No abstract

The aging brain is characterized by neural dedifferentiation, an apparent decrease in the functional selectivity of category-selective cortical regions. Age-related reductions in neural differentiation have been proposed to play a causal role in cognitive aging. Recent findings suggest, however, that age-related dedifferentiation is not equally evident for all stimulus categories and, additionally, that the relationship between neural differentiation and cognitive performance is not moderated by age. In light of these findings, in the present experiment, younger and older human adults (males and females) underwent fMRI as they studied words paired with images of scenes or faces before a subsequent memory task. Neural selectivity was measured in two scene-selective (parahippocampal place area (PPA) and retrosplenial cortex (RSC)] and two face-selective [fusiform face area (FFA) and occipital face area (OFA)] regions using both a univariate differentiation index and multivoxel pattern similarity analysis. Both methods provided highly convergent results, which revealed evidence of age-related reductions in neural dedifferentiation in scene-selective but not face-selective cortical regions. Additionally, neural differentiation in the PPA demonstrated a positive, age-invariant relationship with subsequent source memory performance (recall of the image category paired with each recognized test word). These findings extend prior findings suggesting that age-related neural dedifferentiation is not a ubiquitous phenomenon, and that the specificity of neural responses to scenes is predictive of subsequent memory performance independently of age.

This review focuses on possible contributions of neural dedifferentiation to age-related cognitive decline. Neural dedifferentiation is held to reflect a breakdown in the functional specificity of brain regions and networks that compromises the fidelity of neural representations supporting episodic memory and related cognitive functions. The evidence for age-related dedifferentiation is robust when it is operationalized as neural selectivity for different categories of perceptual stimuli or as decreased segregation or modularity of resting-state functional brain networks. Neural dedifferentiation for perceptual categories appears to demonstrate a negative, age-invariant relationship with performance on tests of memory and fluid processing. Whether this pattern extends to network-level measures of dedifferentiation cannot currently be determined due to insufficient evidence. The existing data highlight the importance of further examination of neural dedifferentiation as a factor contributing to episodic memory and to cognitive performance more generally.

AbstractThe aging brain is characterized by neural dedifferentiation – an apparent decrease in the functional selectivity of category-selective cortical regions. Age-related reductions in neural differentiation have been proposed to play a causal role in cognitive aging. Recent findings suggest, however, that age-related dedifferentiation is not equally evident for all stimulus categories and, additionally, that the relationship between neural differentiation and cognitive performance is not moderated by age. In light of these findings, in the present experiment younger and older human adults (males and females) underwent fMRI as they studied words paired with images of scenes or faces prior to a subsequent memory task. Neural selectivity was measured in two scene-selective (parahippocampal place area and retrosplenial cortex) and two face-selective (fusiform and occipital face areas) regions of interest using both a univariate differentiation index and multivoxel pattern similarity analysis. Both methods provided highly convergent results which revealed evidence of age-related reductions in neural dedifferentiation in scene-selective but not face-selective cortical regions. Additionally, neural differentiation in the parahippocampal place area demonstrated a positive, age-invariant relationship with subsequent source memory performance (recall of the image category paired with each recognized test word). These findings extend prior findings suggesting that age-related neural dedifferentiation is not a ubiquitous phenomenon, and that the specificity of neural responses to scenes is predictive subsequent memory performance independently of age.Significance StatementIncreasing age is associated with reduced neural specificity in cortical regions that are selectively responsive to a given perceptual stimulus category (age-related neural dedifferentiation), a phenomenon which has been proposed to contribute to cognitive aging. Recent findings reveal that age-related neural dedifferentiation is not present for all types of visual stimulus categories, and the factors which determine when the phenomenon arises remain unclear. Here, we demonstrate that scene- but not face-selective cortical regions exhibit age-related neural dedifferentiation during an attentionally-demanding task. Additionally, we report that higher neural selectivity in the scene-selective ‘parahippocampal place area’ is associated with better memory performance after controlling for variance associated with age group, adding to evidence that neural differentiation impacts cognition across the adult lifespan.

