Ian M. McDonough

Age-Related Differences in Prefrontal Cortex Activity during Retrieval Monitoring: Testing the Compensation and Dysfunction Accounts

Current theories of cognitive aging emphasize that the prefrontal cortex might not only be a major source of dysfunction but also a source of compensation. We evaluated neural activity associated with retrieval monitoring--or the selection and evaluation of recollected information during memory retrieval--for evidence of dysfunction or compensation. Younger and older adults studied pictures and words and were subsequently given criterial recollection tests during event-related functional magnetic resonance imaging. Although memory accuracy was greater on the picture test than the word test in both groups, activity in right dorsolateral prefrontal cortex (DLPFC) was associated with greater retrieval monitoring demands (word test > picture test) only in younger adults. Similarly, DLPFC activity was consistently associated with greater item difficulty (studied > nonstudied) only in younger adults. Older adults instead exhibited high levels of DLPFC activity for all of these conditions, and activity was greater than younger adults even when test performance was naturally matched across the groups (picture test). Correlations also differed between DLPFC activity and test performance across the groups. Collectively, these findings are more consistent with accounts of DLPFC dysfunction than compensation, suggesting that aging disrupts the otherwise beneficial coupling between DLPFC recruitment and retrieval monitoring demands.

Dissociating source memory decisions in the prefrontal cortex: Fmri of diagnostic and disqualifying monitoring

We used event-related fMRI to study two types of retrieval monitoring that regulate episodic memory accuracy: diagnostic and disqualifying monitoring. Diagnostic monitoring relies on expectations, whereby the failure to retrieve expected recollections prevents source memory misattributions (sometimes called the distinctiveness heuristic). Disqualifying monitoring relies on corroborative evidence, whereby the successful recollection of accurate source information prevents misattribution to an alternative source (sometimes called recall to reject). Using criterial recollection tests, we found that orienting retrieval toward distinctive recollections (colored pictures) reduced source memory misattributions compared with a control test in which retrieval was oriented toward less distinctive recollections (colored font). However, the corresponding neural activity depended on the type of monitoring engaged on these tests. Rejecting items based on the absence of picture recollections (i.e., the distinctiveness heuristic) decreased activity in dorsolateral prefrontal cortex relative to the control test, whereas rejecting items based on successful picture recollections (i.e., a recall-to-reject strategy) increased activity in dorsolateral prefrontal cortex. There also was some evidence that these effects were differentially lateralized. This study provides the first neuroimaging comparison of these two recollection-based monitoring processes and advances theories of prefrontal involvement in memory retrieval.

Network complexity as a measure of information processing across resting-state networks: evidence from the Human Connectome Project.

An emerging field of research focused on fluctuations in brain signals has provided evidence that the complexity of those signals, as measured by entropy, conveys important information about network dynamics (e.g., local and distributed processing). While much research has focused on how neural complexity differs in populations with different age groups or clinical disorders, substantially less research has focused on the basic understanding of neural complexity in populations with young and healthy brain states. The present study used resting-state fMRI data from the Human Connectome Project (Van Essen et al., 2013) to test the extent that neural complexity in the BOLD signal, as measured by multiscale entropy (1) would differ from random noise, (2) would differ between four major resting-state networks previously associated with higher-order cognition, and (3) would be associated with the strength and extent of functional connectivity—a complementary method of estimating information processing. We found that complexity in the BOLD signal exhibited different patterns of complexity from white, pink, and red noise and that neural complexity was differentially expressed between resting-state networks, including the default mode, cingulo-opercular, left and right frontoparietal networks. Lastly, neural complexity across all networks was negatively associated with functional connectivity at fine scales, but was positively associated with functional connectivity at coarse scales. The present study is the first to characterize neural complexity in BOLD signals at a high temporal resolution and across different networks and might help clarify the inconsistencies between neural complexity and functional connectivity, thus informing the mechanisms underlying neural complexity.

Age-related positivity effects and autobiographical memory detail: evidence from a past/future source memory task.

This study investigated whether the age-related positivity effect strengthens specific event details in autobiographical memory. Participants retrieved past events or imagined future events in response to neutral or emotional cue words. Older adults rated each kind of event more positively than younger adults, demonstrating an age-related positivity effect. We next administered a source memory test. Participants were given the same cue words and tried to retrieve the previously generated event and its source (past or future). Accuracy on this source test should depend on the recollection of specific details about the earlier generated events, providing a more objective measure of those details than subjective ratings. We found that source accuracy was greater for positive than negative future events in both age groups, suggesting that positive future events were more detailed. In contrast, valence did not affect source accuracy for past events in either age group, suggesting that positive and negative past events were equally detailed. Although ageing can bias people to focus on positive aspects of experience, this bias does not appear to strengthen the availability of details for positive relative to negative past events.

The Dynamic Aging Mind Revelations From Functional Neuroimaging Research

The conception of the aging mind that emerged from behavioral and structural imaging studies portrayed the mind as a victim of passive deterioration and decline with age, with a few domains of preserved function. The advent of functional neuroimaging has demonstrated that the aging brain is an adaptive and plastic structure that responds dynamically to cognitive challenge and structural deterioration—thus, fundamentally changing views of cognitive aging. In addition, a neural theory of the aging mind based on behavioral data—the dedifferentiation view of cognitive aging—was largely confirmed when neuroimaging technology became available to test it. We argue that functional neuroimaging has advanced cognitive aging theories by creating a stronger emphasis on compensatory mechanisms related to brain plasticity and potential reorganization as evidenced by the resurgence of interest and research in cognitive training research designed to improve cognition through enhancement of neural structures or reorganization of functional circuitry.

