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Neuroimaging Studies of False Memory: a Selective Review

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Neuroimaging Studies of False Memory: a Selective Review Psychologia, 2012, 55, 131–145 NEUROIMAGING STUDIES OF FALSE MEMORY: A SELECTIVE REVIEW Nobuhito ABE Harvard University, USA It is widely recognized that human memory is an imperfect process that sometimes causes various kinds of distortions and illusions. Recently, some light has been shed on the brain mechanisms involved in this false memory phenomenon as a result of research into its neural basis embarked on by cognitive neuroscientists. This article reviews neuroimaging studies that have attempted to distinguish between true and false memory retrieval. It also reviews neuroimaging studies that have measured neural activity during encoding and addresses the question of whether the encoding- related neural activity predicts subsequent memory distortions. Finally, there is a brief discussion from the cognitive neuroscience perspective about whether the memory distortion reflects deficient cognitive processing or is a by-product of adaptive cognitive processing. Key words: false memory, fMRI, PET, recognition, recollection. Memory problems are mainly characterized by the failure to retrieve desired information, but sometimes people have memories of events that did not occur. Studies of this false memory phenomenon have a long history in the field of psychology, and it is now broadly accepted that human memory is prone to various kinds of distortions and illusions (Roediger, 1996; Schacter, 1999; Loftus, 2003). Memory distortions, as well as normal forgetting, provide valuable opportunities for researchers to analyze scientifically memory processing, which would be extremely difficult if memory were perfect. The development of neuroimaging techniques during the past two decades – positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) – has enabled us directly to measure brain activity associated with various cognitive functions. Many researchers in cognitive neuroscience have used functional neuroimaging to delineate the neural correlates of memory distortion and have attempted to distinguish true and false memories. The present paper reviews current progress in the study of the neural basis of false memory. This paper consists of three main sections. The first section discusses attempts to use PET and fMRI to distinguish retrieval processes between true and false memories. The second section discusses attempts to measure brain activity during encoding processes and to determine whether encoding-related brain activity predicts subsequent memory distortions. The concluding section of this paper briefly discusses from the cognitive neuroscience perspective whether memory distortion reflects deficient cognitive processing or is a by-product of adaptive cognitive processing. The author was supported by JSPS Postdoctoral Fellowships for Research Abroad. Correspondence concerning this article should be addressed to Nobuhito Abe, Department of Psychology, Harvard University, 33 Kirkland Street, Cambridge, MA 02138, USA (e-mail: [email protected]). 131 132 ABE NEUROIMAGING OF FALSE MEMORY – RETRIEVAL-BASED STUDIES Classic models of memory conceptualize memory processes as involving three separate stages: encoding, storage, and retrieval. One of the restrictions in the field of memory research is that whether subjects’ memories are accurate or not is unknown to the experimenters until they examine the data obtained from the retrieval phase. It is therefore not surprising that much attention has been paid to the retrieval mechanisms of false memory. In fact, many of the functional neuroimaging studies have attempted to distinguish between veridical and illusory memories by measuring brain activity at the retrieval phase. Most neuroimaging experiments to distinguish between true and false memory retrieval have been carried out in the context of what has been termed the sensory reactivation hypothesis. This hypothesis assumes that true memories are accompanied by the retrieval of more sensory/perceptual details than false memories (Schacter & Slotnick, 2004; Schacter, Chamberlain, Gaesser, & Gerlach, in press). The hypothesis originated from behavioral studies showing evidence of the retrieval of more sensory/perceptual details during true rather than false memory retrieval (e.g., Schooler, Gerhard, & Loftus, 1986; Johnson, Foley, Suengas, & Raye, 1988; Mather, Henkel, & Johnson, 1997; Norman & Schacter, 1997; Marche, Brainerd, & Reyna, 2010). The sensory reactivation hypothesis also assumes that reactivation of sensory brain areas occurs during true, but not false, memory retrieval. The origins of this line of thinking are apparent in several neurobiologically based models of memory retrieval, which state that episodic retrieval