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Koen, J. D.

Publications and source records attributed to Koen, J. D..

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Dissociative effects of age on neural differentiation at the category and item level

Increasing age is associated with age-related neural dedifferentiation, a reduction in the selectivity of neural representations which has been proposed to contribute to cognitive decline in older age. Recent findings indicate that when operationalized in terms of selectivity for different perceptual categories, age-related neural dedifferentiation, and the apparent age-invariant association of neural selectivity with cognitive performance, are largely restricted to the cortical regions typically recruited during scene processing. It is currently unknown whether this category-level dissociation extends to metrics of neural selectivity defined at the level of individual stimulus items. Here, we examined neural selectivity at the category and item levels using multivoxel pattern similarity analysis (PSA) of fMRI data. Healthy young and older male and female adults viewed images of objects and scenes. Some items were presented singly, while others were either repeated or followed by a similar lure. Consistent with recent findings, category-level PSA revealed robustly lower differentiation in older than younger adults in scene-selective, but not object-selective, cortical regions. By contrast, at the item level, robust age-related declines in neural differentiation were evident for both stimulus categories. Moreover, we identified an age-invariant association between category-level scene-selectivity in the parahippocampal place area and subsequent memory performance, but no such association was evident for item-level metrics. Lastly, category and item-level neural metrics were uncorrelated. Thus, the present findings suggest that age-related category- and item-level dedifferentiation depend on distinct neural mechanisms. Significance StatementCognitive aging is associated with a decline in the selectivity of the neural responses within cortical regions that respond differentially to distinct perceptual categories (age-related neural dedifferentiation). However, prior research indicates that while scene-related selectivity is reduced in older age and is correlated with cognitive performance independently of age, selectivity for object stimuli is typically not moderated by age or memory performance. Here, we demonstrate that neural dedifferentiation is evident for both scene and object exemplars when it is defined in terms of the specificity of neural representations at the level of individual exemplars. These findings suggest that neural selectivity metrics for stimulus categories and for individual stimulus items depend on different neural mechanisms.

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Neural noise is associated with age-related neural dedifferentiation

Age-related neural dedifferentiation - reductions in the selectivity and precision of neural representations - contributes to cognitive aging and is thought to result from age increases in neural noise. This research has primarily used fMRI to examine age-related reductions in neural selectivity for different categories of visual stimuli. The present experiment used EEG to examine the link between neural noise and age-related neural dedifferentiation indexed by the scene-selective (P200) and face-selective (N170) ERP components. Young and older adults viewed images of scenes, objects, and faces during a 1-back task. Whereas both the P200 and N170 showed age-related slowing of peak latency, only the P200 showed age-related reductions in amplitude that were independent of visual and contrast acuity. We also examined the relationship between the ERP peak measures and an index of neural noise, namely the 1/f exponent of the frequency power spectrum. For the P200 amplitude, higher levels of neural noise were associated with smaller P200 amplitudes in young, but not older adults. In contrast, there was an age-invariant relationship between neural noise and N170 amplitude in the left hemisphere with higher levels of neural noise being associated reduced N170 amplitudes. While the present findings provide novel empirical evidence broadly consistent with predictions from computational models of neural dedifferentiation, the results also highlight potential limitations of the computational model that necessitate revision. The results also suggest that, at least for the P200, maintaining levels of neural noise similar to young adults might preserve levels of neural selectivity. Significance StatementA prominent theory of cognitive aging proposes that age-related cognitive decline results from increases in neural noise that reduce the selectivity of neural representations. We examined this predicted link between neural selectivity and neural noise with ERP components that show selectivity for scenes (P200) and faces (N170) and the 1/f aperiodic exponent measure of neural noise. The amplitude for the scene-selective, but not face-selective, ERP component was reduced in older adults, with both components showing age-related slowing. Critically, older adults with higher levels of neural noise showed lower levels of neural selectivity for scenes, but not faces. While these results provide some evidence supporting computational models of neural dedifferentiation, they also highlight important limitations of the model that require revision.

