An Event-Related Functional Magnetic Resonance Imaging Study
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Neural Correlates of Memory for Items and for Associations: An Event-related Functional Magnetic Resonance Imaging Study Ame´lie M. Achim and Martin Lepage Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/4/652/1757197/0898929053467578.pdf by guest on 18 May 2021 Abstract & Although results from cognitive psychology, neuropsychol- coding, greater prefrontal, hippocampal, and parietal activation ogy, and behavioral neuroscience clearly suggest that item was observed for associations, but no significant activation was and associative information in memory rely on partly different observed for items at the selected threshold. During recog- brain regions, little is known concerning the differences and nition, greater activation was observed for associative trials in similarities that exist between these two types of information as the left dorsolateral prefrontal cortex and superior parietal a function of memory stage (i.e., encoding and retrieval). We lobules bilaterally, whereas item recognition trials showed used event-related functional magnetic resonance imaging to greater activation of bilateral frontal regions, bilateral anterior assess neural correlates of item and associative encoding and medial temporal areas, and the right temporo-parietal junction. retrieval of simple images in 18 healthy subjects. During en- Post hoc analyses suggested that the anterior medial temporal coding, subjects memorized items and pairs. During retrieval, activation observed during item recognition was driven mainly subjects made item recognition judgments (old vs. new) and by new items, confirming a role for this structure in novelty de- associative recognition judgments (intact vs. rearranged). Rel- tection. These results suggest that although some structures ative to baseline, item and associative trials activated bilateral such as the medial temporal and prefrontal cortex play a gen- medial temporal and prefrontal regions during both encoding eral role in memory, the pattern of activation in these regions and retrieval. Direct contrasts were then performed between can be modulated by the type of information (items or associa- item and associative trials for each memory stage. During en- tions) interacting with memory stages. & INTRODUCTION view that item and associative information are distinc- An increasing amount of empirical evidence suggests tively processed in memory. It follows that memory for that episodic memories are formed of two main types of these two types of information could rely, at least in part, information: (1) information about individual items and on different brain regions. (2) information about the associations that these items Already, there are a number of findings that support maintain with each other and with their physical (e.g., this inference. Lesion studies in both rodents (Brown & color) or spatio-temporal (e.g., position in space) charac- Aggleton, 2001; Eichenbaum, Otto, & Cohen, 1994; teristics. These two types of information have been Cohen & Eichenbaum, 1993) and humans (Mayes et al., termed item memory and associative (relational) 2001; Mayes, van Eijk, Gooding, Isaac, & Holdstock, 1999; memory, respectively (Murdock, 1982; Humphreys, 1976, Vargha-Khadem et al., 1997) suggest that the hippocam- 1978). Although item and associative memory obviously pus plays a critical role in associative memory, but not share some common underlying episodic memory pro- in item memory. However, item memory is not com- cesses, there could also be some difference in the pro- pletely spared in patients with hippocampal damage, and cessing of these two types of information. For instance, some have argued that the hippocampus could be sim- the longer response times observed during the retrieval ilarly involved in both types of memory (Stark, Bayley, & of associative information relative to item information Squire, 2002; Stark & Squire, 2000, 2001). The prefrontal (Hockley, 1991; Gronlund & Ratcliff, 1989), the greater cortex could also be involved in associative memory as persistence of associative memory over time (Hockley, suggested by other neuropsychological studies that 1991, 1992), and the documentation of distinct receiver have shown that patients with frontal lobe lesions are operating characteristics (Yonelinas, 1997) attests to the relatively more impaired in tasks of associative memory relative to item memory (Johnson, O’Connor, & Cantor, 1997; Janowsky, Shimamura, & Squire, 1989). Lesion McGill University and Douglas Hospital Research Centre, studies, however, do not give information about which Quebec, Canada memory stage is affected. Indeed, the deficits could D 2005 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 17:4, pp. 652–667 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929053467578 by guest on 24 September 2021 reflect that (1) associative information is not success- item, B could be either another item or a feature fully encoded and, thus, cannot be retrieved, (2) asso- associated with A. ciative information has been correctly encoded but In the study by Yonelinas et al. (2001), individual cannot be accessed because of retrieval deficits, or (3) items (black and white images) were presented during both associative encoding and retrieval are impaired. the recognition test and subjects were asked to judge Thus, studying the distinction between item and asso- whether each item was old or new (item recognition) or ciative memory during both encoding and retrieval to judge whether each stimulus was initially presented in should lead to a better understanding of the processes red or green (associative recognition). The associative that support these two types of memory. More specifi- recognition task did not require subjects to distinguish cally, some brain regions could be involved in item or between intact and rearranged associations but instead Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/17/4/652/1757197/0898929053467578.pdf by guest on 18 May 2021 associative memory regardless of the memory stage, but it required them to recall the color initially associated other brain regions could be specifically involved in with each item. When these associative recognition trials encoding or retrieval of a certain type of information. were contrasted to old item recognition trials, hippo- An important advantage of functional brain imaging campal activation was observed. It is, therefore, possible techniques is that they enable us to examine encoding that the demands of generating the initial association, and retrieval separately while looking at the whole brain. not the recognition of associative information per se, During encoding, two main strategies have been adopted resulted in hippocampal activation in this experiment. In to distinguish brain activation specific to associative or the study by Tsukiura et al. (2002), the associative item-oriented encoding. The first strategy is to give the recognition task that gave rise to left parahippocampal subjects different instructions, with one set of instruc- activation might have also involved the generation of tions promoting associative encoding and the other additional associative information. During encoding, set of instructions promoting individual or nonassocia- the subjects were presented with comic strips formed tive encoding. Another strategy is to present stimuli that of 4 images. During recognition, they were cued with either encourage (e.g., pairs of items) or hinder (e.g., in- 2 images and asked to judge whether these images were dividual items) associative encoding. The neuroimaging from the same strip (associative recognition) or whether studies that have used either of these two strategies have both images had been studied before (item recogni- consistently reported greater hippocampal and prefron- tion). It is quite possible that the subjects tried to re- tal activation for associative relative to item encoding member the missing images from the same strip to (Davachi & Wagner, 2002; Davachi, Maril, & Wagner, facilitate their associative recognition judgments. Thus, 2001; Killgore, Casasanto, Yurgelun-Todd, Maldjian, & although the hippocampus is clearly implicated in asso- Detre, 2000; Henke, Weber, Kneifel, Wieser, & Buck, ciative encoding, it is still unclear whether activity in the 1999; Montaldi et al., 1998; Henke, Buck, Weber, & medial temporal lobe can be justifiably linked to asso- Wieser, 1997; Kapur et al., 1996; Vandenberghe, Price, ciative recognition. Wise, Josephs, & Frackowiak, 1996). Because episodic memory encoding and retrieval are During recognition, the most consistent finding is supported by partially different brain regions, and be- greater left prefrontal activation for associative relative cause the activation of specific brain regions (e.g., those to item recognition (Lepage, Brodeur, & Bourgouin, implicated in the processing of item or associative 2003; Badgaiyan, Schacter, & Alpert, 2002; Rugg, Fletch- information) typically depends on the pattern of activa- er, Chua, & Dolan, 1999; Nolde, Johnson, & D’Esposito, tion elsewhere in the brain (McIntosh, 2000), brain 1998; Cabeza et al., 1997), although right prefrontal regions supporting item and associative memory are activation has also been observed (Lepage et al., 2003; likely to differ between encoding and retrieval. It follows Rugg et al., 1999; Cabeza et al., 1997). In contrast to the that studying both encoding and retrieval in the same consistent prefrontal activation, only a few