Functional and effective hippocampal-neocortical connectivity during construction and elaboration of autobiographical memory retrieval

Abstract

Autobiographical memory (AM) provides the opportunity to study interactions among brain areas that support the search for a specific episodic memory (construction), and the later experience of mentally reliving it (elaboration). While the hippocampus supports both construction and elaboration, it is unclear how hippocampal-neocortical connectivity differs between these stages, and how this connectivity involves the anterior and posterior segments of the hippocampus, as these have been considered to support the retrieval of general concepts and recollection processes, respectively. We acquired fMRI data in 18 healthy participants during an AM retrieval task in which participants were asked to access a specific AM (construction) and then to recollect it by recovering as many episodic details as possible (elaboration). Using multivariate analytic techniques, we examined changes in functional and effective connectivity of hippocampal-neocortical interactions during these phases of AM retrieval. We found that the left anterior hippocampus interacted with frontal areas during construction and bilateral posterior hippocampi with visual perceptual areas during elaboration, indicating key roles for both hippocampi in coordinating transient neocortical networks at both AM stages. Our findings demonstrate the importance of direct interrogation of hippocampal-neocortical interactions to better illuminate the neural dynamics underlying complex cognitive tasks such as AM retrieval.

Keywords: anterior and posterior hippocampus; episodic memory; fMRI; partial least squares; structural equation modeling.

Figure 1.

Temporal characteristics of hippocampal activation during AM retrieval. (A) Hippocampal activation (slice number: y = −10) in red across 7 lags (=14 s) that showed a greater bootstrap ratio (BSR) than 3.0 and a cluster size of >10 contiguous voxels. Activation is displayed on a T₁-weighted MRI. (B) Percent signal change for the left (lHC, MNI: −20 −10 −22; peak in lag 2) and right (rHC, MNI: 26 −16 −18; peak in lag 3) hippocampus during AM retrieval (memory) and the control task (math).

Figure 2.

Functional hippocampal–neocortical networks during AM retrieval. Functional connectivity between the hippocampal seed (lHC, MNI: −20 −10 −22) and other brain regions during construction (= lag 2) and elaboration (= lag 6) displayed on a rendered T₁-weigthed MRI. BSR > 2.0 and clusters of more than 5 contiguous voxels were considered significant.

Figure 3.

Location of SEM nodes and correlation to the seed. In addition to the seed voxel in the ant lHC, 10 regions were included in the following SEM analysis. For clarity, individual clusters are displayed separately on a T₁-weighted MRI. The functional connectivity (correlation coefficient, r) between the seed and the peak voxel of the cluster during construction (Con; lag 2) and elaboration (Ela; lag 6) is shown underneath each region.

Figure 4.

Effective hippocampal–neocortical networks during AM retrieval. Red arrows represent positive (solid) or negative (dashed) effective connections that differed between construction and elaboration, white arrows represent anatomical connections that were included in the model but did not differ between both AM retrieval processes. The thickness of the arrows indicates the strength of the influence from one region to the other (path coefficient).