Speaker Competence Affects Prefrontal Theta and Occipital Alpha Power during Selective Word Learning in Preschoolers.

In the present study, we investigated the cognitive processes underlying selective word learning in preschoolers. We measured rhythmic neural activity in the theta (4-8 Hz) and alpha frequency range (7-12 Hz) in 67 four-year-olds. EEG was recorded during anticipation and encoding of novel labeling events performed by a speaker who had previously shown either competence (correct) or incompetence (incorrect) in labeling familiar objects. In both groups, children selected the target object equally often upon recall. However, children observing the incompetent speaker revealed weaker representations of novel words indicated by an increased likelihood for selecting familiar but incorrect items upon recall. Modulations in theta and alpha power suggest differential processing of novel label-object pairs depending on the speakers' competence. In the incompetent, but not the competent, speaker condition, increases in prefrontal theta power during anticipation and encoding were related to increased recall success. Findings suggest that theta power in the present study reflects cognitive control. In both conditions, occipital alpha power-indicating attentional processes-reflected familiarity with novel items, but in opposite directions. In familiar item trials, alpha power was increased observing the incompetent and decreased observing the competent speaker. Thus, both cognitive control and attention processes during word learning are differentially affected by speaker characteristics.

Early visual cortices reveal interrelated item and category representations in aging.

Neural dedifferentiation, the finding that neural representations tend to be less distinct in older adults compared with younger adults, has been associated with age-related declines in memory performance. Most studies assessing the relation between memory and neural dedifferentiation have evaluated how age impacts the distinctiveness of neural representations for different visual categories (e.g., scenes and objects). However, how age impacts the quality of neural representations at the level of individual items is still an open question. Here, we present data from an age-comparative fMRI study that aimed to understand how the distinctiveness of neural representations for individual stimuli differs between younger and older adults and relates to memory outcomes. Pattern similarity searchlight analyses yielded indicators of neural dedifferentiation at the level of individual items as well as at the category level in posterior occipital cortices. We asked whether age differences in neural distinctiveness at each representational level were associated with inter- and/or intraindividual variability in memory performance. While age-related dedifferentiation at both the item and category level related to between-person differences in memory, neural distinctiveness at the category level also tracked within-person variability in memory performance. Concurrently, neural distinctiveness at the item level was strongly associated with neural distinctiveness at the category level both within and across participants, elucidating a potential representational mechanism linking item- and category-level distinctiveness. In sum, we provide evidence that age-related neural dedifferentiation co-exists across multiple representational levels and is related to memory performance.Significance Statement Age-related memory decline has been associated with neural dedifferentiation, the finding that older adults have less distinctive neural representations than younger adults. This has been mostly shown for category information, while evidence for age differences in the specificity of item representations is meager. We used pattern similarity searchlight analyses to find indicators of neural dedifferentiation at both levels of representation (category and item) and linked distinctiveness to memory performance. Both item- and category-level dedifferentiation in the calcarine cortex were related to interindividual differences in memory performance, while category-level distinctiveness further tracked intraindividual variability. Crucially, neural distinctiveness was strongly tied between the item and category levels, indicating that intersecting representational properties of posterior occipital cortices reflect both individual exemplars and categories.

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, the contribution of age-related changes in network organization to dedifferentiation is unknown. Here, we asked whether age differences in a) whole-brain network segregation (i.e., network dedifferentiation) and b) functional connectivity to category-selective neural regions contribute to regional dedifferentiation of categorical representations. Younger and older adults viewed blocks of face and house stimuli 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 connectivity between the FG and early visual cortices. Interindividual correlations demonstrated that regional distinctiveness was related to network segregation as well as connectivity of the FG to the visual network. Together, our findings reveal that dedifferentiation of categorical representations may be linked to age-related reorganization of functional networks.

Grey-matter structure in cortical and limbic regions correlates with general cognitive ability in old age.

