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

Abstract

Episodic memory retrieval involves the coordinated interaction of several cognitive processing stages such as mental search, access to a memory store, associative re-encoding, and post-retrieval monitoring. The neural response during memory retrieval is an integration of signals from multiple regions that may subserve supportive cognitive control, attention, sensory association, encoding, or working memory functions. It is particularly challenging to dissociate contributions of these distinct components to brain responses in regions such as the hippocampus, which lies at the interface between overlapping memory encoding and retrieval, and “default” networks. In the present study, event-related functional magnetic resonance imaging (fMRI) and measures of memory performance were used to differentiate brain responses to memory search from subcomponents of episodic memory retrieval associated with successful recall. During the attempted retrieval of both poorly and strongly remembered word pair associates, the hemodynamic response was negatively deflected below baseline in anterior hippocampus and regions of the default network. Activations in anterior hippocampus were functionally distinct from those in posterior hippocampus and negatively correlated with response times. Thus, relative to the pre-stimulus period, the hippocampus shows reduced activity during intensive engagement in episodic memory search. Such deactivation was most salient during trials that engaged only pre-retrieval search processes in the absence of successful recollection or post-retrieval processing. Implications for interpretation of hippocampal fMRI responses during retrieval are discussed. A model is presented to interpret such activations as representing modulation of encoding-related activity, rather than retrieval-related activity. Engagement in intensive mental search may reduce neural and attentional resources that are otherwise tonically devoted to encoding an individual’s stream of experience into episodic memory.

Portraying the unique contribution of the default mode network to internally driven mnemonic processes

“…Over the past decades, the idea that the hippocampi exclusively support episodic as opposed to semantic memory has been challenged (56), and the contribution of the medial temporal lobe in semantic fluency tasks has gradually become acknowledged (57). The pattern of greater activation during the semantic task is consistent with a recent report of hippocampus suppression during laboratory episodic memory search in humans (58). Hippocampus involvement in the semantic word fluency task can be explained by the type of information retrieved in our study.…”

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

“…In addition, in the case of a functional suppression, one would expect greater suppression to be associated with better performance. Contrary to this, the generally poorer performance in the EC condition relative to the VC condition supports an inverse relationship between the level of negative BOLD signal and performance, similar to the results of Reas et al (2011).…”

“…It is possible that the EC condition, contrary to the prediction, requires a functional suppression of the hippocampus. Such an interpretation was favored by Reas, Gimbel, Hales, and Brewer (2011), who demonstrated a negative BOLD response in the hippocampus during elaborate associative recall, which was greater for poorly remembered than for strongly remembered items. It was argued that the longer memory search accompanying poorly remembered items required a greater suppression of encoding-related activity in the hippocampus, in favor of retrieval-related processes taking place elsewhere.…”

“…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).…”

Adverse Listening Conditions and Memory Load Drive a Common Alpha Oscillatory Network

“…Inhibitory, "top-down" control over task-irrelevant processes and over potentially erroneous behavior is likely to critically depend on the alpha-frequency domain (Klimesch et al, 2007;Jensen and Mazaheri, 2010), within as well as across brain areas. Concomitantly, recent functional imaging studies have pointed out that suppression of BOLD activity (often reported to be anticorrelated with alpha power, Laufs et al, 2003;Sadaghiani et al, 2010) in cingulate areas (i.e., the "default" network, as well as in the TPJ) is pivotal to successful working memory performance (Anticevic et al, 2010(Anticevic et al, , 2011Reas et al, 2011). In line with these studies and an inhibitory function of alpha, we find alpha power in temporoparietal and posterior cingulate areas to be affected by our number of items and acoustic degradation manipulations.…”