Preferential signal pathways during the perception and imagery of familiar scenes: An effective connectivity study

Abstract

The perception and imagery of landmarks activate similar content-dependent brain areas, including occipital and temporo-medial brain regions. However, how these areas interact during visual perception and imagery of scenes, especially when recollecting their spatial location, remains unknown. Here, we combined functional magnetic resonance imaging (fMRI), resting-state functional connectivity (rs-fc), and effective connectivity to assess spontaneous fluctuations and task-induced modulation of signals among regions entailing scene-processing, the primary visual area and the hippocampus (HC), responsible for the retrieval of stored information. First, we functionally defined the scene-selective regions, that is, the occipital place area (OPA), the retrosplenial complex (RSC) and the parahippocampal place area (PPA), by using the face/scene localizer, observing that two portions of the PPA-anterior and posterior PPA-were consistently activated in all subjects. Second, the rs-fc analysis (n = 77) revealed a connectivity pathway similar to the one described in macaques, showing separate connectivity routes linking the anterior PPA with RSC and HC, and the posterior PPA with OPA. Third, we used dynamic causal modelling to evaluate whether the dynamic couplings among these regions differ between perception and imagery of familiar landmarks during a fMRI task (n = 16). We found a positive effect of HC on RSC during the retrieval of imagined places and an effect of occipital regions on both RSC and pPPA during the perception of scenes. Overall, we propose that under similar functional architecture at rest, different neural interactions take place between regions in the occipito-temporal higher-level visual cortex and the HC, subserving scene perception and imagery.

Mapping the functional and structural connectivity of the scene network

“…We began by measuring functional connectivity, during moviewatching and at rest, between the core and extended scene regions (Baldassano et al, 2016;Epstein & Baker, 2019) and early visual regions. In line with previous resting-state studies (Baldassano et al, 2013;Boccia et al, 2017;Nasr et al, 2013;Silson et al, 2016;Tullo et al, 2023), all datasets indicated a bias between posterior and anterior scene networks. Posterior scene regions including the OPA and posterior PPA showed preferential connectivity with early visual regions, consistent with a role in processing egocentric visual features of scenes (Baldassano et al, 2016).…”

“…Within subcortical structures, anterior scene regions showed preferential connectivity with the hippocampus and, less consistently, the thalamus, while both anterior and posterior scene networks showed spatially distinct clusters of preferential connectivity within the cerebellum. The connectivity between anterior scene regions and the hippocampus has been related to the retrieval of imagined places (Tullo et al, 2023 ). Indeed, imagery and recall of familiar environments encompasses many of the extended scene regions implicated in connectivity with the anterior scene network (Boccia et al, 2015 ), consistent with proposed mnemonic functions of this network.…”

“…Although the functional properties of scene‐selective regions have been researched extensively, less is known about how these regions connect with each other and the rest of the brain. Previous studies employing resting‐state functional connectivity have suggested a division between a posterior network including the OPA and posterior portions of the PPA, and an anterior network including the RSC and anterior portions of the PPA (Baldassano et al, 2013 ; Nasr et al, 2013 ; Silson et al, 2016 ; Tullo et al, 2023 ). The majority of studies have focussed on estimating functional connectivity between scene‐responsive regions of interest.…”