According to the maintenance hypothesis (Nyberg et al., 2012), structural integrity of the brain's grey matter helps to preserve cognitive functioning into old age. A corollary of this hypothesis that can be tested in cross-sectional data is that grey-matter structural integrity and general cognitive ability are positively associated in old age. Building on Köhncke et al. (2021), who found that region-specific latent factors of grey-matter integrity are positively associated with episodic memory ability among older adults, we examine associations between general factors of grey-matter integrity and a general factor of cognitive ability in a cross-sectional sample of 1466 participants aged 60-88 years, 319 of whom contributed imaging data. Indicator variables based on T1-weighted images (voxel-based morphometry, VBM), magnetization-transfer imaging (MT), and diffusion tensor imaging-derived mean diffusivity (MD) had sufficient portions of variance in common to establish latent factors of grey-matter structure for a comprehensive set of regions of interest (ROI). Individual differences in grey-matter factors were positively correlated across neocortical and limbic areas, allowing for the definition of second-order, general factors for neocortical and limbic ROI, respectively. Both general grey-matter factors were positively correlated with general cognitive ability. For the basal ganglia, the three modality-specific indicators showed heterogenous loading patterns, and no reliable associations of the general grey-matter factor to general cognitive ability were found. To provide more direct tests of the maintenance hypothesis, we recommend applying the present structural modeling approach to longitudinal data, thereby enhancing the physiological validity of latent constructs of brain structure.

Age differences in neural distinctiveness during memory encoding, retrieval, and 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 encoding, retrieval, and encoding-retrieval reinstatement. Our findings revealed age-related reductions in neural distinctiveness during all memory phases in visual processing regions. Interindividual differences in retrieval- and reinstatement-related distinctiveness were strongly associated with distinctiveness during memory encoding. Both item- and category-level distinctiveness predicted trial-wise mnemonic outcomes. We further demonstrated that the degree of neural distinctiveness during encoding tracked interindividual variability in memory performance better than both retrieval- and reinstatement-related distinctiveness. All in all, we contribute to meager existing evidence for age-related neural dedifferentiation during memory retrieval. We show that neural distinctiveness during retrieval is likely tied to recapitulation of encoding-related perceptual and mnemonic processes.

Altered alpha/beta desynchronization during item-context binding contributes to the associative deficit in older age.

It is proposed that older adults have difficulties to bind item and context and to recruit deep, elaborative processing during encoding. Senescent changes in the oscillatory foundations of these processes are currently unclear. We recorded electroencephalography during item-context memory formation in younger (n = 57) and older (n = 55) adults. At test, we assessed memory for the items and the item-context pairs and examined encoding-related activity based on how much information was recovered at retrieval (miss < item-only < pair). Item memory was comparable between age groups while pair memory was reduced in the older adults. Theta synchronization and alpha/beta desynchronization increased linearly with the amount of information available. Single-trial theta power could not predict subsequent item memory, but predicted pair memory in an age-invariant manner, in line with a mechanism supporting associative memory. In contrast, single-trial alpha/beta power predicted both item and pair memory, in line with a mechanism reflecting the depth of information processing, and predicted pair memory less well in the older than the younger adults. Thus, theta and alpha/beta oscillations contribute differently in shaping the contents of memories and reduced processing capacity contributes to episodic memory decline in older age.

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

One important factor contributing to age-related memory decline is the loss of distinctiveness with which information is represented in brain activity. This loss in neural selectivity may be driven by neural attenuation (i.e., reduced activation to target stimuli) or neural broadening (i.e., increased activation to nontarget stimuli). In this fMRI study, we assessed age differences in neural selectivity during first encoding, repeated encoding, and recognition, as well as the underlying pattern (broadening vs. attenuation). We found lower neural selectivity in older compared to younger adults during all memory stages. Crucially, while reduced selectivity in older adults was due to neural broadening during first encoding, it was driven by neural attenuation during recognition, but revealed no clear pattern during repeated encoding. Our findings suggest that intrinsic differences between memory stages may interact with neural activity to manifest as either neural broadening or attenuation. Moreover, despite these differential patterns, neural selectivity was highly correlated across memory stages, indicating that one common mechanism may underly distinct expressions of age-related neural dedifferentiation.

Spectral pattern similarity analysis: Tutorial and application in developmental cognitive neuroscience.

The human brain encodes information in neural activation patterns. While standard approaches to analyzing neural data focus on brain (de-)activation (e.g., regarding the location, timing, or magnitude of neural responses), multivariate neural pattern similarity analyses target the informational content represented by neural activity. In adults, a number of representational properties have been identified that are linked to cognitive performance, in particular the stability, distinctiveness, and specificity of neural patterns. However, although growing cognitive abilities across childhood suggest advancements in representational quality, developmental studies still rarely utilize information-based pattern similarity approaches, especially in electroencephalography (EEG) research. Here, we provide a comprehensive methodological introduction and step-by-step tutorial for pattern similarity analysis of spectral (frequency-resolved) EEG data including a publicly available pipeline and sample dataset with data from children and adults. We discuss computation of single-subject pattern similarities and their statistical comparison at the within-person to the between-group level as well as the illustration and interpretation of the results. This tutorial targets both novice and more experienced EEG researchers and aims to facilitate the usage of spectral pattern similarity analyses, making these methodologies more readily accessible for (developmental) cognitive neuroscientists.

