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Sander, M. C.

Publications and source records attributed to Sander, M. C..

15 recordsLinked to original sources

Age differences in functional connectivity track dedifferentiation of category representations

With advancing age, the distinctiveness of neural representations of information declines. While the finding of this so-called age-related neural dedifferentiation in category-selective neural regions is well-described, how neural dedifferentiation manifests at the level of large-scale functional networks is less understood. Furthermore, the relationship between age-related changes in network organization and dedifferentiation is unknown. Here, we investigated age-related neural dedifferentiation of category-selective regions as well as whole-brain functional networks. We additionally examined age differences in connectivity of category-selective regions to the rest of the brain. Younger and older adults viewed blocks of face and house stimuli while performing memory encoding and retrieval in the fMRI scanner. We found an age-related decline in neural distinctiveness for faces in the fusiform gyrus (FG) and for houses in the parahippocampal gyrus (PHG). Functional connectivity analyses revealed age-related dedifferentiation of global network structure as well as age differences in the connectivity profiles to category-selective regions. Together, our findings suggest that age-related neural dedifferentiation manifests both in regional categorical representations as well as in whole- brain functional networks. HighlightsO_LICategory representations are less distinctive, or dedifferentiated, in older adults C_LIO_LIFunctional networks are less segregated in older adults C_LIO_LIOlder adults reveal less connectivity between fusiform gyrus and visual cortices C_LI

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Age differences in neural distinctiveness during memory retrieval versus reinstatement

Robust evidence points to mnemonic deficits in older adults related to dedifferentiated, i.e., less distinct, neural responses during memory encoding. However, less is known about retrieval-related dedifferentiation and its role in age-related memory decline. In this study, younger and older adults were scanned both while incidentally learning face and house stimuli and while completing a surprise recognition memory test. Using pattern similarity searchlight analyses, we looked for indicators of neural dedifferentiation during retrieval and asked whether this might explain interindividual differences in memory performance. Our findings revealed age-related reductions in neural distinctiveness during memory retrieval as well as in encoding-retrieval reinstatement in visual processing regions. We further demonstrated that the degree to which patterns elicited during encoding were reinstated during retrieval tracked variability in memory performance better than retrieval-related distinctiveness only. All in all, we contribute to meager existing evidence for age-related neural dedifferentiation during memory retrieval. We propose that the recognition task (as opposed to a cued recall task) may have revealed impairment in perceptual processing in older adults, leading to particularly widespread age differences in neural distinctiveness. We additionally provide support for the idea that well-defined reactivation of encoding patterns plays a major role in successful memory retrieval.

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Out of rhythm: Compromised precision of theta-gamma coupling impairs associative memory in old age

Episodic memory declines with advancing adult age. This decline is particularly pronounced when associations between items and their contexts need to be formed. According to theories of neural communication, the precise coupling of gamma power to the phase of the theta rhythm supports associative memory formation. To investigate whether age differences in associative memory are related to compromised theta-gamma coupling, we took electroencephalographic (EEG) recordings during the encoding phase of an item-context association task. Fifty-eight younger and 55 older adults studied pictures of objects superimposed on background scenes. In a recognition test, objects were presented on old or new backgrounds, and participants responded if they had seen (1) the object and (2) the object-scene pair. Theta-gamma coupling supported pair memory formation in both age groups. Whereas pair memory was associated with coupling closer to the peak of the theta rhythm, item-only memory was associated with a deviation in phase angle relative to pair memory. Furthermore, a stable relation between coupling phase and pair memory performance demonstrated that coupling closer to the peak is beneficial for associative memory. Critically, older adults lower pair memory was accompanied by a shift in coupling phase relative to younger adults. In concert, the present results are consistent with the hypothesis that decrements in the precision with which gamma power is coupled to the theta phase underlie the decline of associative memory in normal cognitive aging. Significance StatementAccording to prominent theories of neural communication, the precise coordination of oscillatory activity enables the formation of associative memories. We propose that normal cognitive aging impairs associative memory formation by compromising the precision of neural communication. We show that the coupling of high-frequency gamma power to low-frequency theta phase supports associative memory formation in both younger and older adults, with coupling closer to the theta peak benefitting memory performance. However, compared to younger adults, the coupling phase angle is shifted and more variable in older adults. We conclude that alterations in the precision of theta-gamma coupling contribute to adult age differences in associative memory.

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Age-related declines in neural selectivity manifest differentially during encoding and recognition

The authors have withdrawn the preprint due to two errors in the analyses: The first error was a failure to account for three dummy volumes (TR = 2s) collected at the beginning of each experimental run. The second error was a coding error related to the definition of the category-selective clusters. Since correcting for these errors drastically altered the results and conclusions of this paper, the authors have withdrawn the preprint and retracted the published paper (https://doi.org/10.1016/j.neurobiolaging.2021.12.001). A report comparing original and corrected results can be found on https://osf.io/7n3mz/. If you have any questions please contact the corresponding author (sander@mpib-berlin.mpg.de).

