Elsevier

Neuropsychologia

Volume 47, Issue 11, September 2009, Pages 2239-2251
Neuropsychologia

Neural systems mediating field and observer memories

https://doi.org/10.1016/j.neuropsychologia.2009.02.019Get rights and content

Abstract

Autobiographical memories are more imbued with affect when one adopts a first-person or field perspective during event retrieval, rather than a third-person or observer perspective. We combined fMRI, event narratives, and subjective ratings to identify the neural networks engaged with field versus observer memories for real-world events. Our results revealed significant decreases in bilateral insula and left somato-motor activity during the recall of observer memories, paired with a small relative increase in right posterior amygdala activity coincident with the recall of field memories. Notably, these regions showed no overlap with those areas mediating the narrative content and subjective emotionality of the remembered events. Our findings suggest that the emotionality of field relative to observer memories is not simply driven by increased limbic activation when one adopts a first-person retrieval perspective. Rather, there is also a significant reduction in one's cortical representations of the physical, embodied self when a third-person – or disembodied – perspective is taken at retrieval.

Introduction

Events of the personal past are retrievable from two perspectives. One is through the rememberer's own eyes, as if he or she were looking outward, watching the events unfold anew. Alternatively, autobiographical memories may be recalled from a spectator's standpoint, which allows an individual to see him or herself as an actor in the memory image. These two modes of remembering are referred to as field and observer memories, respectively.

The distinction is important for several reasons. First, the fact that first-person perceptions can be transformed into third-person recollections reflects the active, reconstructive nature of autobiographical recall and refutes the idea that human memory works like a video camera that passively and veridically records perceptual experience for later playback (Loftus & Loftus, 1980; Nigro & Neisser, 1983). Second, the field/observer distinction underscores the unique capabilities of episodic memory—that “true marvel of nature” which Tulving (2002, p. 1) has brought into bold relief. Besides making it possible for people to reexperience their past and project themselves into the future, and thus travel mentally through subjective time (Tulving, 1983), episodic memory enables rememberers to navigate from either a participant's or an actor's point of view. Third, research reviewed by Schacter (1996, p. 22) leads to the “surprising, even startling observation that … the emotional intensity of a memory is determined, at least in part, by the way in which you, the rememberer, go about remembering the episode. And the emotions that you attribute to the past may sometimes arise from the way in which you set out to retrieve the memory in the present.”

To amplify the last point, several studies have shown that, in comparison with observer memories, field memories are accompanied by more intense affect (Nigro & Neisser, 1983; Robinson & Swanson, 1993; Talarico, LaBar, & Rubin, 2004) and their narratives contain more information about “internal” aspects of the event, such as physical sensations and psychological motivations, but less information about “external” aspects, such as how things looked and where things were. These differences have been demonstrated in research on autobiographical memory for both innocuous incidents and traumatic events, such as shooting a basketball versus being struck with a baseball bat (McIsaac and Eich, 2002, McIsaac and Eich, 2004; Robinson, 1996).

Though earlier experiments have established a connection between retrieval perspective and event emotionality, how this relation is mediated in the brain remains unknown. Here we combined fMRI, event narratives, and subjective ratings in a novel attempt to isolate the neural systems engaged with field versus observer memories for complex, naturalistic events.

At least two systems are apt to be involved. On the one hand, not only is the amygdala integral to emotion-related effects on memory encoding and consolidation (Dolcos, LaBar, & Cabeza, 2004; Hamann, Elt, Grafton, & Kilts, 1999; Kensinger & Schacter, 2006; McGaugh, 2004, Phelps, 2004; Richardson, Strange, & Dolan, 2004), but also, recent evidence suggests that the amygdala also plays a central role in the retrieval of emotional memories (Cabeza & St. Jacques, 2007; Daselaar et al., 2008; Dolcos, LaBar, & Cabeza, 2005; Fink et al., 1996, Greenberg et al., 2005, LaBar, 2007; Smith, Dolan, & Rugg, 2004). On the other hand, awareness of one's on-going subjective emotional states is inextricably linked to the conscious monitoring of one's on-going visceral, physiological states (Damasio, 1994), an idea traceable to James (1884) over a century ago. Critical to this interoceptive ability are the insula and somatosensory cortices (Critchley, Wiens, Rothstein, Öhman, & Dolan, 2004; Damasio et al., 2000; Pollatos, Gramann, & Schandry, 2006). Given that visual-perceptual aspects of memory retrieval rely on the same cortical systems used when actually perceiving a stimulus (e.g., Handy et al., 2004; Wheeler, Petersen, & Buckner, 2000; see Cabeza & St. Jacques, 2007), we hypothesized that either or both of these emotion-related systems might show a similar reactivation in response to autobiographical memory retrieval. Accordingly, the primary aim of our study was to test the prediction of a greater response in the amygdala, insula, and somatosensory regions for field relative to observer memories.

We also had a secondary, control-related aim. In particular, the recall of complex autobiographical memories unconstrained for field versus observer perspective has been linked to an extensive network of brain regions, including left ventral, dorsal, and medial prefrontal cortices, medial temporal areas, and the inferior parietal lobule (Cabeza & St. Jacques, 2007; Maguire, 2001; Schacter, Addis, & Buckner, 2007). Critically, however, brain regions engaged during memory retrieval are not limited to those associated with the act of retrieval itself. In addition, the subjective experience of the retrieved memory will also influence the pattern of activation obtained. This introduces a source of variance in fMRI data that is associated with the phenomenological attributes of the event being recalled, rather than with the retrieval network itself (Addis, Wong, & Schacter, 2007). Thus the secondary aim of our study was to identify any brain regions that correlate positively with phenomenological differences between field and observer memories, as reflected in either recall narratives or subjective ratings, in order to dissociate retrieval networks per se from those regions that simply vary with the subjective experience of remembering, independent of the specific mode of retrieval.

Section snippets

Overview

The experiment took place over two days for each participant. On the first day, university students completed four complex, physical tasks, such as creating an original work of art and taking a roundabout walk across campus. One week later, participants were scanned as they silently recalled each task twice: the first time from either the field or observer perspective, and the second time from either the same perspective as on the initial recall occasion (field/field vs. observer/observer

Subjective ratings

Data summarized in Table 1A show that although the participants were adept at maintaining the observer perspective during task recall (mean rating = 3.77 on a 1–5 scale), they found it even easier to maintain the field perspective (mean = 4.68; F(1/15) = 16.30, p < 0.01). This was true the first time they recalled a given task as well as the second time (ps > 0.10 for both the main effect of Recall Occasion and the Recall Occasion × Recall Perspective interaction). There was also a significant advantage of

Discussion

Evidence from several behavioral sources suggests that memories relived from a field or first-person perspective have an increased level of subjective emotionality, relative to memories retrieved from an observer or third-person perspective (e.g., McIsaac & Eich, 2002; Nigro & Neisser, 1983; Robinson & Swanson, 1993). This study sought to identify the neural systems mediating this effect. More to the point, a number of different brain regions have been reliably implicated in autobiographical

Acknowledgements

Preparation of this article was aided by grants to E.E. and T.C.H. from the Natural Sciences and Engineering Research Council of Canada and by the advice and assistance provided by Kalina Christoff, Joanne Elliott, Trudy Harris, Lindsay Nagamatsu, Alexandra Percy, and Dan Schacter. T.C.H. was also supported by the Michael Smith Foundation for Health Research.

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