Search-Related Suppression of Hippocampus and Default Network Activity during Associative Memory Retrieval - PubMed (original) (raw)
Search-Related Suppression of Hippocampus and Default Network Activity during Associative Memory Retrieval
Emilie T Reas et al. Front Hum Neurosci. 2011.
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.
Keywords: default network; fMRI; hippocampus; memory; retrieval.
Figures
Figure 1
Experimental design. (A) Prior to scanning, 64 word pairs were presented sequentially and subjects were instructed to memorize each pair. (B) During scanning, trials randomly alternated between classify and recall task conditions. In the classify task, a green box cued subjects to classify the presented word as living or non-living. In the recall task a red box cued subjects to recall and classify the pair of the presented word. (C) In a post-scan recall test, subjects saw one word at a time from each pair and were asked to recall and vocally report the word’s pair.
Figure 2
Strongly remembered minus classify, poorly remembered minus classify, and poorly minus strongly remembered contrasts. Regions with significant BOLD signal differences (p < 0.01) between strongly remembered and classify trials (A), poorly remembered and classify trials (B), and poorly and strongly remembered trials (C). Positive activity differences are displayed in warm colors and negative activity differences are displayed in cool colors. Subtraction maps are overlaid on every five axial slices of an average anatomical image of all subjects. As depicted in Figure 5A, these activation differences are expected to represent processing related to search, retrieval and post-retrieval processing (A,C), or search only (B).
Figure 3
Anterior and posterior hippocampal activity. (A) Left anterior hippocampus showed greater deactivation during strongly and poorly remembered relative to classify trials (right, p < 0.05). Impulse response curves (left) illustrate a graded pattern of deactivation from fixation baseline greatest for poorly remembered (blue), intermediate for strongly remembered (red), and minimal for classify (green) trials. **Indicates poorly remembered < classify, strongly remembered < classify, and poorly remembered < strongly remembered (paired _t_-tests, p < 0.01). (B) Bilateral posterior hippocampus was more active for strongly versus poorly remembered trials (p < 0.05). Impulse response curves reveal late deactivation for poorly remembered trials only. *Indicates poorly remembered < classify and poorly remembered < strongly remembered (paired _t_-tests, p < 0.01). (C) Bilateral hippocampus showed a gradient of decreasing deactivation, from 7.5 to 12.5 s, from anterior to posterior regions. Each hippocampal subregion represents a 4-mm thick slice along the long axis of the hippocampus. Error bars represent SE of the mean. Subtraction maps are overlaid on sagittal (A) and coronal (B) slices of the average anatomical image of all subjects.
Figure 4
Regions fitting the anterior hippocampus response model. Clusters that directly fit the response model (warm colors) or fit the inverse of the response model (cool colors) for the classify, strongly remembered, and poorly remembered conditions are overlaid on the left medial (top left) and lateral (top right) pial surface of the Talairach and Tournoux N27 average brain (p < 0.001). Color intensity represents strength of fit with the anterior hippocampal impulse response model presented in Figure 3A. The average impulse response curves (bottom) from the medial prefrontal cortex (A), posterior cingulate (B), left inferior parietal cortex (C), and left and right temporal pole (D) show decreased activity below fixation baseline for classify (green), followed by greater deactivation for strongly remembered (red), and greatest deactivation for poorly remembered (blue).
Figure 5
Cognitive and neural processing models. (A) The hypothetical cognitive processes involved in an elaborative associative retrieval task, and the magnitude to which each task condition engages these processes, are depicted. The _y_-axis represents arbitrary units measuring degree of engagement. From this model, the following cognitive processes are expected to result from task condition contrasts: If engaged more for strongly remembered than classify, the process(es) might be search, retrieval, or post-retrieval processing; if engaged more for poorly remembered than classify and for poorly than strongly remembered, the process might be search. C, classify; SR, strongly remembered; PR, poorly remembered. (B) Hippocampal activity for each task condition is illustrated, under alternative models for encoding- and recall-mediated responses. Both strongly and poorly remembered trials are hypothesized to reduce encoding-related activity (left). Strongly remembered trials are expected to increase recall-related activity (right). The _x_-axes and _y_-axes are in arbitrary units of time and neural activity, respectively.
References
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