Memory, scene construction, and the human hippocampus

Abstract

We evaluated two different perspectives about the function of the human hippocampus-one that emphasizes the importance of memory and another that emphasizes the importance of spatial processing and scene construction. We gave tests of boundary extension, scene construction, and memory to patients with lesions limited to the hippocampus or large lesions of the medial temporal lobe. The patients were intact on all of the spatial tasks and impaired on all of the memory tasks. We discuss earlier studies that associated performance on these spatial tasks to hippocampal function. Our results demonstrate the importance of medial temporal lobe structures for memory and raise doubts about the idea that these structures have a prominent role in spatial cognition.T wo traditions of work have influenced discussion about the function of the hippocampus (1). One tradition is based on work with memory-impaired patients and the idea that the hippocampus is important for a particular kind of memory (2, 3). The other tradition is based on work with rodents and the idea that the hippocampus is critical for spatial mapping (4). Its possible role in spatial processing has been recently explored in humans as well (5), and it has been proposed that the human hippocampus is essential for the ability to construct spatially coherent scenes (6, 7).This view of hippocampal function has depended on evidence from two kinds of tasks: boundary extension and scene construction (6,8). Boundary extension refers to the tendency to reconstruct a scene such that it has a larger background than was actually presented (9). In the Mullally et al. (8) study, memoryimpaired patients exhibited boundary extension less strongly than controls. Scene construction refers to the ability to imagine and describe spatially coherent scenes. In two studies, memoryimpaired patients made few references to space when visualizing and describing imagined scenes (6,8).It is unclear how to reconcile such findings with the view that the hippocampus chiefly supports memory functions. In particular, the idea that the construction and visualization of scenes involves the hippocampus seems at odds with the historic distinction between short-term (working) memory and long-term memory and the related idea that short-term memory is independent of the hippocampus (10-12). According to this perspective, hippocampal damage should not impair performance on spatial tasks, so long as testing puts no burden on long-term memory. In an attempt to clarify these issues, we gave tests of boundary extension, scene construction, and memory to patients with well-characterized lesions limited to the hippocampus or large lesions of the medial temporal lobe.Results Experiment 1. Both controls and hippocampal patients exhibited boundary extension. That is, both groups drew the central objects such that they occupied less area than in the original photographs ( Fig. 1 controls = 61.9% of the original area, hippocampal patients = 62.5% of the original area, P < 0.01). The extent of reduction was simil...

The Cognitive Architecture of Spatial Navigation: Hippocampal and Striatal Contributions

“…It can also be seen as a system for enabling information from long-term memory to be rendered in parietal cortex as a coherent egocentric spatial scene consistent with a single viewpoint (Burgess et al, 2001;Byrne et al, 2007). This would explain the hippocampal role in imagery for spatial layout (Hassabis and Maguire, 2007;Schacter and Addis, 2007), but not for single objects (Kim et al, 2015). In either case, the hippocampal system can be used to generate information corresponding to upcoming states for use in planning, as consistent with recent experiments showing that self-generated place cell sequences do not necessarily reproduce the animal's most frequent behavior and instead sometimes generate paths never traversed by the animal (Gupta et al, 2010;Ó lafsdó ttir et al, 2015).…”

Boundary Extension in Face Processing

“…Mullally et al (2012) found that patients with selective bilateral damage to hippocampus demonstrated less BE errors than control participants, supporting the role of hippocampus in BE. Inconsistent with this finding, Kim, Dede, Hopkins, and Squire (2015) found that amnestic patients with hippocampal damage exhibited BE similarly to healthy controls. Furthermore, Park, Intraub, Yi, Widders, and Chun (2007) demonstrated that BE task causes selective activation in the PPA, a region associated with processing scenes such as landscapes or buildings (Epstein & Kanwisher, 1998), but not in the Lateral Occipital Cortex, typically associated with object recognition (Grill-Spector et al, 1999).…”

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

“…Here, too, we localised HC using a working memory task, thus complementing previous studies that find evidence for HC recruitment across a range of cognitive tasks. Indeed, several studies of patients with HC atrophy have reported scene‐specific deficits for both memory and perceptual tasks [Bird et al, 2008; Hartley et al, 2007; Lee et al, 2005a, 2005b; Mullally et al, 2012; but see Kim et al, 2011, 2015]. Functional neuroimaging studies have likewise found group‐level HC activation during scene discrimination [Aly et al, 2013; Lee et al, 2008], scene construction/imagining [Zeidman et al, 2015], and working memory [Lee and Rudebeck, 2010b; Park et al, 2003].…”