The neural dynamics of novel scene imagery

Abstract

41Retrieval of long-term episodic memories is characterised by synchronised neural activity between 42 hippocampus and ventromedial prefrontal cortex (vmPFC), with additional evidence that vmPFC 43 activity leads that of the hippocampus. It has been proposed that the mental generation of scene 44 imagery is a crucial component of episodic memory processing. If this is the case, then a comparable 45 interaction between the two brain regions should exist during the construction of novel scene 46 imagery. To address this question, we leveraged the high temporal resolution of 47 magnetoencephalography (MEG) to investigate the construction of novel mental imagery. We 48 tasked male and female humans with imagining scenes and single isolated objects in response to 49 one-word cues. We performed source level power, coherence and causality analyses to characterise 50 the underlying inter-regional interactions. Both scene and object imagination resulted in theta 51 power changes in the anterior hippocampus. However, higher theta coherence was observed 52 between the hippocampus and vmPFC in the scene compared to the object condition. This inter-53 regional theta coherence also predicted whether or not imagined scenes were subsequently 54 remembered. Dynamic causal modelling of this interaction revealed that vmPFC drove activity in 55 hippocampus during novel scene construction. Additionally, theta power changes in the vmPFC 56 preceded those observed in the hippocampus. These results constitute the first evidence in humans 57 that episodic memory retrieval and scene imagination rely on similar vmPFC-hippocampus neural 58 dynamics. Furthermore, they provide support for theories emphasising similarities between both 59 cognitive processes, and perspectives that propose the vmPFC guides the construction of context-60 relevant representations in the hippocampus. 61 62 63

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

“…The reminder engaged the recollection network which included the hippocampus and vPFC, with vPFC activation preceding peak activity in the right anterior hippocampus. These findings suggest that the reminder's memory‐enhancing effect was mediated by priming prefrontal cortical nodes of the recollection network that are typically engaged during schematic memory retrieval or general event/scene construction, followed by elaborative episodic memory retrieval mediated by the hippocampus (Addis, Knapp, Roberts, & Schacter, 2012; Barry et al, 2019; Holland, Addis, & Kensinger, 2011). Many of the same regions were activated during retrieval itself but there was no difference in hippocampal activation for memories whose retrieval was preceded by a reminder compared to those that were recalled in the absence of a reminder, consistent with our observation that the quality of the memories did not differ from one another.…”

“…Presentation of the reminder cue, which intentionally contained no coherent scene information, activated vlPFC followed by peak activation of the right anterior hippocampus. While the contribution of these regions remains speculative, the vPFC's early activation in response to the visual stimulus and title likely reflects their interaction with one another in the construction of either a mental scene or schematic event (Barry et al, 2019; Gilboa & Marlatte, 2017; Bonasia et al, 2018; McCormick, Ciaramelli, De Luca, & Maguire, 2018; van Kesteren et al, 2013). This output then biases the subsequent activation of the anterior hippocampus and elaboration of coarsely detailed memory for the event (Poppenk, Evensmoen, Moscovitch, & Nadel, 2013; Poppenk & Moscovitch, 2011).…”

“…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).…”

“…Several studies seeking to identify how the prefrontal‐hippocampal 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.…”

Does hippocampal volume explain performance differences on hippocampal-dependant tasks?

“…Neuroimaging studies of healthy individuals performing tasks related to these cognitive functions reliably show engagement of the hippocampus ( Addis et al., 2007 ; Barry et al., 2018 ; Brown et al., 2010 ; Buckner and Carroll, 2007 ; Dalton et al., 2018 ; Spiers and Maguire, 2006 ; Svoboda et al., 2006 ). Moreover, damage to the hippocampus leads to impaired performance on similar tasks (e.g.…”