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Memory specificity is linked to repetition effects in event-related potentials across the lifespan

The specificity with which past experiences can be remembered varies across the lifespan, possibly due to differences in how precisely information is encoded. Memory formation can be investigated through repetition effects, the common finding that neural activity is altered when stimuli are repeated. However, whether differences in this indirect measure of memory formation relate to lifespan differences in memory specificity has not yet been established. In the present study, we examined repetition effects in event-related potentials and their relation to recognition. During incidental encoding, children (aged 7-9 years), young adults (18-30 years), and older adults (65-76 years) viewed repeated object images from different categories. During subsequent recognition, we distinguished memory for the specific items versus the general categories. We identified repetition suppression in all age groups, and repetition enhancement for adults. Furthermore, individual item recognition performance comprising lure discrimination was positively associated with the magnitude of the neural repetition effects, which did not differ between groups, indicating common neural mechanisms of memory formation. Our findings demonstrate that neural repetition effects reflect the formation of highly specific memory representations and highlight their significance as a neural indicator of individual differences in episodic memory encoding across the lifespan.

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Tracking age differences in neural distinctiveness across representational levels

The authors have withdrawn the preprint due to two errors in the analyses: The first error was a failure to account for three dummy volumes (TR = 2s) collected at the beginning of each experimental run. The second error was a coding error related to the definition of the category-selective clusters. Since correcting for these errors drastically altered the results and conclusions of this paper, the authors have withdrawn the preprint and retracted the published paper. More information as well as a report comparing original and corrected results can be found on https://osf.io/t8dpv/. If you have any questions please contact the corresponding author (sander@mpib-berlin.mpg.de).

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Item recognition and lure discrimination in younger and older adults are supported by alpha/beta desynchronization

Our episodic memories vary in their specificity, ranging from a mere sense of familiarity to detailed recollection of the initial experience. Recent work suggests that alpha/beta desynchronization promotes information flow through the cortex, tracking the richness in detail of recovered memory representations. At the same time, as we age, memories become less vivid and detailed, which may be reflected in age-related reductions in alpha/beta desynchronization during retrieval. To understand age differences in the specificity of episodic memories, we investigated differences in alpha/beta desynchronization between younger (18-26 years, n = 31) and older (65-76 years, n = 27) adults during item recognition and lure discrimination. Alpha/beta desynchronization increased linearly with the demand for memory specificity, i.e., the requirement to retrieve details for an accurate response, across retrieval situations (correct rejections < item recognition < lure discrimination). Stronger alpha/beta desynchronization was related to memory success, as indicated by reliable activation differences between correct and incorrect memory responses. In line with the assumption of a loss of mnemonic detail in older age, older adults had more difficulties than younger adults to discriminate lures from targets. Importantly, they also showed a reduced modulation of alpha/beta desynchronization across retrieval demands. Together, these results extend previous findings by demonstrating that alpha/beta desynchronization dissociates between item recognition and the retrieval of highly detailed memories as required in lure discrimination, and that age-related impairments in episodic retrieval are accompanied by attenuated modulations in the alpha/beta band. Thus, we provide novel findings suggesting that alpha/beta desynchronization tracks mnemonic specificity and that changes in these oscillatory mechanisms may underlie age-related declines in episodic memory.

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Hippocampal and parahippocampal grey matter structural integrity assessed by multimodal imaging is associated with episodic memory in old age

Maintained structural integrity of hippocampal and cortical grey matter may explain why some older adults show rather preserved episodic memory. However, viable measurement models for estimating individual differences in grey matter structural integrity are lacking; instead, findings rely on fallible single indicators of integrity. Here, we introduce multitrait-multimethod (MTMM) methodology to capture individual differences in grey matter integrity, based on multimodal structural imaging in a large sample of 1,522 healthy adults aged 60 to 88 years from the Berlin Aging Study II, including 331 participants who underwent MR imaging. Structural integrity factors expressed the common variance of voxel-based morphometry (VBM), mean diffusivity (MD), and magnetization transfer ratio (MT) for each of four regions of interest (ROI): hippocampus, parahippocampal gyrus, prefrontal cortex, and precuneus. Except for precuneus, the integrity factors correlated with episodic memory. Associations with hippocampal and parahippocampal integrity persisted after controlling for age, sex, and education. Our results support the proposition that episodic memory ability in old age benefits from maintained structural integrity of hippocampus and parahippocampal gyrus. Exploratory follow-up analyses on sex differences showed that this effect is restricted to men. Multimodal factors of structural brain integrity might help improve our biological understanding of human memory aging.

