Functional disruption of the medial temporal lobe-dependent networks is thought to underlie episodic memory deficits in aging and Alzheimer's disease. Previous studies revealed that the anterior medial temporal lobe is more vulnerable to pathological and neurodegenerative processes in Alzheimer's disease. In contrast, cognitive and structural imaging literature indicates posterior, as opposed to anterior, medial temporal lobe vulnerability in normal aging. However, the extent to which Alzheimer's and aging-related pathological processes relate to functional disruption of the medial temporal lobe-dependent brain networks is poorly understood. To address this knowledge gap, we examined functional connectivity alterations in the medial temporal lobe and its immediate functional neighborhood - the Anterior-Temporal and Posterior-Medial brain networks - in normal agers, individuals with preclinical Alzheimer's disease, and patients with Mild Cognitive Impairment or mild dementia due to Alzheimer's disease. In the Anterior-Temporal network and in the perirhinal cortex, in particular, we observed an inverted 'U-shaped' relationship between functional connectivity and Alzheimer's stage. According to our results, the preclinical phase of Alzheimer's disease is characterized by increased functional connectivity between the perirhinal cortex and other regions of the medial temporal lobe, as well as between the anterior medial temporal lobe and its one-hop neighbors in the Anterior-Temporal system. This effect is no longer present in symptomatic Alzheimer's disease. Instead, patients with symptomatic Alzheimer's disease displayed reduced hippocampal connectivity within the medial temporal lobe as well as hypoconnectivity within the Posterior-Medial system. For normal aging, our results led to three main conclusions: (1) intra-network connectivity of both the Anterior-Temporal and Posterior-Medial networks declines with age; (2) the anterior and posterior segments of the medial temporal lobe become increasingly decoupled from each other with advancing age; and, (3) the posterior subregions of the medial temporal lobe, especially the parahippocampal cortex, are more vulnerable to age-associated loss of function than their anterior counterparts. Together, the current results highlight evolving medial temporal lobe dysfunction in Alzheimer's disease and indicate different neurobiological mechanisms of the medial temporal lobe network disruption in aging vs. Alzheimer's disease.
Abstract INTRODUCTION The generalizability of neuroimaging and cognitive biomarkers in their sensitivity to detect preclinical Alzheimer's disease (AD) and power to predict progression in large, multisite cohorts remains unclear. METHOD Longitudinal demographics, T1‐weighted magnetic resonance imaging (MRI), and cognitive scores of 3036 cognitively unimpaired (CU) older adults (amyloid beta [Aβ]‐negative/positive [A–/A+]: 1270/1558) were included. Cross‐sectional and longitudinal cognition and medial temporal lobe (MTL) structural measures were extracted. Cross‐sectional MTL tau burden (T) was computed from tau positron emission tomography ( N = 1095). RESULTS We found cross‐sectional tau and longitudinal structural biomarkers best separated A+ CU from A– CU. A–T+ CU had significantly faster neurodegeneration rate compared to A–T– CU. MTL tau was significantly correlated with MRI and cognitive biomarkers regardless of Aβ status. MTL tau, MRI, and cognition provided complementary information about disease progression. DISCUSSION This large multisite study replicates prior findings in CU older adults, supporting the utility of neuroimaging and cognitive biomarkers in preclinical AD clinical trials and normal aging studies. Highlights We investigated neuroimaging and cognitive biomarkers in 3036 cognitively unimpaired (CU) participants. Medial temporal lobe (MTL) tau and longitudinal MTL atrophy best separate amyloid beta positive (A+) CU from amyloid beta negative (A–) CU. A– tau positive (T+) CU had a significantly faster neurodegeneration rate compared to A–T– CU. MTL tau correlated with structural magnetic resonance imaging (MRI) and cognition regardless of amyloid beta status. Combined baseline MTL tau, MRI, and cognition best predict Alzheimer's disease progression.
Objective: Olfactory function declines during normal aging; however, accelerated olfactory decline is observed in neurodegenerative diseases, such as Alzheimer’s disease (AD). Moreover, olfactory deficits in pre-clinical AD are associated with future cognitive decline. Odor identification and memory deficits have been consistently reported in early stage AD indicating its potential sensitivity to AD pathophysiology in olfactory and limbic structures, yet few studies of olfaction have incorporated structural measures in a well-characterized cohort of older adults. In the current study we examined the association between odor identification impairment, cognition, and medial temporal lobe (MTL) sub-regions in cognitively unimpaired and impaired older adults. Participants and Methods: We enrolled 140 participants (age=72.25±6.54, 56% female, years of education=16.30±2.63, 82% Caucasian, 15% Black/AA, 3% Multiracial) from the Penn Alzheimer’s Disease Research Center Clinical Cohort. Participants completed the Sniffin’ Sticks Odor Identification Test (SS-OIT), cognitive testing (NACC UDS2 or UDS3 and additional cognitive tests), and MRI scans (3T Siemens MAGNETOM Prisma MRI scanner). For the SS-OIT, participants were presented with 16 odorants using felt-tipped pen dispensers and asked to identify each odor from four multiple-choice options. Scores range from 0 to 16. Additionally, cognitive domains were created by averaging z-scores from tests within each domain: attention, memory, language, executive function, and visuospatial. This cohort was divided into participants with unimpaired cognition (n=96) and impaired cognition (MCI, dementia; n=44) using established normative data and consensus diagnosis. Linear regressions were performed to examine the association between SS-OIT score, each cognitive domain, and MTL measurements for unimpaired and impaired groups. For all analyses, we controlled for age, race, sex, education, smoking status, and hypertension and additionally for MOCA score and intracranial volume with MTL measurements. Results: In the unimpaired group, SS-OIT significantly associated with language (p<.05). In the impaired group, SS-OIT significantly associated with language and memory (p<.05). In the unimpaired group, SS-OIT significantly associated with right anterior hippocampal volume (p<.05). In the impaired group, significant associations were found between SS-OIT and right anterior hippocampal volume (p<.05) and left hippocampal mean thickness (p<.05). Additionally, SS-OIT significantly associated with left and right entorhinal cortex volume (p<.05) and mean thickness (p<.05). Conclusions: This study reveals that lower odor identification performance is related to lower performance on measures of cognition and atrophy in MTL sub-regions in unimpaired and impaired older adults. Our findings support prior results demonstrating relationships between olfactory function, cognition, and MTL sub-regions. Specifically, olfactory function and episodic memory have been shown to follow similar patterns of decline in the course of AD, potentially reflecting AD pathology in shared regions of the MTL subserving episodic memory and olfactory function. Our findings demonstrate that reductions in both cortical thickness and grey matter volume of MTL regions are linked to olfactory deficits in individuals at risk for Alzheimer’s dementia. Future steps will include the analysis of longitudinal cognitive and imaging indices and the incorporation of fluid biomarker data.
