A network linking scene perception and spatial memory systems in posterior cerebral cortex

Abstract

word count: 75 Main text word count: 1,913ABSTRACT Here, we report a new link between the spatial-memory and scene-perception systems of the human brain. Using fine-grained individual-subject fMRI, we describe three cortical areas, each lying immediately anterior to a region of the scene perception network, that are selectively activated when recalling familiar places. Network analyses show that these regions constitute a distinct functional network and interface with memory systems during naturalistic scene understanding. These regions may bridge perception and memory, supporting visually-guided navigation. MAIN TEXTSuccessful navigation requires integrating the current field-of-view with memory of the larger spatial context. While the neural systems supporting visual scene processing in posterior cerebral cortex 1-7 and spatial memory in the hippocampus and medial temporal lobe 8-15 are welldescribed in humans, little is known about how visual and spatio-mnemonic systems interface in the brain. Two disparate lines of inquiry yield different hypotheses. On the one hand, explicit recall of visual scenes (i.e. mental imagery) is thought to reinstate the same activity as perception in visual regions of the brain, including areas of the scene-perception network (parahippocampal place area (PPA), occipital place area (OPA), and medial place area (MPA)) [16][17][18][19] . On the other hand, theories of scene processing have posited that memory-based representations are not colocalized with perceptual representations, but instead, that visual information transitions from perceptual to memory-based representations moving anteriorly from areas of the sceneperception network 1,20-23 . Distinguishing between these possibilities is critical to understanding the neural mechanisms underlying navigation. Do scene perception and place memory share common neural substrates in the human brain?To address these issues, we used individual-subject fMRI to map the topology of sceneperception and place-memory related activity in the human brain in fine-grained detail and assess whether these responses are co-localized at the individual subject level. First, we independently localized the three regions of the scene-perception network by comparing activation when participants viewed images of scenes, people, and objects (Methods). Next, in the same subjects, we localized areas that showed preferential BOLD-activation when participants (N=14) recalled personally familiar places (e.g. their house) and people (e.g. their mother).This analysis revealed a striking topological pattern. In all participants, we found three clusters of place-memory activity proximate to, but distinct from, the three areas of the scene-perception network, which we refer to as 'place-memory areas' for brevity ( Figure 1). Across the lateral, ventral and medial cortical surfaces, the pairs of place-memory and scene-perception areas

Transforming the Concept of Memory Reactivation

“…Similar posterior (perception) to anterior (memory retrieval) shifts have been observed in other sceneselective areas, including lateral occipital and medial parietal areas [14,28]. Resting state fMRI analyses have shown that anterior and posterior aspects of ventral, lateral, and medial sceneselective areas have different connectivity profiles with the rest of the brain, consistent with the idea that scene perception and scene memory are supported by segregated visual cortical networks [14,[27][28][29]. Related work has suggested that this posterior-to-anterior division between visual perception and visual memory extends to stimulus classes other than scenes, such as objects, and to aspects of lateral and ventral temporal cortex outside of the scene network [30,31].…”

“…In an unpublished study, this striking dissociation was replicated in a paradigm that directly compared perception and memory retrieval using a within-subjects design [14]. Similar posterior (perception) to anterior (memory retrieval) shifts have been observed in other sceneselective areas, including lateral occipital and medial parietal areas [14,28]. Resting state fMRI analyses have shown that anterior and posterior aspects of ventral, lateral, and medial sceneselective areas have different connectivity profiles with the rest of the brain, consistent with the idea that scene perception and scene memory are supported by segregated visual cortical networks [14,[27][28][29].…”

“…Connectivity with the hippocampus may also explain the anterior bias for memory-based representations in the visual system, as the same anterior regions that exhibit a memory bias also exhibit relatively stronger connectivity to the hippocampus [14,27]. It is also of note that the hippocampus, itself, has been shown to more strongly represent retrieved content than perceived content [16,42].…”

“…Understanding the ways in which memory representations differ from perceptual representations will critically inform theoretical accounts of memory and will help clarify how the brain recreates the past. contain more information about the content of an experience when that experience is being retrieved from memory compared with when it is perceptually experienced [14][15][16][17]. The clear implication of this is that measures of reactivation, which only test whether activity patterns evoked during retrieval are similar to those evoked during perception, will systematically underestimate the amount, strength, or qualities of content representations during retrieval.…”

“…For example, a meta-analysis of over 100 functional magnetic resonance imaging (fMRI) studies found that scene perception recruits relatively posterior aspects of the parahippocampal place area (PPA), whereas retrieving scenes from memory recruits relatively anterior aspects of PPA [27]. In an unpublished study, this striking dissociation was replicated in a paradigm that directly compared perception and memory retrieval using a within-subjects design [14]. Similar posterior (perception) to anterior (memory retrieval) shifts have been observed in other sceneselective areas, including lateral occipital and medial parietal areas [14,28].…”