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Age Differences in Hemispheric Lateralization in Spatial and Verbal Visual Working Memory

Due to hemispheric specialization of the human brain, neural signatures of visual working memory (WM) performance are expected to differ between tasks involving verbal versus spatial memoranda. Theories of cognitive aging suggest a reduction of hemispheric specialization in older adults. Using behavioral and neural WM capacity markers, we assessed hemispheric lateralization in younger and older adults performing a spatial or verbal visual WM task. Participants encoded information presented in the left or right hemifield. We observed behavioral advantages for spatial stimuli processed in the right hemisphere and for verbal stimuli processed in the left hemisphere. While younger adults showed lateralization in both tasks, older adults showed lateralization only in the verbal task. Lateralization was assessed by the contralateral delay activity (CDA) on the neural level. CDA amplitudes displayed hemispheric lateralization for verbal versus spatial material, but this effect was age-invariant. While our findings support right-hemispheric specialization for spatial information maintenance, and left-hemispheric specialization for verbal information maintenance, we could not confirm a generalized reduction in hemispheric lateralization at older ages.

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Noradrenergic responsiveness preserves selective attention across the adult life span

Selectively attending to relevant information while blocking out distractors is crucial for goal-directed behavior, yet with advancing age, deficits emerge in attentional selectivity. Decrements in attention have been associated with altered noradrenergic activity in animals. However, research linking noradrenergic functioning to attention in aging humans is scarce, likely reflecting long-standing methodological challenges in non-invasive assessments. We studied whether age-related differences in the noradrenergic system predict differences in attention. We measured pupil dilation, a non-invasive marker of phasic norepinephrine (NE) release, while concurrently recording the electroencephalogram (EEG), of younger (N=39[male]; 25.2{+/-}3.2 years) and older adults (N=38[male]; 70.6{+/-}2.7 years). NE release was triggered on a trial-by-trial basis using fear-conditioned (CS+) stimuli. During conditioning, pupil and EEG markers related to heightened NE activity were identified. Afterwards, in a dichotic listening task, participants were cued to direct attention to either the left or right ear while highly similar syllable pairs were presented simultaneously to both ears. During the dichotic listening task, presentation of fear-conditioned stimuli reinstated the acquired fear response, as reflected in pupil and EEG alpha-beta-band responses. Critically, pupil dilation to CS+ was correlated with stronger EEG alpha-beta desynchronization, suggesting a common dependence on NE release. On a behavioral level, NE release facilitated attention. In particular, structural equation modeling revealed that the responsiveness of the NE system is associated with attention on a latent construct level, measured by several indicator tasks. Overall, our results suggest that the responsiveness of the NE system supports attention across the life span. Significance statementIn old age the ability to selectively process relevant aspects of the environment fades. Animal research suggests that the neuromodulator norepinephrine helps to maintain selective attention. We tested younger and older adults across a variety of attention tasks. In addition, we used arousing stimuli to experimentally activate participants noradrenergic system while recording pupillometry and electroencephalography (EEG) to infer its functional capacity. Older adults showed compromised attention and reduced noradrenergic responsiveness as indicated by interrelated pupil and EEG markers. Crucially, in both age groups a more responsive noradrenergic system was strongly associated to attention. Our findings link animal and human studies on the neural underpinning of attention in aging and underscore the importance of the noradrenergic system in late life cognition.

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Memory quality modulates the effect of aging on memory consolidation during sleep: Reduced maintenance but intact gain

Successful consolidation of associative memories relies on the coordinated interplay of slow oscillations and sleep spindles during non-rapid eye movement (NREM) sleep, enabling the transfer of labile information from the hippocampus to permanent memory stores in the neocortex. During senescence, the decline of the structural and functional integrity of the hippocampus and neocortical regions is paralleled by changes of the physiological events that stabilize and enhance associative memories during NREM sleep. However, the currently available evidence is inconclusive if and under which circumstances aging impacts memory consolidation. By tracing the encoding quality of single memories in individual participants, we demonstrate that previous learning determines the extent of age-related impairments in memory consolidation. Specifically, the detrimental effects of aging on memory maintenance were greatest for mnemonic contents of medium encoding quality, whereas memory gain of weakly encoded memories did not differ by age. Using multivariate techniques, we identified profiles of alterations in sleep physiology and brain structure characteristic for increasing age. Importantly, while both aged sleep and aged brain structure profiles were associated with reduced memory maintenance, inter-individual differences in neither sleep nor structural brain integrity qualified as the driving force behind age differences in sleep-dependent consolidation in the present study.

