An fMRI investigation of short-term source memory in young and older adults

doi:10.1016/j.neuroimage.2005.09.039

NeuroImage

Volume 30, Issue 2, 1 April 2006, Pages 627-633

https://doi.org/10.1016/j.neuroimage.2005.09.039 Get rights and content

Abstract

Using functional magnetic resonance imaging (fMRI) and a working memory procedure, we compared source memory judgments (format and location) with old–new judgments in young and older adults. Consistent with previous fMRI findings, for young adults, an area of left dorsolateral prefrontal cortex showed greater activity during format than old–new judgments made immediately, as well as those made after a brief, filled delay. In contrast, for older adults, activity in this area was not greater during format than old–new judgments at either retention interval. These data provide additional evidence that left lateral prefrontal cortex is important in monitoring specific source information and new evidence that older adults' source memory deficits may be related, in part, to reduced function of this brain area.

Section snippets

Participants

Young participants (n = 13 [6 females], M age = 25.0 years [SD = 3.2 years]) were healthy, college students who had not participated in our earlier short-term source monitoring studies. Older participants (n = 13 [7 females], M age = 67.4 years [SD = 2.6 years]) were healthy, independently living adults from surrounding communities. Data from one additional young participant were excluded because of excessive head movement. Young and older adults did not differ significantly on an abbreviated

Behavioral results

Fig. 2 shows accuracy, measured as d-prime. A 2 (Age) × 2 (Interval: immediate, delay) × 3 (Condition: ON, PW, LR) ANOVA showed a main effect of age (Ms = 2.22, 1.46 for young and older adults, respectively; F[1,24] = 15.67, MSe = 1.45, P < 0.001), main effect of condition (Ms = 2.28, 1.92, 1.32 for ON, PW, and LR, respectively; F[2,48] = 17.87, MSe = 0.69, P < 0.00001), and a main effect of interval (Ms = 2.26, 1.43 for immediate and delay trials, respectively; F[1,24] = 48.88, MSe = 0.55, P

General discussion

Behaviorally, under the current short-term memory conditions, older adults showed poorer old–new and source memory than did young adults. Long-term memory studies often show disproportionate age-related source memory deficits relative to item memory (e.g., Simons et al., 2004, Wegesin et al., 2000; see, e.g., Johnson et al., 1993, Spencer and Raz, 1995 for reviews). This is generally thought to reflect relatively preserved familiarity supporting item recognition and relatively disrupted

Acknowledgments

This research was supported by NIA grants AG09253 and AG15793. We thank Hedy Sarofin and Cheryl McMurray for technical assistance in fMRI data collection, and Joseph McGuire for help with figure preparation.

