Scene-Selective Cortical Regions in Human and Nonhuman Primates

Abstract

FMRI studies have revealed three scene-selective regions in human visual cortex (the Parahippocampal Place Area (PPA), Transverse Occipital Sulcus (TOS) and RetroSplenial Cortex (RSC)), which have been linked to higher-order functions such as navigation, scene perception/recognition, and contextual association. Here, we document corresponding (presumptively homologous) scene-selective regions in the awake macaque monkey, based on direct comparison to human maps, using identical stimuli and largely overlapping fMRI procedures. In humans, our results showed that the three scene-selective regions are centered near - but distinct from - the gyri/sulci for which they were originally named. In addition, all these regions are located within or adjacent to known retinotopic areas. Human RSC and PPA are located adjacent to the peripheral representation of primary and secondary visual cortex, respectively. Human TOS is located immediately anterior/ventral to retinotopic area V3A, within retinotopic regions LO-1, V3B, and/or V7. Mirroring the arrangement of human regions FFA and PPA (which are adjacent to each other in cortex), the presumptive monkey homologue of human PPA is located adjacent to the monkey homologue of human FFA, near the posterior superior temporal sulcus. Monkey TOS includes the region predicted from the human maps (macaque V4d), extending into retinotopically-defined V3A. A possible monkey homologue of human RSC lies in the medial bank, near peripheral V1. Overall, our findings suggest a homologous neural architecture for scene-selective regions in visual cortex of humans and non-human primates, analogous to the face-selective regions demonstrated earlier in these two species.

Evidencing a place for the hippocampus within the core scene processing network

“…Comparing the peaks in each ROI with meta‐analytic maps revealed that most group‐level maxima were in the vicinity of scene‐related coordinates reported previously. The group‐level peak for PHG was situated at the most posterior and lateral part of the structure, close to the collateral sulcus and the adjacent temporal fusiform gyrus, as observed previously [Nasr et al, 2011; Park and Chun, 2009]. The RSC peak activation was, again, located near previously reported coordinates (see section “Comparison with Previous Literature”).…”

“…While previous studies have attempted to characterise scene‐sensitivity—and its individual‐level consistency—these studies have often used limited sample sizes [e.g., Nasr et al, 2011; Spiridon et al, 2006], or have restricted analysis to a single brain region [e.g., Peelen and Downing, 2005]. We provide, therefore, the first detailed investigation of scene‐sensitivity within a large sample and across a range of regions.…”

“…2). Given the anatomical variability of the TOS across individuals (maximum overlap for the TOS in this atlas is 46%), a more liberal probability threshold of 25% was used to define the mask, providing coverage of TOS and partial coverage of the adjacent lateral occipital cortex (LOC) and occipital pole [Nasr et al, 2011]. Using standard anatomical guidelines for identifying sulci [Duvernoy, 1999; Iaria and Petrides, 2007], the placement of the TOS ROI was confirmed on the standard MNI‐152 brain template.…”

“…As such, it is unsurprising that functional neuroimaging techniques have revealed a putative “core” scene processing network in the human brain that responds strongly when viewing navigationally relevant stimuli (e.g., scenes) versus other visual categories. This core network is thought to include posterior parahippocampal gyrus [PHG; Aguirre et al, 1998a; Epstein et al, 2003; Epstein and Kanwisher, 1998], retrosplenial cortex [RSC; Auger et al, 2012; Epstein et al, 2007; Vann et al, 2009] and the transverse occipital sulcus [TOS; Dilks et al, 2013; Ganaden et al, 2013; He et al, 2013; Mullin and Steeves, 2011; Nasr et al, 2011]. As seen in the neural processing of other visual categories [Taylor and Downing, 2011], these regions appear to support distinct but complementary aspects of scene processing, and are differentially modulated by changes in viewpoint [Epstein et al, 2003, 2007; Park and Chun, 2009], spatial layout [Harel et al, 2013; Park et al, 2015], and lower‐level spatial features [Kravitz et al, 2011a; Nasr et al, 2014].…”

“…While several studies have attempted to characterise the individual‐level consistency of scene‐sensitive brain activations, these studies have either used small sample sizes [Nasr et al, 2011; Spiridon et al, 2006], or focussed on a single scene processing region [e.g., Peelen and Downing, 2005]. …”