involves the reinstatement of processes that were active at the time of encoding (Alvarez & Squire, 1994; Rolls, 2000; Shastri, 2002; Norman & O’Reilly, 2003). According to such models, recollection of an event occurs when a pattern of cortical activity corresponding to the event is reinstated by activation of a stored representation of that pattern through hippocampal activity. These ideas have been integrated into what has been called the cortical reinstatement hypothesis (Rugg, Johnson, Park, & Uncapher, 2008), and several neuroimaging experiments have provided direct evidence supporting this hypothesis (e.g., Nyberg, Habib, McIntosh, & Tulving, 2000; Persson & Nyberg, 2000; Wheeler, Petersen, & Buckner, 2000; Nyberg et al., 2001; Vaidya, Zhao, Desmond, & Gabrieli, 2002; Johnson & Rugg, 2007; Ueno et al., 2007; Ueno et al., 2009). In the pioneering study of neuroimaging of false memory, Schacter et al. (1996) used PET to clarify the neural correlates of true and false recognition and to test the sensory reactivation hypothesis. False recognition is a process whereby people incorrectly claim that they have recently seen or heard a stimulus they have not encountered (Underwood, 1965). False recognition is not accompanied by a subjective feeling that people are responding untruthfully, and therefore researchers need to be able to detect a difference between true and false recognition that is not apparent to the conscious mind. A necessary condition for conducting such investigations, especially in functional neuroimaging experiments, is to obtain enough trials of false recognition to produce a stable brain activation map. To this end, Schacter et al. (1996) used as experimental stimuli the set of word lists NEUROIMAGING OF FALSE MEMORY 133 Fig. 1. Blood flow increases associated with true versus false recognition. Significant differences were found in the vicinity of the left superior temporal gyrus, temporal plane, and supramarginal gyrus. Adapted from Schacter et al. (1996) with permission from Elsevier. developed by Deese (1959) and Roediger and McDermott (1995). In this Deese- Roediger-McDermott (DRM) paradigm, participants hear a number of lists consisting of semantic associates (e.g., moon, light, shine, bright, hot, gleam, etc). During a subsequent test phase, subjects are presented with previously studied true targets (e.g., hot), nonstudied false targets (e.g., sun) that are semantically related to the studied items (i.e., lures for false recognition), and unrelated new targets (e.g., building). The merits for the use of this paradigm are twofold. The first obvious reason is that this paradigm can produce gist-based false recognition (i.e., false recognition where people fail to recollect specific details of an experience and instead remember general information of the gist of what happened) in response to the false targets with high probability (for a review, see Gallo, 2010). The second reason is that this word-list paradigm, which can be used either in an auditory or a visual modality, is particularly suitable for testing the sensory reactivation hypothesis. By auditorily presenting stimuli at encoding and visually presenting stimuli at retrieval (with scanning), it is possible to determine whether the regions responsible for auditory processing are reactivated during true, but not false, recognition. Schacter et al. (1996) found both commonalities and differences in brain activation between true recognition and false recognition. They found that, compared with a common baseline condition, both true and false recognition were associated with increased blood flow in regions implicated in memory processing such as the anterior prefrontal cortex, dorsolateral prefrontal cortex, medial parietal cortex, and medial temporal lobe. They also found that the left temporoparietal cortex, a region previously implicated in auditory processing, showed greater activation during true than false recognition (Fig. 1). They interpreted this finding in the context of the sensory reactivation hypothesis: because subjects had heard true, but not false, targets during the auditory encoding phase, left 134 ABE temporoparietal activation for true recognition might be a sensory signature that reflects memory traces for auditory aspects of previously studied words. Although their follow-up study using fMRI (Schacter, Buckner, Koutstaal, Dale, & Rosen, 1997) failed to replicate the greater activation in the left temporoparietal area during true than false recognition (for discussion, see Johnson et al., 1997), a subsequent study by Cabeza, Rao, Wagner, Mayer, and Schacter (2001) again supported the sensory reactivation hypothesis. Cabeza et al. conducted an fMRI study using the DRM paradigm with study conditions that promoted the encoding of sensory information. First, subjects viewed videotapes
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