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      Attenuated Boundary Extension Produces a Paradoxical Memory Advantage in Amnesic Patients

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      1 , , 2 , 1 , ∗∗
      Current Biology
      Cell Press

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          Summary

          Background

          When we view a scene, we construct an internal representation of the scene that extends beyond its given borders. This cognitive phenomenon is revealed by a subsequent memory error when we confidently misremember the extended scene instead of the original. This effect is known as “boundary extension” and is apparent in adults, children, and babies.

          Results

          Here we show that seven patients with selective bilateral hippocampal damage and amnesia, who cannot imagine spatially coherent scenes, displayed attenuated levels of boundary extension on three separate measures. Paradoxically, this reduced boundary extension resulted in better memory for the stimuli compared with matched control participants, because the patients' recall was less encumbered by the boundary extension error. A further test revealed that although patients could generate appropriate semantic, conceptual, and contextual information about what might be beyond the view in a scene, their representation of the specifically spatial aspect of extended scenes was markedly impoverished.

          Conclusions

          The patients' superior memory performance betrayed a fundamental deficit in scene processing. Our findings indicate that the hippocampus supports the internal representation of scenes and extended scenes when they are not physically in view, and this may involve providing a spatial framework in scenes. We suggest that interference with the ability to internally represent space may prevent the construction of spatially coherent scenes, with possible consequences for navigation, recollection of the past, and imagination of the future, which depend on this function.

          Highlights

          ► Patients with hippocampal damage and amnesia cannot imagine spatially coherent scenes ► Boundary extension (BE) is when people remember seeing more of a scene than was shown ► Amnesic patients had attenuated BE, which paradoxically permitted better memory ► Hippocampus supports scene representations, possibly supplying the spatial framework

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          Most cited references44

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          Loss of recent memory after bilateral hippocampal lesions.

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            The human hippocampus and spatial and episodic memory.

            Finding one's way around an environment and remembering the events that occur within it are crucial cognitive abilities that have been linked to the hippocampus and medial temporal lobes. Our review of neuropsychological, behavioral, and neuroimaging studies of human hippocampal involvement in spatial memory concentrates on three important concepts in this field: spatial frameworks, dimensionality, and orientation and self-motion. We also compare variation in hippocampal structure and function across and within species. We discuss how its spatial role relates to its accepted role in episodic memory. Five related studies use virtual reality to examine these two types of memory in ecologically valid situations. While processing of spatial scenes involves the parahippocampus, the right hippocampus appears particularly involved in memory for locations within an environment, with the left hippocampus more involved in context-dependent episodic or autobiographical memory.
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              Remembering the past and imagining the future: common and distinct neural substrates during event construction and elaboration.

              People can consciously re-experience past events and pre-experience possible future events. This fMRI study examined the neural regions mediating the construction and elaboration of past and future events. Participants were cued with a noun for 20s and instructed to construct a past or future event within a specified time period (week, year, 5-20 years). Once participants had the event in mind, they made a button press and for the remainder of the 20s elaborated on the event. Importantly, all events generated were episodic and did not differ on a number of phenomenological qualities (detail, emotionality, personal significance, field/observer perspective). Conjunction analyses indicated the left hippocampus was commonly engaged by past and future event construction, along with posterior visuospatial regions, but considerable neural differentiation was also observed during the construction phase. Future events recruited regions involved in prospective thinking and generation processes, specifically right frontopolar cortex and left ventrolateral prefrontal cortex, respectively. Furthermore, future event construction uniquely engaged the right hippocampus, possibly as a response to the novelty of these events. In contrast to the construction phase, elaboration was characterized by remarkable overlap in regions comprising the autobiographical memory retrieval network, attributable to the common processes engaged during elaboration, including self-referential processing, contextual and episodic imagery. This striking neural overlap is consistent with findings that amnesic patients exhibit deficits in both past and future thinking, and confirms that the episodic system contributes importantly to imagining the future.
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                Author and article information

                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                21 February 2012
                21 February 2012
                : 22
                : 4
                : 261-268
                Affiliations
                [1 ]Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, 12 Queen Square, London WC1N 3BG, UK
                [2 ]Department of Psychology, University of Delaware, 108 Wolf Hall, Newark, DE 19716, USA
                Author notes
                []Corresponding author s.mullally@ 123456ucl.ac.uk
                [∗∗ ]Corresponding author e.maguire@ 123456ucl.ac.uk
                Article
                CURBIO9317
                10.1016/j.cub.2012.01.001
                3315012
                22264610
                2940ec32-c4fd-4109-b715-f7b46aebbb7e
                © 2012 ELL & Excerpta Medica.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 10 November 2011
                : 14 December 2011
                : 3 January 2012
                Categories
                Article

                Life sciences
                Life sciences

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