Meta‐analytic and functional connectivity evidence from functional magnetic resonance imaging for an anterior to posterior gradient of function along the hippocampal axis

Abstract

There is considerable evidence from non-human animal studies that the anterior and posterior regions of the hippocampus have different anatomical connections and support different behavioural functions. Although there are some recent human studies using functional magnetic resonance imaging (fMRI) that have addressed this idea directly in the memory and spatial processing domains and provided support for it, there has been no broader meta-analysis of the fMRI literature to determine if there is consistent evidence for functional dissociations in anterior and posterior hippocampus across all of the different cognitive domains in which the hippocampus participates. The purpose of this review is to address this gap in our knowledge using three approaches. One approach involved PubMed searches to identify relevant fMRI papers reporting hippocampal activation during episodic encoding and retrieval, semantic retrieval, working memory, spatial navigation, simulation/scene construction, transitive inference, and social cognition tasks. The second was to use a large meta-analytic database (neurosynth) to find text terms and coactivation maps associated with the anterior and posterior hippocampal regions identified in the literature search. The third approach was to contrast the resting-state functional connectivity of the anterior and posterior hippocampal regions using a publicly available database that includes a large sample of adults. These three approaches provided converging evidence that not only are cognitive processes differently distributed along the hippocampal axis, but there also are distinct areas coactivated and functionally connected with the anterior and posterior segments. This anterior/posterior distinction involving multiple cognitive domains is consistent with the animal literature and provides strong support from fMRI for the idea of functional dissociations across the long axis of the hippocampus. K E Y

Zooming In and Out on One's Life: Autobiographical Representations at Multiple Time Scales

“…represented throughout the cortical hierarchy (Clewett et al, 2019;Cowell et al, 2019;Horner & Doeller, 2017), thereby supporting the mental simulation of specific events or scenes (Mullally & Maguire, 2014;Schacter et al, 2012). The evidence suggests that the longitudinal axis of the hippocampus may in fact provide a gradient of representational granularity, with an anterior-to-posterior gradient of coarse-to-fine grained representations (Brunec, Bellana, et al, 2018;Collin et al, 2015;Grady, 2019). Indeed, work on rodents and humans suggest that the posterior hippocampus (in interaction with posterior neocortical structures) mediates the representation of the perceptual details of events, whereas the anterior hippocampus (in interaction with anterior neocortical structures) mediates the representation of the gist or general context of events (for review, see Sekeres et al, 2018).Thus, the mental simulation of the experiential content and unfolding of specific events may mainly depend on the posterior hippocampus, in interaction with posterior cortical regions, whereas the representation of the essential content of events-their gist or conceptual frame-may mainly depend on the anterior hippocampus (Moscovitch et al, 2016;Poppenk et al, 2013;Sekeres et al, 2018;Sheldon & Levine, 2016).…”

Age‐related alterations in functional connectivity along the longitudinal axis of the hippocampus and its subfields

“…For example, the amygdala projects to the anterior ERC, which then connects with the anterior hippocampus, while visual information is funneled through perirhinal and parahippocampal cortices into the posterior ERC and then to the posterior aspects of the hippocampus. Based on these observations, the theory has been proposed that the posterior extent of the hippocampus (corresponding to the dorsal hippocampus in rodents) is more likely to be involved in memory retrieval, spatial memory and navigation, while the anterior extent may be more involved in stress, emotion, goal‐directed activity, and memory encoding (Bast & Feldon, 2003; Bast, Wilson, Witter, & Morris, 2009; Bienkowski et al, 2018; Fanselow & Dong, 2010; Grady, 2020; Lau et al, 2010; Moser & Moser, 1998; Poppenk, Evensmoen, Moscovitch, & Nadel, 2013). Moreover, the anterior–posterior axis of the hippocampus may interact with two larger cortical systems to support memory‐guided behavior: an anterior temporal system that includes the PRC, lateral orbitofrontal cortex, amygdala, and ventral temporopolar cortex, and a posterior medial system that includes the PHC, retrosplenial cortex, and other “default network” regions (Ranganath & Ritchey, 2012).…”

Longitudinal Differences in Human Hippocampal Connectivity During Episodic Memory Processing

“…2014 ; Strange et al. 2014 ; Grady 2019 ). While this question has mainly been addressed in humans with fMRI, a much wider range of methods has been employed with experimental rodents, including single unit and local field potential recordings.…”