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Oscillatory Mechanisms of Successful Memory Formation in Younger and Older Adults Are Related to Structural Integrity

We studied oscillatory mechanisms of successful memory formation in 47 younger and 52 older adults in an intentional associative memory task with cued recall. While older adults showed reduced memory performance, we found subsequent memory effects (SME) in alpha/beta and theta frequency bands in both age groups. Using logistic mixed effect models, we then investigated whether interindividual differences in structural integrity of memory regions that were functionally linked to oscillatory dynamics in previous studies (Hanslmayr et al., 2011) could account for interindividual differences in the strength of the SME. Structural integrity of inferior frontal gyrus (IFG) and hippocampus (HC) was reduced in older adults. SME in the alpha/beta band were indeed modulated by the cortical thickness of inferior frontal gyrus (IFG), in line with its hypothesized role for deep semantic elaboration. Importantly, this structure-function relationship did not differ by age group. However, older adults were more frequently represented among the participants with low cortical thickness and consequently weaker SME in the alpha band. Thus, our results suggest that differences in the structural integrity of the IFG are the basis not only for interindividual, but also for age differences in memory formation.

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Neural pattern similarity differentially affects memory performance of younger and older adults

Age-related memory decline is associated with changes in neural functioning but little is known about how aging affects the quality of information representation in the brain. Whereas a long-standing hypothesis of the aging literature links cognitive impairments to less distinct neural representations in old age, memory studies have shown that high similarity between activity patterns benefits memory performance for the respective stimuli. Here, we addressed this apparent conflict by investigating between-item representational similarity in 50 younger (19-27 years old) and 63 older (63-75 years old) human adults (male and female) who studied scene-word associations using a mnemonic imagery strategy while electroencephalography was recorded. We compared the similarity of spatiotemporal frequency patterns elicited during encoding of items with different subsequent memory fate. Compared to younger adults, older adults memory representations were more similar to each other but items that elicited the most similar activity patterns early in the encoding trial were those that were best remembered by older adults. In contrast, young adults memory performance benefited from decreased similarity between earlier and later periods in the encoding trials, which might reflect their better success in forming unique memorable mental images of the joint picture-word pair. Our results advance the understanding of the representational properties that give rise to memory quality as well as how these properties change in the course of aging. Significance statementDeclining memory abilities are one of the most evident limitations for humans when growing older. Despite recent advances of our understanding of how the brain represents and stores information in distributed activation patterns, little is known about how the quality of information representation changes during aging and thus affects memory performance. We investigated how the similarity between neural representations relates to subsequent memory quality in younger and older adults. We present novel evidence that the interaction of pattern similarity and memory performance differs between age groups: Older adults benefited from increased similarity during early encoding whereas young adults benefited from decreased similarity between early and later encoding. These results provide insights into the nature of memory and age-related memory deficits.

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Cue-related phase reset accounts for age differences in phasic alerting

Alertness is fundamental for the efficiency of information processing. A persons level of alertness refers to the systems state of general responsiveness, and can be temporarily increased by presenting a neutral warning cue shortly before an event occurs (Posner & Petersen, 1990). However, effects of alerts on subsequent stimulus processing are less consistent in older than in younger individuals. In this study, we investigated the neural underpinnings of age differences in processing of auditory alerting cues. We measured electroencephalographic power and phase locking in response to alerting cues in a visual letter report task, in which younger but not older adults showed a cue-related behavioral advantage.\n\nAlerting cues evoked a significant increase in power as well as in inter-trial phase locking, with a maximum effect in the alpha frequency (8-12 Hz) in both age groups. Importantly, these cue-related increases in phase locking and power were stronger in older than in younger adults and were negatively correlated with the behavioral alerting effect in the older sample.\n\nOur results are in accordance with the assumption that older adults neural responses may be more strongly driven by external input and less variable than younger adults. A stronger resetting of the system in response to the auditory cue may have hindered older adults effective use of the warning signal to foster processing of the following visual stimulus.

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Youth-like Precision of Slow Oscillation-Spindle Coupling Promotes Memory Consolidation Across the Adult Lifespan

Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO) and sleep spindles (SP) and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that the fine-tuned SO-SP coupling that is present in younger adults diffuses with advanced age and shifts both in time and frequency. Crucially, we show that the tight precision of SO-SP coupling promotes memory consolidation in younger and older adults, and that brain integrity in source regions for the generation of SOs and SPs reinforces this beneficial SO-SP coupling in old age. Our results reveal age-related differences in SO-SP coupling in healthy elderly individuals. Furthermore, they broaden our understanding of the conditions and the functional significance of SO-SP coupling across the entire adult lifespan.

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