortex (vmPFC) appear to be critical for episodic future simulation. Damage to either structure affects ones ability to remember the past and imagine the future, and both structures are commonly activated as part of a wider core network during future simulation. However, the precise role played by each of these structures and, indeed, the direction of information flow between them during episodic simulation, is still not well understood. In this study, we scanned participants using functional magnetic resonance imaging while they imagined future events in response to object cues. We then used dynamic causal modeling to examine effective connectivity between the left anterior hippocampus and vmPFC during the initial mental construction of the events. Our results show that while there is strong bidirectional intrinsic connectivity between these regions (i.e., irrespective of task conditions), only the hippocampus to vmPFC connection increases during the construction of episodic future events, suggesting that the hippocampus initiates event simulation in response to retrieval cues, driving activation in the vmPFC where episodic details may be further integrated.

Content-specific phenomenological similarity between episodic memory and simulation

ABSTRACT Numerous studies have indicated that remembering specific past experiences (i.e., episodic memory) and imagining specific novel future experiences (i.e., episodic simulation) are supported by common mental processes. An open question, however, is whether and to what extent the content of specific past episodes is sampled when simulating a specific future episode. The current study aimed to answer this question. Participants recalled past episodes each comprising two episodic details, a personally familiar location and person. Participants also simulated novel future episodes using recombined pairs of person and location details taken from different recalled episodes. Participants rated the vividness of each location and person in their memory and simulation. We conducted a multi-level analysis where the vividness rating during memory was used to predict the vividness rating during simulation at the level of individual shared details (i.e., location or person). The vividness of the memorial detail co-varied with the vividness of the simulated detail; this relationship persisted even after accounting for the underlying familiarity of the details. These findings strongly suggest that simulations of specific future experiences are based upon the contents of specific prior episodes.

Core Network Contributions to Remembering the Past, Imagining the Future, and Thinking Creatively

The core network refers to a set of neural regions that have been consistently associated with episodic memory retrieval and episodic future simulation. This network is thought to support the constructive thought processes that allow the retrieval and flexible combination of stored information to reconstruct past and construct novel future experiences. Recent behavioral research points to an overlap between these constructive processes and those also engaged during divergent thinking—the ability to think creatively and generate novel ideas—but the extent to which they involve common neural correlates remains unclear. Using fMRI, we sought to address this question by assessing brain activity as participants recalled past experiences, simulated future experiences, or engaged in divergent thinking. Consistent with past work, we found that episodic retrieval and future simulation activated the core network compared with a semantic control condition. Critically, a triple conjunction of episodic retrieval, future simulation, and divergent thinking revealed common engagement of core network regions, including the bilateral hippocampus and parahippocampal gyrus, as well as other regions involved in memory retrieval (inferior frontal gyrus) and mental imagery (middle occipital gyrus). The results provide further insight into the roles of the hippocampus and the core network in episodic memory retrieval, future simulation, and divergent thinking and extend recent work highlighting the involvement of constructive episodic processes in creative cognition.

Transcranial magnetic stimulation of the left angular gyrus during encoding does not impair associative memory performance

ABSTRACT The left angular gyrus (AG) is thought to play a critical role in episodic retrieval and has been implicated in the recollection of specific details of prior episodes. Motivated by recent fMRI studies in which it was reported that elevated neural activity in left AG during study is predictive of subsequent associative memory, the present study investigated whether the region plays a causal role in associative memory encoding. Participants underwent online transcranial magnetic stimulation (TMS) while encoding word pairs prior to an associative memory test. We predicted that TMS to left AG during encoding would result in reduced subsequent memory accuracy, especially for estimates of recollection. The results did not support this prediction: estimates of both recollection and familiarity-driven recognition were essentially identical for words pairs encoded during TMS to left AG relative to a vertex control site. These results suggest that the left AG may not play a necessary role in associative memory encoding. TMS to left AG did however affect confidence for incorrect ‘intact’ judgments to rearranged pairs and incorrect ‘rearranged’ judgments to intact pairs. These findings suggest that the left AG supports encoding processes that contribute to aspects of subjective mnemonic experience.