Evidence for an anterior–posterior differentiation in the human hippocampal formation revealed by meta-analytic parcellation of fMRI coordinate maps: Focus on the subiculum

Abstract

Previous studies, predominantly in experimental animals, have suggested the presence of a differentiation of function across the hippocampal formation. In rodents, ventral regions are thought to be involved in emotional behavior while dorsal regions mediate cognitive or spatial processes. Using a combination of modeling the co-occurrence of significant activations across thousands of neuroimaging experiments and subsequent data-driven clustering of these data we were able to provide evidence of distinct subregions within a region corresponding to the human subiculum, a critical hub within the hippocampal formation. This connectivity-based model consists of a bilateral anterior region, as well as separate posterior and intermediate regions on each hemisphere. Functional connectivity assessed both by meta-analytic and resting fMRI approaches revealed that more anterior regions were more strongly connected to the default mode network, and more posterior regions were more strongly connected to ‘task positive’ regions. In addition, our analysis revealed that the anterior subregion was functionally connected to the ventral striatum, midbrain and amygdala, a circuit that is central to models of stress and motivated behavior. Analysis of a behavioral taxonomy provided evidence for a role for each subregion in mnemonic processing, as well as implication of the anterior subregion in emotional and visual processing and the right posterior subregion in reward processing. These findings lend support to models which posit anterior-posterior differentiation of function within the human hippocampal formation and complement other early steps toward a comparative (cross-species) model of the region.

Knowing what from where: Hippocampal connectivity with temporoparietal cortex at rest is linked to individual differences in semantic and topographic memory

“…Consistent with a graded view of hippocampal function (Strange et al, 2014;Ranganath & Ritchey, 2012;Chase et al, 2015), we found that changes in the anterior-posterior and leftright connectivity within the human HC was related to differences in both connectivity and had a unique relationship to different aspects of memory. Anterior hippocampus showed stronger connectivity with inferior frontal and lateral temporal cortex: meta-analytic decoding revealed functional labels including emotion, sensori-motor and autobiographical memory.…”

“…Horner, Bisby, Bush, Lin, & Burgess, 2015). It is increasingly recognised that differences in connectivity along the posterior-anterior axis of the hippocampus could give rise to functional specialisation (Poppenk, Evensmoen, Moscovitch, & Nadel, 2013;Strange, Witter, Lein, & Moser, 2014;Ranganath & Ritchey, 2012;Chase et al, 2015). For example, connections from the posterior hippocampus to occipital and parietal regions provide perceptual information about objects and places (Nadel & Peterson, 2013;Bird & Burgess, 2008;Hassabis & Maguire, 2011).…”

Topographic separation of fornical fibers associated with the anterior and posterior hippocampus in the human brain: An MRI‐diffusion study

“…Nevertheless, it is most likely that the MRI signals principally reflect the topography of hippocampal efferents as the reciprocal afferent fibers are far less numerous within the tract (Saunders & Aggleton, 2007). These hippocampal efferents principally arise from the CA fields and the subicular cortices (Chase et al., 2015; Saunders & Aggleton, 2007). For this reason it can be inferred that the more lateral fornix fibers preferentially innervate targets like the prefrontal cortex, nucleus accumbens, and the anteromedial thalamic nucleus, as in every instance the anterior hippocampus provides the most numerous inputs to these sites (Aggleton, Wright, Rosene, & Saunders, 2015; Barbas & Blatt, 1995; Chase et al., 2015; Christiansen, Dillingham, et al., 2016).…”

“…These hippocampal efferents principally arise from the CA fields and the subicular cortices (Chase et al., 2015; Saunders & Aggleton, 2007). For this reason it can be inferred that the more lateral fornix fibers preferentially innervate targets like the prefrontal cortex, nucleus accumbens, and the anteromedial thalamic nucleus, as in every instance the anterior hippocampus provides the most numerous inputs to these sites (Aggleton, Wright, Rosene, & Saunders, 2015; Barbas & Blatt, 1995; Chase et al., 2015; Christiansen, Dillingham, et al., 2016). In contrast, more posterior hippocampal projections in the fornix include the dense inputs to the mammillary bodies (Christiansen, Dillingham, et al., 2016).…”

“…Of the two areas, the anterior hippocampus has been more linked to stress, anxiety, and emotional processing (Bannerman et al., 1999; Chase et al., 2015; O'Mara, 2005), whereas the posterior hippocampus is more typically linked to fine‐grain spatial processing (Poppenk et al., 2013; Strange et al., 2014). These differences do not, however, reflect a dichotomy, rather a gradation of change along the anterior–posterior axis (Collin et al., 2015; Poppenk et al., 2013; Strange et al., 2014).…”