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 EEG recordings during the encoding phase of an item-context association task. Fifty-eight younger (33 females) and 55 older (24 females) 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 that of younger adults. In concert, the present results are consistent with the hypothesis that decrements in the temporal precision with which gamma power is coupled to a specific theta phase underlie the decline of associative memory in normal cognitive aging.SIGNIFICANCE STATEMENT According 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 temporal 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 with younger adults, the coupling phase angle is shifted in time and is more variable in the older adults. We conclude that alterations in the precise timing of theta-gamma coupling contribute to adult age differences in associative memory.

Contributions of representational distinctiveness and stability to memory performance and age differences.

Long-standing theories of cognitive aging suggest that memory decline is associated with age-related differences in the way information is neurally represented. Multivariate pattern similarity analyses enabled researchers to take a representational perspective on brain and cognition, and allowed them to study the properties of neural representations that support successful episodic memory. Two representational properties have been identified as crucial for memory performance, namely the distinctiveness and the stability of neural representations. Here, we review studies that used multivariate analysis tools for different neuroimaging techniques to clarify how these representational properties relate to memory performance across adulthood. While most evidence on age differences in neural representations involved stimulus category information , recent studies demonstrated that particularly item-level stability and specificity of activity patterns are linked to memory success and decline during aging. Overall, multivariate methods offer a versatile tool for our understanding of age differences in the neural representations underlying memory.

Effects of age differences in memory formation on neural mechanisms of consolidation and retrieval.

Episodic memory decline is a hallmark of cognitive aging and a multifaceted phenomenon. We review studies that target age differences across different memory processing stages, i.e., from encoding to retrieval. The available evidence suggests that age differences during memory formation may affect the quality of memory representations in an age-graded manner with downstream consequences for later processing stages. We argue that low memory quality in combination with age-related neural decline of key regions of the episodic memory network puts older adults in a double jeopardy situation that finally results in broader memory impairments in older compared to younger adults.

Tracking Age Differences in Neural Distinctiveness across Representational Levels.

The distinctiveness of neural information representation is crucial for successful memory performance but declines with advancing age. Computational models implicate age-related neural dedifferentiation on the level of item representations, but previous studies mostly focused on age differences of categorical information representation in higher-order visual regions. In an age-comparative fMRI study, we combined univariate analyses and whole-brain searchlight pattern similarity analyses to elucidate age differences in neural distinctiveness at both category and item levels and their relation to memory. Thirty-five younger (18-27 years old) and 32 older (67-75 years old) women and men incidentally encoded images of faces and houses, followed by an old/new recognition memory task. During encoding, age-related neural dedifferentiation was shown as reduced category-selective processing in ventral visual cortex and impoverished item specificity in occipital regions. Importantly, successful subsequent memory performance built on high item stability, that is, high representational similarity between initial and repeated presentation of an item, which was greater in younger than older adults. Overall, we found that differences in representational distinctiveness coexist across representational levels and contribute to interindividual and intraindividual variability in memory success, with item specificity being the strongest contributor. Our results close an important gap in the literature, showing that older adults' neural representation of item-specific information in addition to categorical information is reduced compared with younger adults.SIGNIFICANCE STATEMENT A long-standing hypothesis links age-related cognitive decline to a loss of neural specificity. While previous evidence supports the notion of age-related neural dedifferentiation of category-level information in ventral visual cortex, whether or not age differences exist at the item level was a matter of debate. Here, we observed age group differences at both levels as well as associations between both categorical distinctiveness and item specificity to memory performance, with item specificity being the strongest contributor. Importantly, age differences in occipital item specificity were largely due to reduced item stability across repetitions in older adults. Our results suggest that age differences in neural representations can be observed across the entire cortical hierarchy and are not limited to category-level information.

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.

Hippocampal and Parahippocampal Gray Matter Structural Integrity Assessed by Multimodal Imaging Is Associated with Episodic Memory in Old Age.

