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

Abstract

Functional neuroimaging studies have identified several “core” brain regions that are preferentially activated by scene stimuli, namely posterior parahippocampal gyrus (PHG), retrosplenial cortex (RSC), and transverse occipital sulcus (TOS). The hippocampus (HC), too, is thought to play a key role in scene processing, although no study has yet investigated scene‐sensitivity in the HC relative to these other “core” regions. Here, we characterised the frequency and consistency of individual scene‐preferential responses within these regions by analysing a large dataset (n = 51) in which participants performed a one‐back working memory task for scenes, objects, and scrambled objects. An unbiased approach was adopted by applying independently‐defined anatomical ROIs to individual‐level functional data across different voxel‐wise thresholds and spatial filters. It was found that the majority of subjects had preferential scene clusters in PHG (max = 100% of participants), RSC (max = 76%), and TOS (max = 94%). A comparable number of individuals also possessed significant scene‐related clusters within their individually defined HC ROIs (max = 88%), evidencing a HC contribution to scene processing. While probabilistic overlap maps of individual clusters showed that overlap “peaks” were close to those identified in group‐level analyses (particularly for TOS and HC), inter‐individual consistency varied across regions and statistical thresholds. The inter‐regional and inter‐individual variability revealed by these analyses has implications for how scene‐sensitive cortex is localised and interrogated in functional neuroimaging studies, particularly in medial temporal lobe regions, such as the HC. Hum Brain Mapp 37:3779–3794, 2016. © 2016 Wiley Periodicals, Inc.

Ultra-High-Field fMRI Reveals a Role for the Subiculum in Scene Perceptual Discrimination

“…Critically, therefore, these retinotopic size differences were not mirrored in terms of a similar numerical pattern in our main anteromedial subicular results. This result, alongside work showing hippocampal scene-sensitivity for size-matched items (Barense et al, 2010; Lee and Rudebeck, 2010; Hodgetts et al, 2016), indicates that these results are not driven by stimulus size.…”

“…The anterior hippocampus also responds strongly when the spatial configuration of scenes is altered (Howard et al, 2011) and during the passive viewing of scene exemplars (Zeidman et al, 2015a). A recent large-scale fMRI study confirmed robust group-level and individual-level scene activations in the anterior hippocampus during a one-back task (Hodgetts et al, 2016). The anterior hippocampus has been associated with global/coarse spatial representations, whereas the posterior hippocampus has been argued to support more fine-grained spatial processing (Poppenk et al, 2013).…”

“…Smaller clusters were found in the lateral occipital cortex/transverse occipital sulcus bilaterally. This broader network of regions during scene oddity corresponds to those regions showing strong intrinsic functional connectivity at rest (Baldassano et al, 2016), and increased functional activity during 3 T task fMRI (Hodgetts et al, 2016). The activation coordinates for this analysis are shown in Table 3.…”

“…Previous group-level fMRI studies at 3 T have reported scene-selectivity in the anterior- medial region of the hippocampus (Zeidman et al, 2015a; Hodgetts et al, 2016), and electrophysiological studies in animals have revealed that place cells show greater spatial coherence and firing rate in the medial versus lateral subiculum (Sharp and Green, 1994; Kim et al, 2012). To test this potential functional distinction along the transverse axis, the anterior subiculum was divided into medial and lateral sections on individual structural scans (Fig.…”

“…Indeed, while several 3 T fMRI studies report scene sensitivity in the posterior hippocampus (Lee et al, 2008; Barense et al, 2010; Liang et al, 2013), there is emerging evidence that the anterior hippocampus may be particularly responsive to scenes (Lee et al, 2013; Hodgetts et al, 2016; Zeidman and Maguire, 2016), potentially via its broader functional connectivity within an anterior scene processing network (Baldassano et al, 2016). A recent account proposes a role for the anterior hippocampus—and in particular the subiculum—in constructing internal scene “models” (Zeidman and Maguire, 2016).…”