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Rugg, M. D.

Publications and source records attributed to Rugg, M. D..

23 records · Page 2Linked to original sources

Age differences in retrieval-related reinstatement reflect age-related dedifferentiation at encoding

Age-related reductions in neural specificity have been linked to cognitive decline. We examined whether age differences in specificity of retrieval-related cortical reinstatement could be explained by analogous differences at encoding, and whether reinstatement was associated with memory performance in an age-dependent or age-independent manner. Young and older adults underwent fMRI as they encoded words paired with images of faces or scenes. During a subsequent scanned memory test participants judged whether test words were studied or unstudied and, for words judged studied, also made a source memory judgment about the associated image category. Using multi-voxel pattern analyses, we identified a robust age-related decline in scene reinstatement. This decline was fully explained by age differences in neural differentiation at encoding. These results suggest that, regardless of age, the specificity with which events are neurally processed at the time of encoding determines the fidelity of cortical reinstatement at retrieval.

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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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Stimulation of the posterior cingulate impairs episodic memory encoding

Neuroimaging experiments implicate the posterior cingulate cortex (PCC) in episodic memory processing, making it a potential target for responsive neuromodulation strategies outside of the hippocampal network. However, causal evidence for the role PCC plays in memory encoding is lacking. In patients undergoing seizure mapping, we investigated functional properties of the PCC using deep brain stimulation (DBS) and stereotactic electroencephalography (stereo EEG). These techniques allow precise targeting of deep cortical structures including the PCC, and simultaneous acquisition of oscillatory recordings from neighboring regions such as the hippocampus. We used a free recall experiment in which PCC was stimulated during item encoding period of half of the study lists, while no stimulation was applied during encoding period of the remaining lists. We evaluated if stimulation affected memory and/or modulated hippocampal activity. Results revealed four main findings. (i) Stimulation during encoding impaired memory for early items on the study lists. (ii) Stimulation increased hippocampal gamma band power. (iii) Stimulation-induced gamma power predicted memory impairment. (iv) Functional connectivity between the hippocampus and PCC predicted the degree of stimulation effect on memory. Our findings offer the first causal evidence implicating the PCC in episodic memory encoding. Importantly, results highlight that stimulation targeted outside of the temporal lobe can modulate hippocampal activity with implications on behavior. Furthermore, a-priori measures of connectivity between brain regions within a functional network can be informative in predicting behavioral effects of stimulation. Our findings have significant implications for developing therapie to treat diseases of memory loss and cognitive impairment using DBS.\n\nSignificance StatementCognitive impairment and memory loss are critical public health challenges. Deep brain stimulation (DBS) is a promising tool for developing strategies to ameliorate memory disorders by targeting brain regions involved in mnemonic processing. Using DBS, our study sheds light on the lesser-known role of the posterior cingulate cortex (PCC) in memory encoding. Stimulating the PCC during encoding impairs subsequent recall memory. The degree of impairment is predictedby stimulation-induced hippocampal gamma oscillations and functional connectivity between PCC and hippocampus. Our findings provide the first causal evidence implicating PCC in memory encoding and highlight the PCC as a favorable target for neuromodulation strategies, using a-priori connectivity measures to predict stimulation effects. This has significant implications for developing therapies for memory diseases.

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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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