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Age-related neural dedifferentiation for individual stimuli: An across-participant pattern similarity analysis

Age-related neural dedifferentiation - reductions in the regional specificity and precision of neural representations - is proposed to compromise the ability of older adults to form sufficiently distinct neural representations to support episodic memory encoding. The computational model that spurred investigations of age-related neural dedifferentiation initially characterized this phenomenon as a reduction in the specificity of neural patterns for individual items or stimuli. Most investigations have focused on reductions in neural differentiation for patterns of neural activity associated with category level information, such as reduced neural selectivity between categories of visual stimuli (e.g., scenes, objects, and faces). Here, I report a novel across-participant pattern similarity analysis method to measure neural distinctiveness for individual stimuli that were presented to participants on a single occasion. Measures of item level pattern similarity during encoding showed a graded positive subsequent memory effect in younger, with no significant subsequent memory effect in older adults. These results suggest that age-related reductions in the distinctiveness of neural patterns for individual stimuli during age differences in memory encoding. Moreover, a measure of category level similarity demonstrated a significant subsequent memory effect associated with item recognition (regardless of an object source memory detail), whereas the effect in older was associated with source memory. These results converge with predictions of computational models of dedifferentiation showing age-related reductions in the distinctiveness of neural patterns across multiple levels of representation.

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The hippocampus shows an own-age bias during unfamiliar face viewing

The present study investigated the neural correlates of the own-age bias for face recognition in a repetition suppression paradigm. Healthy young and older adults viewed upright and inverted unfamiliar faces. Some of the upright faces were repeated following one of two delays (lag 0 or lag 11). Repetition suppression effects were observed in bilateral fusiform cortex. However, there were no significant effects indicating an own-age bias in repetition suppression. The absence of these effects is arguably inconsistent with perceptual expertise accounts of own-age biases in face processing. By contrast, the right anterior hippocampus showed an own-age bias (greater activity for own-than other-age faces) when viewing an unfamiliar face for the first time. Given the importance of the hippocampus for episodic memory encoding, we conjecture that the increased hippocampal activity for own-age relative to other-age faces reflects differential engagement of neural processes supporting the episodic encoding of faces and might provide insight into the neural underpinnings of own-age biases in face recognition memory.

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Transcranial magnetic stimulation of right dorsolateral prefrontal cortex does not affect associative retrieval in healthy young or older adults

We examined whether post-retrieval monitoring processes supporting memory performance are more resource limited in older adults relative to younger individuals. We predicted that older adults would be more susceptible to an experimental manipulation that reduced the neurocognitive resources available to support post-retrieval monitoring. Young and older adults received transcranial magnetic stimulation (TMS) to the right dorsolateral prefrontal cortex (DLPFC) or a vertex control site during an associative recognition task. The right DLPFC was selected as a TMS target because the region is held to be a key member of a network of regions engaged during retrieval monitoring and is readily accessible to administration of TMS. We predicted that TMS to the right DLPFC would lead to reduced associative recognition accuracy, and that this effect would be more prominent in older adults. The results did not support this prediction. Recognition accuracy was significantly reduced in older adults relative to their younger counterparts but the magnitude of this age difference was unaffected following TMS to the right DLPFC or vertex. These findings suggest that TMS to the right DLPFC was insufficient to deplete the neurocognitive resources necessary to support post-retrieval monitoring.

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Medial prefrontal cortex has a causal role in selectively enhanced consolidation of emotional memories after a 24-hour delay: An iTBS study

Previous research points to an association between retrieval-related activity in the medial prefrontal cortex (mPFC) and preservation of emotional information compared to co-occurring neutral information following sleep. Although the role of the mPFC in emotional memory likely begins at encoding, little research has examined how mPFC activity during encoding interacts with consolidation processes to enhance emotional memory. This issue was addressed in the present study using transcranial magnetic stimulation in conjunction with an emotional memory paradigm. Healthy young adults encoded negative and neutral scenes while undergoing concurrent TMS with a modified short intermittent theta burst stimulation (sTBS) protocol. Participants received stimulation to either the mPFC or an active control site (motor cortex) during the encoding phase. Recognition memory for scene components (objects and backgrounds) was assessed after a short (30-minute) and a long delay (24-hour, including a night of sleep) to obtain measures of specific and gist-based memory processes. The results demonstrated that, relative to control stimulation, sTBS to the mPFC enhanced memory for negative objects on the long delay test (collapsed across specific and gist-based memory measures). mPFC stimulation had no discernable effect on memory for objects on the short delay test nor on the background images at either test. These results suggest that mPFC activity occurring during encoding interacts with consolidation processes to preferentially preserve negatively salient information. Significance StatementUnderstanding how emotional information is remembered over time is critical to understanding memory in the real world. The present study used noninvasive brain stimulation (repetitive transcranial magnetic stimulation, rTMS) to investigate the interplay between mPFC activity that occurs during memory encoding and its subsequent interactions with consolidation processes. rTMS delivered to the mPFC during encoding enhanced memory for negatively valenced pictures on a test following a 24-hr delay, with no such effect on a test occurring shortly after the encoding phase. These results are consistent with the hypothesis that emotional aspects of memories are differentially subjected to consolidation processes, and that the mPFC might contribute to this "tag-and-capture" mechanism during the initial formation of such memories.