Autobiographical elaboration reduces memory distortion: cognitive operations and the distinctiveness heuristic.

Retrieval monitoring enhances episodic memory accuracy. For instance, false recognition is reduced when participants base their decisions on more distinctive recollections, a retrieval monitoring process called the distinctiveness heuristic. The experiments reported here tested the hypothesis that autobiographical elaboration during study (i.e., generating autobiographical memories in response to cue words) would lead to more distinctive recollections than other item-specific encoding tasks, enhancing retrieval monitoring accuracy at test. Consistent with this hypothesis, false recognition was less likely when participants had to search their memory for previous autobiographical elaborations, compared to previous semantic judgments. These false recognition effects were dissociated from true recognition effects across four experiments, implicating a recollection-based monitoring process that was independent from familiarity-based processes. Separately obtained subjective measures provided converging evidence for this conclusion. The cognitive operations engaged during autobiographical elaboration can lead to distinctive recollections, making them less prone to memory distortion than other types of deep or semantic encoding.

Memory’s Aging Echo: Age-related Decline in Neural Reactivation of Perceptual Details During Recollection

Episodic memory decline is a hallmark of normal cognitive aging. Here, we report the first event-related fMRI study to directly investigate age differences in the neural reactivation of qualitatively rich perceptual details during recollection. Younger and older adults studied pictures of complex scenes at different presentation durations along with descriptive verbal labels, and these labels subsequently were used during fMRI scanning to cue picture recollections of varying perceptual detail. As expected from prior behavioral work, the two age groups subjectively rated their recollections as containing similar amounts of perceptual detail, despite objectively measured recollection impairment in older adults. In both age groups, comparisons of retrieval trials that varied in recollected detail revealed robust activity in brain regions previously linked to recollection, including hippocampus and both medial and lateral regions of the prefrontal and posterior parietal cortex. Critically, this analysis also revealed recollection-related activity in visual processing regions that were active in an independent picture-perception task, and these regions showed age-related reductions in activity during recollection that cannot be attributed to age differences in response criteria. These fMRI findings provide new evidence that aging reduces the absolute quantity of perceptual details that are reactivated from memory, and they help to explain why aging reduces the reliability of subjective memory judgments.

Impaired retrieval monitoring for past and future autobiographical events in older adults.

Older adults are more likely than younger adults to confuse real and imagined events in episodic memory. This deficit may be attributed to a reduction in the specific features available for recollection (i.e., retrieval success) or to a deficit in the search and decision processes operating during recollection attempts (i.e., retrieval monitoring). The present experiments used a two-phase event-generation task to manipulate retrieval success and test for age-related deficits in retrieval monitoring. In the first phase, participants generated real autobiographical events from their past and imagined plausible future events in response to cue words. We used elaboration instructions to experimentally manipulate the amount of features associated with these generated events. In the second phase administered 24 hours later, we gave recollection tests that required participants to discriminate between these previously generated past and future events in memory. As predicted, the elaboration manipulation increased the amount of features that could be recollected in association with the generated events in both age groups (including cognitive operations in Experiment 1 and perceptual details in Experiment 2). However, older adults were more likely than younger adults to confuse past and future events in memory, and critically, elaboration did not minimize these age-related confusions. These findings imply that aging impairs the ability to accurately monitor retrieval for features that are characteristic of autobiographical events, above and beyond age-related impairments in the retrieval of the recollected information itself.

Separating past and future autobiographical events in memory: Evidence for a reality monitoring asymmetry

After thinking about the past and imagining the future, how do people separate these real and imagined events in memory? We had subjects engage in past and future autobiographical elaboration, then later take memory tests that required them to recollect these earlier generated events. In Experiment 1, testing memory for previously generated past or future autobiographical events led to fewer source memory confusions than did an elaborative control task, suggesting that the distinctive features of autobiographical elaboration improved subsequent retrieval monitoring accuracy. In Experiment 2, we directly compared retrieval monitoring accuracy for previously generated past and future autobiographical events and found that subjects made fewer source confusions when searching memory for future events. This asymmetry suggests that the features characterizing future elaborations (e.g., cognitive operations) were used more effectively during reality monitoring than were the features characterizing past elaborations (e.g., perceptual details), and has implications for future-oriented theories of memory.

The Synapse Project: Engagement in mentally challenging activities enhances neural efficiency

Purpose: Correlational and limited experimental evidence suggests that an engaged lifestyle is associated with the maintenance of cognitive vitality in old age. However, the mechanisms underlying these engagement effects are poorly understood. We hypothesized that mental effort underlies engagement effects and used fMRI to examine the impact of high-challenge activities (digital photography and quilting) compared with low-challenge activities (socializing or performing low-challenge cognitive tasks) on neural function at pretest, posttest, and one year after the engagement program. Methods: In the scanner, participants performed a semantic-classification task with two levels of difficulty to assess the modulation of brain activity in response to task demands. Results: The High-Challenge group, but not the Low-Challenge group, showed increased modulation of brain activity in medial frontal, lateral temporal, and parietal cortex—regions associated with attention and semantic processing—some of which were maintained a year later. This increased modulation stemmed from decreases in brain activity during the easy condition for the High-Challenge group and was associated with time committed to the program, age, and cognition. Conclusions: Sustained engagement in cognitively demanding activities facilitated cognition by increasing neural efficiency. Mentally-challenging activities may be neuroprotective and an important element to maintaining a healthy brain into late adulthood.