Recent research suggests that episodic memory is associated with systematic differences in the localization of neural activity observed during memory encoding and retrieval. The retrieval-related anterior shift is a phenomenon whereby the retrieval of a stimulus event (e.g., a scene image) is associated with a peak neural response which is localized more anteriorly than the response elicited when the stimulus is experienced directly. Here, we examine whether the magnitude of the anterior shift, i.e., the distance between encoding-and retrieval-related response peaks, is moderated by age, and also whether the shift is associated with memory performance. Younger and older human subjects of both sexes underwent fMRI as they completed encoding and retrieval tasks on word-face and word-scene pairs. We localized peak scene-and face-selectivity for each individual participant within the face-selective precuneus (PCU) and in three scene-selective (parahippocampal place area [PPA], medial place area [MPA], occipital place area [OPA]) regions of interest (ROIs). In line with recent findings, we identified an anterior shift in PPA and OPA in both age groups and, in older adults only, in MPA and PCU also. Of importance, the magnitude of the anterior shift was larger in older than in younger adults. The shift within the PPA exhibited an age-invariant across-participant negative correlation with source memory performance, such that a smaller displacement between encoding-and retrieval-related neural activity was associated with better performance. These findings provide novel insights into the functional significance of the anterior shift, especially in relation to memory decline in older age.

Retrieval gating refers to the ability to modulate the retrieval of features of a single memory episode according to behavioral goals. Recent findings demonstrate that younger adults engage retrieval gating by attenuating the representation of task-irrelevant features of an episode. Here, we examine whether retrieval gating varies with age. Younger and older adults incidentally encoded words superimposed over scenes or scrambled backgrounds that were displayed in one of three spatial locations. Participants subsequently underwent fMRI as they completed two memory tasks: the background task, which tested memory for the word's background, and the location task, testing memory for the word's location. Employing univariate and multivariate approaches, we demonstrated that younger, but not older adults, exhibited attenuated reinstatement of scene information when it was goal-irrelevant (during the location task). Additionally, in younger adults only, the strength of scene reinstatement in the parahippocampal place area during the background task was related to item and source memory performance. Together, these findings point to an agerelated decline in the ability to engage retrieval gating.

Recent research suggests that episodic memory is associated with systematic differences in the localization of neural activity observed during memory encoding and retrieval. The retrieval-related anterior shift is a phenomenon whereby the retrieval of a stimulus event (e.g., a scene image) is associated with a peak neural response which is localized more anteriorly than the response elicited when the stimulus is experienced directly. Here, we examine whether the magnitude of the anterior shift, i.e., the distance between encoding- and retrieval-related response peaks, is moderated by age, and also whether the shift is associated with memory performance. Younger and older human subjects of both sexes underwent fMRI as they completed encoding and retrieval tasks on word-face and word-scene pairs. We localized peak scene- and face-selectivity for each individual participant within the face-selective precuneus (PCU) and in three scene-selective (parahippocampal place area [PPA], medial place area [MPA], occipital place area [OPA]) regions of interest (ROIs). In line with recent findings, we identified an anterior shift in PPA and OPA in both age groups and, in older adults only, in MPA and PCU also. Of importance, the magnitude of the anterior shift was larger in older than in younger adults. The shift within the PPA exhibited an age-invariant across-participant negative correlation with source memory performance, such that a smaller displacement between encoding- and retrieval-related neural activity was associated with better performance. These findings provide novel insights into the functional significance of the anterior shift, especially in relation to memory decline in older age.

Objectives It is well known that age differentially impacts aspects of long-term episodic memory (EM): Whereas a binding deficit indicates that older adults are less capable than younger adults to encode or retrieve associations between information (e.g., the pairing between two memoranda, such as lock – race), item memory is relatively intact (e.g., recognizing lock without its original pairing). Method We tested whether this deficit could be corrected by facilitating establishment of the bindings in working memory (WM) through adapting the semantic relatedness of studied pairs according to participants’ ongoing performance (Experiments 1 and 2). We also examined whether this was evident for the long-term retention of pairs that were not tested in WM (Experiment 2). Results The results revealed matched binding and item memory in WM and EM between age groups. Most importantly, older adults required increased semantic strength between word pairs to achieve similar performance to that of younger adults, regardless of whether pairs were immediately tested during the WM task. Discussion These findings indicate that relying on their superior semantic memory can correct the commonly exhibited profound deficit in binding memory in older age.