Constructing, Perceiving, and Maintaining Scenes: Hippocampal Activity and Connectivity

Cerebral Cortex, October 2015;25: 3836–3855 doi: 10.1093/cercor/bhu266 Advance Access Publication Date: 18 November 2014 Original Article ORIGINAL ARTICLE Constructing, Perceiving, and Maintaining Scenes: Peter Zeidman, Sinéad L. Mullally, and Eleanor A. Maguire Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London WC1N 3BG, UK Address correspondence to Prof. Eleanor A. Maguire. Email: Abstract In recent years, evidence has accumulated to suggest the hippocampus plays a role beyond memory. A strong hippocampal response to scenes has been noted, and patients with bilateral hippocampal damage cannot vividly recall scenes from their past or construct scenes in their imagination. There is debate about whether the hippocampus is involved in the online processing of scenes independent of memory. Here, we investigated the hippocampal response to visually perceiving scenes, constructing scenes in the imagination, and maintaining scenes in working memory. We found extensive hippocampal activation for perceiving scenes, and a circumscribed area of anterior medial hippocampus common to perception and construction. There was significantly less hippocampal activity for maintaining scenes in working memory. We also explored the functional connectivity of the anterior medial hippocampus and found significantly stronger connectivity with a distributed set of brain areas during scene construction compared with scene perception. These results increase our knowledge of the hippocampus by identifying a subregion commonly engaged by scenes, whether perceived or constructed, by separating scene construction from working memory, and by revealing the functional network underlying scene construction, offering new insights into why patients with hippocampal lesions cannot construct scenes. Key words: episodic memory, fMRI, hippocampus, perception, scene construction, scenes Introduction The neuroimaging literature is replete with studies showing that posterior parahippocampal cortex (PHC) and retrosplenial cortex (RSC) are more engaged by scenes than other types of stimuli (Epstein and Kanwisher 1998; Epstein 2008; Ranganath and Ritchey 2012). While PHC and RSC involvement in processing scene‐related information is not in doubt, in recent years the hippocampus has also been linked with scenes. Patients with bilateral hippocampal damage and amnesia are not only impaired at recalling events from their past, but also at imagining events in their personal future. Klein et al. (2002) described patient D.B., who was amnesic and could not imagine his personal past or future, but had preserved semantic knowledge and could use it to reason about general (nonpersonal) past and future events. Andelman et al. (2010) reported the case of patient M.C. who, following an epileptic episode, experienced bilateral hippocampal damage and similarly could not recall years of her past or imagine her personal future. To investigate the shared process which may underlie recalling past and imagining future scenes, Hassabis, Kumaran, and Vann et al. (2007) asked a group of patients with bilateral hippocampal damage and amnesia to construct atemporal scenes (i.e., not set in the past or the future) in their imagination. The patients were impaired at constructing scenes relative to matched control subjects (replicated by Mullally, Intraub, and Maguire 2012) with a specific deficit noted in the spatial coherence of their imagined experiences. This suggested that the hippocampus may perform a common function for the construction of scenes in the imagination, © The Author 2014. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Hippocampal Activity and Connectivity Scenes and the Hippocampus | 3837 may not be required for processing the scene currently in view. Mullally, Intraub, and Maguire (2012) similarly tested 7 patients with focal bilateral hippocampal damage and amnesia on their ability to describe a scene photograph. They found that participants could accurately describe a photograph, and they could reason about what objects may come into view if the participant imagined that the standpoint of the picture was moved backward by a few paces. However, in contrast to healthy controls, the patients omitted references to the spatial arrangement of objects beyond the edges of a picture, suggesting that the hippocampus may only be required for processing the scene beyond the current view. Although one study found that hippocampal patients were impaired in describing real-life and pictorial scenes (Zeman et al. 2013), this was based on patients with mixed etiology, no structural detail on their lesions was provided and this could not be replicated in a subsequent study by Race et al. (2013). In summary, there is a lack of consensus in the literature over whether the hippocampus is involved in scene perception, and this is complicated by potential confounds such as memory encoding. On the basis that scene construction engages the hippocampus during imagination (Hassabis, Kumaran, Vann, et al. 2007, Hassabis, Kumaran, and Maguire 2007), we hypothesized that, in neurologically healthy participants, simply perceiving scenes (without a comparison or discrimination task) may engage the hippocampus, reflecting the creation of an internal model of the scene. Under this hypothesis, differences in findings across studies on scene perception would be due to whether or not participants constructed a spatially coherent model of the scene on each trial of the experiment. This idea accords with recent findings that the hippocampus is engaged by discriminating scenes based on their global configuration, or “strength-based perception,” but not when discriminations are based on differences in local visual features, or “state-based perception” (Aly and Yonelinas 2012; Aly et al. 2013). Similarly, Hartley et al. (2007) proposed that the hippocampus would be engaged “when a flexible or allocentric representation of spatial layout is required.” In this study, for the first time, we set out to directly compare scene perception and scene construction to test whether there is evidence that both functions share a neural substrate involving, in particular, the hippocampus. We also took this opportunity to investigate a second aspect of scene construction. When someone constructs a scene in his or her imagination, in addition to creating the scene representation, he or she must also maintain it in working memory. While the established model of hippocampal function is that it is not involved in working memory (Cave and Squire 1992; Alvarez et al. 1994), this has been challenged in recent years (see Ranganath and Blumenfeld 2005 for review) and is a (...truncated)