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Older adults often mistake new information as ‘old’, yet the mechanisms underlying this response bias remain unclear. Typically, false alarms by older adults are thought to reflect pattern completion – the retrieval of a previously encoded stimulus in response to partial input. However, other work suggests that age-related retrieval errors can be accounted for by deficient encoding processes. In the present study, we used eye movement monitoring to quantify age-related changes in behavioral pattern completion as a function of eye movements during both encoding and partially cued retrieval. Consistent with an age-related encoding deficit, older adults executed more gaze fixations and more similar eye movements across repeated image presentations than younger adults, and such effects were predictive of subsequent recognition memory. Analysis of eye movements at retrieval further indicated that in response to partial lure cues, older adults reactivated the similar studied image, indexed by the similarity between encoding and retrieval gaze patterns, and did so more than younger adults. Critically, reactivation of encoded image content via eye movements was associated with lure false alarms in older adults, providing direct evidence for a pattern completion bias. Together, these findings suggest that age-related changes in both encoding and retrieval processes, indexed by eye movements, underlie older adults' increased vulnerability to memory errors.
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Source memory is broadly defined as remembered information that specifies how an event was experienced, such as perceptual (e.g., color, format of a stimulus), spatial-temporal, and affective details (Glisky, Polster, & Routhieaux, 1995; Johnson, Hashtroudi, & Lindsay, 1993). A source memory task usually requires participants to retrieve associated information, such as which list a word was encountered on (e.g., Wilding & Rugg, 1996), whether a learned stimulus was presented in auditory or visual modality during study (e.g., Bornstein & LeCompte, 1995), or whether a stored semantic representation was acquired from a word or a picture (e.g., Mitchell, Johnson, Raye, & Greene, 2004; Mitchell, Raye, Johnson, & Greene, 2006). In the current study, as well as in Chen, Carlson, and Wyble (2018), the source memory refers to the memory of source format information of a semantic representation of a stimulus (e.g., whether a specific color representation was extracted from the color of a square or the identity of a color word).
Failing to remember the source of retrievable information is known as source amnesia. This phenomenon has been extensively investigated in long-term memory but rarely in working memory, as we share the intuition that the source information of an item that we have encountered in the immediate past is always available. However, a recent study (Chen, Carlson, & Wyble, 2018) challenged this common sense by showing the source amnesia for simple visual stimuli (e.g., colored square) in the context of working memory when participants did not expect having to report source information, which indicated that the source information of visual stimuli was not automatically encoded into working memory. The current study sought to further examine this newly discovered phenomenon by testing whether it persists with complex and meaningful stimuli in the visual modality (Experiments 1, 4a & 4b), cross-visual-and-auditory modalities (Experiments 2a & 2b), and within-auditory modality (Experiment 3). Interestingly, the results revealed that short-term source amnesia was a robust effect in the visual modality even for complex and meaningful stimuli, whereas it was absent in the cross-visual-and-auditory or within-auditory modalities, regardless of reporting expectation. This indicates differences in working memory representations of visual and auditory stimuli, namely, the representation of auditory stimuli was stored together with the corresponding original sources, while that of visual stimuli was stored independently of its source information. These findings have crucial implications for further clarifying the longstanding debate regarding whether or not there is a modality-independent working memory storage system for different modalities.
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There is considerable evidence for age-related decrements in source memory retrieval, but the literature on the neural correlates of these impairments is mixed. In this study, we used functional magnetic resonance imaging to examine source memory retrieval-related brain activity, and the monotonic relationship between retrieval-related brain activity and source memory accuracy, as a function of both healthy aging (younger vs older) and memory ability within the older adult group (Hi-Old vs Lo-Old). Participants studied lists of word pairs, half visually, half aurally; these were re-presented visually in a scanned test phase and participants indicated if the pair was ‘seen’ or ‘heard’ in the study phase. The Lo-Old, but not the Hi-Old, showed source memory performance decrements compared to the Young. During retrieval of source memories, younger and older adults engaged lateral and medial prefrontal cortex (PFC) and medial posterior parietal (and occipital) cortices. The groups differed in how brain activity related to source memory accuracy in dorsal anterior cingulate cortex, precuneus/cuneus, and the inferior parietal cortex; in each of these areas, greater activity was associated with poorer accuracy in the Young, but with higher accuracy in the Hi-Old (anterior cingulate and precuneus/cuneus) and Lo-Old (inferior parietal lobe). Follow-up pairwise group interaction analyses revealed that greater activity in right parahippocampal gyrus was associated with better source memory in the Hi-Old, but not in the Lo-Old. We conclude that older adults recruit additional brain regions to compensate for age-related decline in source memory, but the specific regions involved differ depending on their episodic memory ability.
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However, older participants were less likely to claim that the falsely identified object was presented in the same location as the similar perceived object, suggesting that perceptual and contextual features of the studied stimuli are less tightly bound with age. In line with this idea, older adults engage the hippocampus and lateral PFC areas less than younger adults during successful source encoding, reflective of decreased relational processing (Dennis et al., 2008a, 2007; Dulas and Duarte, 2014; Mitchell et al., 2006). During source retrieval, older adults also show reduced event-related potential (ERP) correlates of recollection (manifesting as a weaker parietal old-new effect, Dulas and Duarte, 2013).
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Rapid CommunicationAn fMRI investigation of short-term source memory in young and older adults

Abstract

Section snippets

Participants

Behavioral results

General discussion

Acknowledgments

NeuroImage

Neuropsychologia

Comput. Biomed. Res.

J. Exp. Child Psych.

Neuron

Neuropsychologia

NeuroImage

Biol. Psychol.

Trends Cogn. Sci.

Cogn. Brain Res.

Trends Cogn. Sci.

Trends Cogn. Sci.

NeuroImage

Neuropsychologia

Cogn. Brain Res.

Hemispheric asymmetry reduction in older adults: the HAROLD model

Psychol. Aging

Imaging cognition II: an empirical review of 275 PET and fMRI studies

J. Cogn. Neurosci.

Lateralization of prefrontal activity during episodic memory retrieval: evidence for the production-monitoring hypothesis

J. Cogn. Neurosci.

Feature memory and binding in young and older adults

Mem. & Cog.

An embedded-processes model of working memory

Relations between source amnesia and frontal lobe functioning in older adults

Psychol. Aging

The Human Brain: Surface, Three-Dimensional Sectional Anatomy with MRI, and Blood Supply

Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold

Magn. Reson. Med.

Double dissociation between item and source memory

Neuropsychology

Hippocampal formation size predicts declining memory performance in normal aging

Neurology

Aging and the neural correlates of successful picture encoding: frontal activations compensate for deactivations

J. Cogn. Neurosci.

Aging and source monitoring: cognitive processes and neuropsychological correlates

J. Exp. Psychol. Gen.

Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis

Brain

MEM: mechanisms of recollection

J. Cogn. Neurosci.

Emotion and MEM

Source monitoring

Psychol. Bull.

Aging and single versus multiple cues in source monitoring

Psychol. Aging

Rapid Communication
An fMRI investigation of short-term source memory in young and older adults