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Neural differentiation is moderated by age in scene- but not face-selective cortical regions

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 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.

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The relationship between age, neural differentiation, and memory performance

Healthy aging is associated with decreased neural selectivity (dedifferentiation) in category-selective cortical regions. This finding has prompted the suggestion that dedifferentiation contributes to age-related cognitive decline. Consistent with this possibility, dedifferentiation has been reported to negatively correlate with fluid intelligence in older adults. Here, we examined whether dedifferentiation is associated with performance in another cognitive domain - episodic memory - that is also highly vulnerable to aging. Given the proposed role of differentiation in age-related cognitive decline, we predicted there would be a stronger link between dedifferentiation and episodic memory performance in older than in younger adults. Young (18-30 yrs) and older (64-75 yrs) male and female humans underwent fMRI scanning while viewing images of objects and scenes prior to a subsequent recognition memory test. We computed a differentiation index in two regions-of-interest (ROIs): parahippocampal place area (PPA) and lateral occipital complex (LOC). This index quantified the selectivity of the BOLD response to an ROIs preferred versus non-preferred category (scenes for PPA, objects for LOC). The differentiation index in the PPA, but not the LOC, was lower in older than in younger adults. Additionally, the PPA differentiation index predicted recognition memory performance for the studied items. This relationship was independent of and not moderated by age. The PPA differentiation index also predicted performance on a latent fluency factor derived from a neuropsychological test battery; this relationship was also age invariant. These findings suggest that two independent factors, one associated with age, and the other with cognitive performance, drive neural differentiation.\n\nSignificance StatementAging is associated with neural dedifferentiation - reduced neural selectivity in category selective cortical brain regions - which has been proposed to mediate cognitive aging. Here, we examined whether neural differentiation is predictive of episodic memory performance, and whether the relationship is moderated by age. A neural differentiation index was estimated for scene-(PPA) and object-(LOC) selective cortical regions while participants studied images for a subsequent memory test. Age related reductions were observed for the PPA, but not the LOC, differentiation index. Importantly, the PPA differentiation index demonstrated age invariant correlations with subsequent memory performance and a fluency factor derived from a neuropsychological battery. Together, these findings suggest that neural differentiation is associated with two independent factors: age and cognitive performance.

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Age-related differences in prestimulus subsequent memory effects assessed with event-related potentials

Prestimulus subsequent memory effects (preSMEs) - differences in neural activity elicited by a task cue at encoding that are predictive of later memory performance - are thought to reflect differential engagement of preparatory processes that benefit episodic memory encoding. We investigated age differences in preSMEs indexed by differences in ERP amplitude just prior to the onset of a study item. Young and older adults incidentally encoded words for a subsequent memory test. Each study word was preceded by a task cue that signaled the judgment to perform on the word. Words were presented for either a short (300 ms) or a long (1000 ms) duration with the aim of placing differential benefits on engaging preparatory processes initiated by the task cue. ERPs associated with subsequent successful and unsuccessful recollection, operationalized here by source memory accuracy, were estimated time-locked to the onset of the task cue. In a late time-window (1000-2000 ms following onset of the cue), young adults demonstrated frontally distributed preSMEs for both the short and the long study durations, albeit with opposite polarities in the two conditions. This finding suggests that preSMEs in young adults are sensitive to perceived task demands. Although older adults showed no evidence of preSMEs in the same late time window, significant preSMEs were observed in an earlier time window (500-1000 ms) that were invariant with study duration. These results are broadly consistent with the proposal that older adults differ from their younger counterparts in how they engage preparatory processes during memory encoding.

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