Transversal functional connectivity and scene-specific processing in the human entorhinal-hippocampal circuitry

Abstract

Scene and object information reach the entorhinal-hippocampal circuitry in partly segregated cortical processing streams. Converging evidence suggests that such information-specific streams organize the cortical - entorhinal interaction and the circuitry's inner communication along the transversal axis of hippocampal subiculum and CA1. Here, we leveraged ultra-high field functional imaging and advance Maass, Berron et al. (2015) who report two functional routes segregating the entorhinal cortex (EC) and the subiculum. We identify entorhinal subregions based on preferential functional connectivity with perirhinal Area 35 and 36, parahippocampal and retrosplenial cortical sources (referred to as ECArea35-based, ECArea36-based, ECPHC-based, ECRSC-based, respectively). Our data show specific scene processing in the functionally connected ECPHC-based and distal subiculum. Another route, that functionally connects the ECArea35-based and a newly identified ECRSC-based with the subiculum/CA1 border, however, shows no selectivity between object and scene conditions. Our results are consistent with transversal information-specific pathways in the human entorhinal-hippocampal circuitry, with anatomically organized convergence of cortical processing streams and a unique route for scene information. Our study thus further characterizes the functional organization of this circuitry and its information-specific role in memory function.

New insights into anatomical connectivity along the anterior–posterior axis of the human hippocampus using in vivo quantitative fibre tracking

“…For example, the anterior medial clusters of high endpoint density observed in this study appear to extend across the distal subiculum and proximal presubiculum and lateral clusters appear to extend across the proximal subiculum and distal CA1. This mirrors recent observations in the functional literature that suggest functional clusters also extend across classically defined subfield boundaries ( Dalton et al, 2019a ; Grande et al, 2022 ). Indeed, more fine-grained segmentation can reveal that results, initially attributed to a specific subfield, may actually be driven by a specific subportion within that subfield ( Dalton et al, 2019a ).…”

Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T

“…Extending this work to human data, a recent study from Dalton et al (2022) applied tract density mapping to diffusion MRI data, and found that areas of high tract endpoint density tended to extend across classical subfield boundaries (e.g., across the distal subiculum-proximal presubiculum border, and across proximal subiculum and distal CA1 border). This finding also resonates with functional connectivity studies that show long- and transverse-axis gradients of scene selectivity, not only within entorhinal cortex, but also subicular complex (Grande et al, 2022; Maass et al, 2015; Navarro Schröder et al, 2015; see also Schultz, Sommer & Peters, 2015). Overall, therefore, scene selectivity is likely to be distributed across, and vary within, the borders of cytoarchitecturally defined subfields – a pattern that anatomically-defined subfield ROI-based analyses cannot capture without drawing arbitrary sub-divisions (e.g., splitting subicular complex into medial and lateral components in Hodgetts et al, 2017).…”

“…Extending this work to human data, a recent study from Dalton et al (2022) applied tract density mapping to diffusion MRI data, and found that areas of high tract endpoint density tended to extend across classical subfield boundaries (e.g., across the distal subiculumproximal presubiculum border, and across proximal subiculum and distal CA1 border). This finding also resonates with functional connectivity studies that show long-and transverse-axis gradients of scene selectivity, not only within entorhinal cortex, but also subicular complex (Grande et al, 2022;Maass et al, 2015;Navarro Schröder et al, 2015; see also Schultz, Sommer & Peters, 2015 ).…”

“…Unlike the putative spatially modulated circuit, this is proposed to carry face/object information (Dalton & Maguire, 2017, Dalton et al, 2018) due to direct links with the perirhinal cortex (PRC; Insausti and Muñoz, 2001), which is critical to performance of face oddity judgement tasks (Lee et al, 2005; Berhmann et al, 2016). These parallel scene and face/object processing streams are also apparent in the entorhinal cortex; human functional connectivity work has shown PRC- and PHC-preferential functional connectivity with anterior-lateral and posterior-medial entorhinal cortex, respectively which, in turn, show different connectivities with lateral subicular complex (and CA1 border) and medial subicular complex (Grande et al, 2022; Maass et al, 2015). It may be possible, therefore, that more sensitive approaches (e.g., MVPA) can identify patterns of activity that are sensitive to face-related information during visual perception, particularly in more lateral parts of the hippocampal formation, thus revealing two parallel processing streams for different information categories, converging in different locations of the hippocampus.…”

A combined DTI-fMRI approach for optimizing the delineation of posteromedial vs. anterolateral entorhinal cortex

“…Note however, that our results could be influenced by the low number of seed regions used. Connectivity from the EC to even more brain regions should be investigated to more accurately map the topography of connections, as different regions might be structurally and/or functionally connected with distinct subparts of MEC and LEC (Grande et al, 2022; Witter and Amaral, 2021; Witter et al, 2017).…”