Research reportAge-related changes in source memory retrieval: an ERP replication and extension
Introduction
Older adults are less adept at monitoring the context of information they have received and are less able to recover the context or ‘source’ of previously experienced events, e.g., temporal context [15], [60], [65], spatial context [44], [72], or perceptual context [38]. Similarly, studies of reality monitoring have shown that older adults are impaired at remembering if recalled items were internally generated (imagined) or externally generated (heard or seen) [22]. However, they are less impaired or are not impaired at all on simple item recognition memory, i.e., in identifying whether an item is old or new [9], [15], [60]. A recent meta-analysis demonstrated that the effect size for item recognition memory deficits in aging (d=0.57) was smaller than that for remembering either the stimulus-related context (d=0.80) or spatiotemporal context (d=1.17) of the to-be-remembered material [58]. This source memory impairment has been implicated as contributing to other memory problems seen in older adults, such as telling the same story twice [31] or attributing false fame to a previously-presented non-famous name [14].
Patients with frontal lobe damage are also impaired in making source memory judgments [3], [39], [33], as are non-human primates with discrete mid-dorsal frontal lesions [45]. Hence, source memory is thought to depend upon a frontally-based system [14], [25], whereas item memory appears to depend more upon the medial temporal lobe system [59]. Given the older adults’ disproportionate difficulty with source compared to item memory, it appears that age-related memory decline is due, at least in part, to frontal lobe dysfunction.
Neuroimaging studies also provide evidence for frontal lobe deficits in the old. For example, recent positron emission tomography (PET) imaging studies revealed that the right prefrontal cortex is involved in the retrieval of temporal-order memories [6] and that older adults show reduced right prefrontal activity in such temporal-order memory tasks compared to the young [4]. Similarly, in a test of word recall, young adults showed activation in anterior frontal regions, which was not seen in older adults [51]. Accordingly, right prefrontal cortex appears to be engaged under more challenging retrieval conditions, and a deficit in right prefrontal cortex may help explain the differences in the effect of aging on recognition compared to recall and source retrieval performance [9].
Event-related potential (ERP) studies of memory have revealed two major electrophysiological correlates of contextual recollection. The first component is the well-studied left parietal episodic memory (EM) effect, for which old words are more positive-going than new words from approximately 400 to 800 ms (for a review, see Ref. [16]). The amplitude of this EM effect is larger in association with items rated as being consciously remembered [50], [53], [54], [61], for correctly recognized items that are subsequently recalled [49], and for words whose study context is correctly retrieved [61], [69], [70], [68]. Intracranial studies have reported similar EM effects recorded directly from the hippocampus and surrounding subcortical structures over a similar time course as the surface effect [23], [56]. Further, the left parietal EM effect has been reported to be reduced in epilepsy patients who have undergone medial temporal lobectomy [55], [29], and in seizure patients with known medial temporal lobe pathology [66], suggesting that the EM effect recorded at the scalp receives contributions from structures within the medial temporal lobe memory system.
The second EM effect of particular relevance to source memory tasks occurs at right prefrontal scalp sites starting around 600 ms and continuing through the end of the recording epoch [1], [29], [61], [71], [68]. The functional interpretation of the right prefrontal activity remains unclear; in some ERP studies it has been proposed to reflect retrieval success [34], [70]. Others have interpreted the right prefrontal EM effect to reflect post-retrieval processing [61]. This involves manipulating the information retrieved from the hippocampal system, or as in Moscovitch’s theory [41], ‘working with memory’. Such processes could include evaluating how the retrieved information relates to the task at hand or how the retrieved information can be used to guide subsequent behavior.
Few studies have examined the effects of aging on EM effects associated with source retrieval, and the limited results that are available have been mixed. Mark and Rugg [34] presented words during a lexical-decision task in either a male or female voice, and then required participants to make old–new recognition decisions to visually presented words. For items judged old, subjects made a subsequent voice (i.e., source) judgment. Both young and old subjects showed a left parietal EM effect that did not differ in magnitude between the two groups. Likewise, both groups showed right prefrontal EM effects that were similar in magnitude and topography. The authors concluded that the neural centers subserving source retrieval were situated in the right prefrontal cortex and were relatively spared by the aging process.
However, two other studies [61], [62] have failed to show the right prefrontal EM effect in the ERPs of older adults. For Trott et al.’s task [61], as in the current design, young and old participants studied two lists of sentences each of which contained two nouns and were subsequently tested on item (old/new) and source (list 1/list 2) memory. The left parietal EM effect was present in both young and old subjects. However, only the young produced the right prefrontal EM effect that differed as a function of subsequent source attribution. Trott et al. suggested that this later EM effect was related to the search for and/or retrieval of temporal source information and that the lack of this prefrontal activity in the old, in addition to their poorer source performance, was consistent with the proposal that older adults use a less efficient strategy to retrieve and/or search for source information than the young.
The current study is a replication and extension of the Trott et al. investigation [61]. In that study, though older adults performed above chance levels, their performance was relatively poor (uncorrected percentage of hits with correct source=55%). Several changes were implemented in the temporal source task used by Trott et al. [61] in an attempt to increase the source performance of the old participants. First, current participants had an unlimited amount of time to study the sentences. Second, each sentence was presented on the monitor in its entirety, as opposed to presenting each word of the sentence sequentially. Each of the sentences appeared twice within the study list to give subjects more exposure to the study words prior to the test. Further, elaborative encoding was promoted by asking subjects to make a pleasant/unpleasant (liking) judgment for each sentence. More significantly, the 16-word study lists used by Trott et al., were halved to eight words per list to decrease the memory load, and participants were coached in the use of different mnemonic strategies that could be used to improve their memory performance. We hypothesized that if the lack of a right prefrontal EM effect in the old was related to poor source memory performance, then enhanced performance should evoke the EM effect observed in Trott et al.’s young subjects. Finally, to improve the spatial detail observed in maps of memory-related ERP activity, we recorded from 62 channels and used current source density analysis to resolve better the scalp distributions of the various EM effects that were expected to be recorded.
Section snippets
Participants
Fourteen young (18–28 years) and 14 old (60–80 years) women recruited by community flyers, newspaper advertisements and word of mouth participated in the study. All subjects reported themselves to be native English speakers, in good physical health and were free from medications known to affect the central nervous system. All participants were paid for their time. The New York State Psychiatric Institute’s institutional review board approved the project, and all subjects provided written,
Behavioral data
Measures of item discrimination (dL) and response bias (cL) were based on logistic distributions in a signal detection model [57]. Button press performance, shown in Table 3, indicates that young subjects more accurately discriminated old and new words than the older subjects [F (1, 26)=31.7, P<0.001]. No differences were revealed between the two groups on the measure of response bias, as both groups were relatively conservative in their judgments. Young women also outperformed the older women
Discussion
A central aim of the current study was to revise our previous source memory paradigm [61] in order to improve the source accuracy of the older women to investigate whether, with enhanced source memory performance, they would exhibit the right prefrontal EM effect that is observed in the ERPs of the young. The higher source memory performance reported here suggests that the revisions made in the experimental protocol were successful in boosting the performance of the older adults. In fact,
Acknowledgements
The authors gratefully acknowledge Charles L. Brown III for computer programming and technical assistance, Charlotte Trott for assistance in task development and the volunteers for their time and cooperation. This study was supported in part by K01 AG00879-01 and R03 AG16396-01 from NIA (D.J.W. Ph.D., Principal Investigator) and AG05213 from NIA and K05 MH01225 from NIMH (D.F., Ph.D., Prinicipal Investigator).
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