Elsevier

NeuroImage

Volume 47, Issue 4, 1 October 2009, Pages 1747-1756
NeuroImage

Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception

https://doi.org/10.1016/j.neuroimage.2009.04.058Get rights and content

Abstract

Constructing a rich and continuous visual experience requires computing specific details across views as well as integrating similarities across views. In this paper, we report functional magnetic resonance imaging (fMRI) evidence that these distinct computations may occur in two scene-sensitive regions in the brain, the parahippocampal place area (PPA) and retrosplenial cortex (RSC). Participants saw different snapshot views from panoramic scenes, which represented clearly different views, but appeared to come from the same scene. Using fMRI adaptation, we tested whether the PPA and RSC treated these panoramic views as the same or different. In the panoramic condition, three different views from a single panoramic scene were presented. We did not find any attenuation for panoramic repeats in the PPA, showing viewpoint-specificity. In contrast, RSC showed significant attenuation for the panoramic condition, showing viewpoint-integration. However, when the panoramic views were not presented in a continuous way, both the specificity in the PPA and the integration in RSC were lost. These results demonstrate that the PPA and RSC compute different properties of scenes: the PPA focuses on selective discrimination of different views while RSC focuses on the integration of scenes under the same visual context. These complementary functions of the PPA and RSC enable both specific and integrative representations of scenes across several viewpoints.

Introduction

A central task of the human visual system is to maintain a cohesive visual experience from discrete snapshots of retinal input. Multiple physiological constraints limit the amount of visual input, and constant eye and head movements change the retinal projection every moment. Nevertheless, we experience the space around us as continuous and coherent. How do we achieve such an integrated percept of the world while preserving specific information in each individual view? To enable both specificity and invariance, multiple levels of scene representation might co-exist. In this paper, we present fMRI data showing such different kinds of scene representations in the brain. Specifically, we aim to answer whether scene-specific areas in the brain represent specific visual details of each individual scene, or an extended representation that includes multiple successive views.

A recent fMRI study suggests that at least one scene-specific area in the brain represents scenes in a viewpoint-specific way. The parahippocampal place area (PPA) is a scene-specific region in the ventral visual stream (Aguirre et al., 1996, Epstein and Kanwisher, 1998). Using sets of scenes that had viewpoint changes, Epstein et al. (2003) demonstrated that the PPA treated scenes with viewpoint changes as different scenes. This suggests that this area represents scenes as individual snapshots of each view rather than as a broader scene that integrates multiple similar snapshots.

However, a number of recent studies have shown that people represent integrative, expansive space (McNamara et al., 2003, Tversky, 2005). For example, learning spaces or routes for navigation requires associating a current scene or self to a larger scale environment (McNamara et al., 2003). Viewpoint selective responses provide information about the relative position of a viewer in a scene layout. But to navigate through a broader, global environment, viewers need a more expansive representation of the space beyond what is currently in view, based on associations with views that were seen before. The PPA may not be sufficient for such integrative functions: a study that directly tested navigation function in the PPA showed that the PPA does not play a role in guiding navigation through the immediate environment (Epstein et al., 1999).

Instead, another scene-specific area in the brain, the retrosplenial cortex (RSC), has been highlighted as an area important for navigation and route learning (Cain et al., 2006, Cooper and Mizumori, 2001, Maguire et al., 1997Maguire et al., 1998, Maguire, 2001, O'Craven and Kanwisher, 2000). For example, patients who have retrosplenial cortex damage were able to identify scenes or landmarks, but lost the ability to use these landmarks to orient themselves or to navigate through a larger environment (Aguirre and D'Esposito, 1999, Maguire, 2001, Valenstein et al., 1987). This contrasts with patients who have damage to their parahippocampal area and could not identify scenes or landmarks at all (Mendez and Cherrier, 2003).

In addition to such neurological evidence, number of recent fMRI results suggest that the PPA and RSC may play distinct roles in object and scene perception (Bar and Aminoff, 2003, Epstein and Higgins, 2007, Epstein et al., 2007a, Henderson et al., 2008). For example, Bar and Aminoff (2003) proposed that RSC represents abstracted prototypical properties of an object context, while the PPA processes physical properties of an object context. Epstein et al., 2007a, Epstein et al., 2007b) also reported that the PPA processes visual details of a scene, while RSC processes each scene as part of a broader frame or memory. The results of the current study to these recent fMRI findings will be discussed more extensively in the discussion.

These neurological and fMRI studies suggest that the PPA and RSC might encode different kinds of scene representations. More specifically, the PPA may represent physical details of the scenes such as landmarks, while RSC may represent the navigationally relevant properties of the scene, such as the association of the current scene or objects with other related scenes. In sum, we hypothesized that the scene representation in RSC may have a viewpoint-invariant scene representation used to create a more integrative cognitive map of the environment.

We measured repetition attenuation to test the nature of scene representations in the PPA and RSC. fMRI can reveal the properties of scene-specific representations, as activity is lower for repeated items compared to novel items (Schacter and Buckner, 1998, Wiggs and Martin, 1998). This repetition attenuation can reveal if a particular neuronal population treats two stimuli as the same or different from each other (Grill-Spector and Malach, 2001). For example, the fMRI response in the PPA shows less activity for repeated scenes than for novel scenes (Epstein et al., 2003, Park et al., 2007, Yi and Chun, 2005).

We presented panoramic scene stimuli (Fig. 1). Three sections were taken from a single panoramic image of a scene, producing three spatially continuous snapshots of a single space. These three scenes were presented in contiguous order, each overlapping 66% with the previous section (in other words, the 1st and the 3rd scene overlapped 33%). Thus, when these scenes were consecutively presented, a strong sense of continuity was achieved through the visual overlap across repetition and the coherent temporal order in which they appeared. This panoramic presentation resembles our usual survey of the environment, sampling views of scenes through successive eye movements. If scene representation in a brain region is viewpoint-specific, these three scenes will be treated as different from each other and will result in no attenuation for panoramic repetition. On the other hand, if the scene representation is viewpoint-independent, the brain will treat these scenes as one integrated scene, just as we experience everyday, and will show attenuation for panoramic repetition.

Section snippets

Methods

Experiment 1 directly tested two contrasting hypotheses about the functions of the PPA and RSC in scene perception. Since scene representation in the PPA is sensitive to details of individual scenes, we hypothesized that there would be little panoramic repetition attenuation in the PPA. In contrast, if RSC serves a more integrative function, associating a number of panoramically-related scenes as a single scene, then we should expect panoramic repetition attenuation in RSC. Experiment 2 asked

ROI analyses

Repeated-measures ANOVA and paired t-tests between conditions were performed on the averages of the peak amplitude responses in the PPA and RSC ROIs. There was no main effect of hemisphere in any of the ROIs, and hemisphere did not interact with any combination of the other factors. Thus, both hemispheres were collapsed for analysis (Fs < 4, P > 0.1).

Repeated-measures ANOVA with region (PPA or RSC), condition (panoramic repeat, identical repeat), and repetition (1st or 3rd) revealed a significant

Discussion

The current study tested whether two major scene-selective regions in the brain represent scenes in a viewpoint-specific way or a more integrative, viewpoint-invariant way. The results suggest that viewpoint-specific and invariant representations co-exist in these scene recognition networks of the brain. Furthermore, perceptual continuity across repetition is important for both discriminating and associating different views of the same scene. When viewpoint changes occur continuously, allowing

Acknowledgments

This work was supported by National Institutes of Health Grants to M. M. C. (EY014193 and P30 EY000785).

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