Going Their Separate Ways: Dissociation of Hippocampal and Dorsolateral Prefrontal Activation during Episodic Retrieval and Post-retrieval Processing

Abstract

Hippocampal activity is modulated during episodic memory retrieval. Most consistently, a relative increase in activity during confident retrieval is observed. Dorsolateral prefrontal cortex (DLPFC) is also activated during retrieval, but may be more generally activated during cognitive-control processes. The "default network," regions activated during rest or internally focused tasks, includes the hippocampus, but not DLPFC. Therefore, DLPFC and the hippocampus should diverge during difficult tasks suppressing the default network. It is unclear, however, whether a difficult episodic memory retrieval task would suppress the default network due to difficulty or activate it due to internally directed attention. We hypothesized that a task requiring episodic retrieval followed by rumination on the retrieved item would increase DLPFC activity, but paradoxically reduce hippocampal activity due to concomitant suppression of the default network. In the present study, blocked and event-related fMRI were used to examine hippocampal activity during episodic memory recollection and postretrieval processing of paired associates. Subjects were asked to make living/nonliving judgments about items visually presented (classify) or items retrieved from memory (recall-classify). Active and passive baselines were used to differentiate task-related activity from default-network activity. During the "recall-classify" task, anterior hippocampal activity was selectively reduced relative to "classify" and baseline tasks, and this activity was inversely correlated with DLPFC. Reaction time was positively correlated with DLPFC activation and default-network/hippocampal suppression. The findings demonstrate that frontal and hippocampal activity are dissociated during difficult episodic retrieval tasks and reveal important considerations for interpreting hippocampal activity associated with successful episodic retrieval.

Search-Related Suppression of Hippocampus and Default Network Activity during Associative Memory Retrieval

“…Event-related fMRI was used to investigate BOLD responses during cued recall and post-retrieval processing of previously studied word pairs relative to a non-memory classification task. Consistent with prior evidence of hippocampal deactivation during elaborative associative recall of paired visual objects (Israel et al, 2010), results confirmed that hippocampal deactivation occurs during elaborative associative recall of paired words, allowing further isolation and examination of the factors that modulate this suppression. To investigate the neural correlates underlying retrieval-related components of memory search, successful retrieval, and post-retrieval processing, we examined task conditions that had different levels of each.…”

“…Task-related deactivation, such as that seen in default network regions, might also explain relative signal differences in the hippocampus. A prior study demonstrated robust hippocampal deactivation during cued recall and post-retrieval processing of visual paired associates (Israel et al, 2010), described as “elaborative associative recall.” Externally directed thought and task difficulty are known to deactivate the default network (Greicius et al, 2003b; McKiernan et al, 2003; Vincent et al, 2008), and maintenance of an item in working memory can suppress hippocampal activity (Axmacher et al, 2007). It is therefore possible that either directed search effort prior to retrieval or post-retrieval working memory processing is a primary mediator of hippocampal activity during memory retrieval, rather than the retrieval event, itself.…”

Retrieval Search and Strength Evoke Dissociable Brain Activity during Episodic Memory Recall

“…In this study, although the hippocampal response during successful recall was below threshold, the hippocampal response during failed recall was robustly deactivated, consistent with Reas et al (2011). Despite evidence for default network activations during memory retrieval, which are generally attributed to autobiographical or self-referential task conditions (Spreng & Grady, 2010; Maguire, 2001; Andreasen et al, 1995), these results provide further evidence for task-negative responses in these regions during effortful episodic memory retrieval (Gimbel & Brewer, 2011; Israel, Seibert, Black, & Brewer, 2010), which may be driven by mental search processes (Reas et al, 2011). Furthermore, they expand on prior studies, which did not simultaneously assess effects of search and associative memory strength, to reveal that default network deactivations are more likely attributable to search than retrieval strength differences.…”

Negative BOLD Response in the Hippocampus during Short-term Spatial Memory Retrieval

“…Furthermore, it is noteworthy that several of the studies demonstrating hippocampal deactivations in arguably hippocampusrelevant conditions reported worse behavioral performance in that particular condition (Lambrey et al, 2012;Rodriguez, 2010;Shipman & Astur, 2008;Rekkas et al, 2005). However, the coupling of the hippocampus with other default regions during memory retrieval appears to vary according to task condition Huijbers, Pennartz, Cabeza, & Daselaar, 2011;Reas et al, 2011), which indicates that the areas deactivated during memory retrieval may only partially overlap with those deactivated during nonmemory tasks (Israel, Seibert, Black, & Brewer, 2010). In relation to this, although the more difficult EC condition was associated with deactivations in default regions such as the medial pFC, the posterior cingulate cortex, and the inferior parietal lobule, it was associated with strong activations in another default region, the retrosplenial cortex (Buckner, Andrews-Hanna, & Schacter, 2008).…”