Maintained structural integrity of hippocampal and cortical gray matter may explain why some older adults show rather preserved episodic memory. However, viable measurement models for estimating individual differences in gray matter structural integrity are lacking; instead, findings rely on fallible single indicators of integrity. Here, we introduce multitrait-multimethod methodology to capture individual differences in gray matter integrity, based on multimodal structural imaging in a large sample of 1522 healthy adults aged 60-88 years from the Berlin Aging Study II, including 333 participants who underwent magnetic resonance imaging. Structural integrity factors expressed the common variance of voxel-based morphometry, mean diffusivity, and magnetization transfer ratio for each of four regions of interest: 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 to improve our biological understanding of human memory aging.

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.

Noradrenergic Responsiveness Supports Selective Attention across the Adult Lifespan.

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 noninvasive assessments. We studied whether age-related differences in the noradrenergic system predict differences in attention. We measured pupil dilation, a noninvasive marker of arousal-related norepinephrine (NE) release, while concurrently recording the EEG of male younger (N = 39; 25.2 ± 3.2 years) and older adults (N = 38; 70.6 ± 2.7 years). Arousal was modulated on a trial-by-trial basis using fear-conditioned (CS+) stimuli. During conditioning, pupil and EEG markers related to heightened arousal were identified. Afterward, 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 arousal response, as reflected in pupil and EEG α-ß band responses. Critically, pupil dilation to CS+ was correlated with stronger EEG α-ß desynchronization, suggesting a common dependence on NE release. On a behavioral level, stronger arousal reactions were associated with better 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 lifespan.SIGNIFICANCE STATEMENT In 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 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 with 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.

(Only) time can tell: Age differences in false memory are magnified at longer delays.

Older adults often report memories of past events that are partly false. To date, age differences in memory errors have primarily been examined after a delay of minutes to hours. However, in real-life situations we rely on memories formed days to weeks in the past. We examined associative memory for unrelated scene-word pairs in younger and older adults after 24 hr and 8 days. Age differences in memory were magnified after 8 days due to a disproportionate increase in false alarms to rearranged pairs in older adults. In both age groups, the effects of delay were modulated by memory fidelity and whether or not participants had experienced similar events, which potentially caused interference. Older adults were particularly vulnerable to associative memory errors having experienced similar events, even when the initial memory was of high fidelity. We suggest that the fidelity of memory representations in concert with monitoring processes to resolve interference determine how the passage of time affects the propensity to falsely remember details of the past. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

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

We studied oscillatory mechanisms of memory formation in 48 younger and 51 older adults in an intentional associative memory task with cued recall. While older adults showed lower memory performance than young adults, we found subsequent memory effects (SME) in alpha/beta and theta frequency bands in both age groups. Using logistic mixed effects models, we investigated whether interindividual differences in structural integrity of key memory regions could account for interindividual differences in the strength of the SME. Structural integrity of inferior frontal gyrus (IFG) and hippocampus was reduced in older adults. SME in the alpha/beta band were modulated by the cortical thickness of 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 contribute not only to interindividual, but also to age differences in memory formation.

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. This enables 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 as to whether and under which circumstances memory consolidation is impacted during aging. To approach this question, 30 younger adults (19-28 years) and 36 older adults (63-74 years) completed a memory task based on scene-word associations. By tracing the encoding quality of participants' individual memory associations, 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 intermediate encoding quality, whereas memory gain of poorly encoded memories did not differ by age. Ambulatory polysomnography (PSG) and structural magnetic resonance imaging (MRI) data were acquired to extract potential predictors of memory consolidation from each participant's NREM sleep physiology and brain structure. Partial Least Squares Correlation was used to identify profiles of interdependent alterations in sleep physiology and brain structure that are characteristic for increasing age. Across age groups, both the 'aged' sleep profile, defined by decreased slow-wave activity (0.5-4.5 â€‹Hz), and a reduced presence of slow oscillations (0.5-1 â€‹Hz), slow, and fast spindles (9-12.5 â€‹Hz; 12.5-16 â€‹Hz), as well as the 'aged' brain structure profile, characterized by gray matter reductions in the medial prefrontal cortex, thalamus, entorhinal cortex, and hippocampus, were associated with reduced memory maintenance. However, inter-individual differences in neither sleep nor structural brain integrity alone qualified as the driving force behind age differences in sleep-dependent consolidation in the present study. Our results underscore the need for novel and age-fair analytic tools to provide a mechanistic understanding of age differences in memory consolidation.