Abstract Functional disruption of the medial temporal lobe-dependent networks is thought to underlie episodic memory deficits in aging and Alzheimer’s disease. Previous studies revealed that the anterior medial temporal lobe is more vulnerable to pathological and neurodegenerative processes in Alzheimer’s disease. In contrast, cognitive and structural imaging literature indicates posterior, as opposed to anterior, medial temporal lobe vulnerability in normal aging. However, the extent to which Alzheimer’s and aging-related pathological processes relate to functional disruption of the medial temporal lobe-dependent brain networks is poorly understood. To address this knowledge gap, we examined functional connectivity alterations in the medial temporal lobe and its immediate functional neighbourhood—the Anterior-Temporal and Posterior-Medial brain networks—in normal agers, individuals with preclinical Alzheimer’s disease and patients with Mild Cognitive Impairment or mild dementia due to Alzheimer’s disease. In the Anterior-Temporal network and in the perirhinal cortex, in particular, we observed an inverted ‘U-shaped’ relationship between functional connectivity and Alzheimer’s stage. According to our results, the preclinical phase of Alzheimer’s disease is characterized by increased functional connectivity between the perirhinal cortex and other regions of the medial temporal lobe, as well as between the anterior medial temporal lobe and its one-hop neighbours in the Anterior-Temporal system. This effect is no longer present in symptomatic Alzheimer’s disease. Instead, patients with symptomatic Alzheimer’s disease displayed reduced hippocampal connectivity within the medial temporal lobe as well as hypoconnectivity within the Posterior-Medial system. For normal aging, our results led to three main conclusions: (i) intra-network connectivity of both the Anterior-Temporal and Posterior-Medial networks declines with age; (ii) the anterior and posterior segments of the medial temporal lobe become increasingly decoupled from each other with advancing age; and (iii) the posterior subregions of the medial temporal lobe, especially the parahippocampal cortex, are more vulnerable to age-associated loss of function than their anterior counterparts. Together, the current results highlight evolving medial temporal lobe dysfunction in Alzheimer’s disease and indicate different neurobiological mechanisms of the medial temporal lobe network disruption in aging versus Alzheimer’s disease.
Abstract Background Previous work suggests functional abnormalities in the human brain in preclinical Alzheimer’s disease. However, little has been explored about the relationship between BOLD fMRI signal amplitude/energy over time and AD pathology. In this work we analyzed the effects of AD progression on amplitude of low‐frequency fluctuations (ALFF) during resting‐state fMRI scans both at the whole‐brain level and at a more granular level, focused on regions of the medial temporal lobe (MTL) that are most vulnerable to AD pathology. Method In this cross‐sectional study, we analyzed data from 224 individuals from the Penn ADRC cohort (Table 1). All participants underwent structural and functional MRI on a Siemens 3T Prisma system, and 18F‐Florbetaben or 18F‐Florbetapir amyloid‐PET imaging. 125 participants also underwent 18F‐Flortaucipir tau‐PET scans. Functional images were preprocessed using a custom implementation of fMRIprep and ALFF was extracted using Conn software. In the whole‐brain analyses we performed voxelwise GLMs with age and sex as covariates. Results We observed reduced ALFF in both preclinical AD (Amyloid‐positive (Aß+) cognitively unimpaired, CU) and Aß+ cognitively impaired (CI) individuals. Relative to Aß‐ controls, individuals with preclinical AD displayed lower ALFF in frontal, parietal and temporal association cortices (Fig 1, top left). CI individuals displayed lower ALFF in most of the brain, except in inferior temporal cortex, temporal pole, and MTL. The effect of AD progression on ALFF was characterized by a progressive reduction primarily in frontal and parietal regions that roughly align with the anatomy of the default mode network. In contrast, transentorhinal tau pathology was negatively associated with ALFF in frontal and anterior temporal lobes, as well as insula and MTL (Figure 1 bottom right). Negative association between tau burden and MTL ALFF was observed in all main MTL subregions, and strongest in the transetorhinal cortex (Figure 2). Conclusion We conclude that: (1) ALFF might be a promising biomarker for studying functional abnormalities in preclinical AD, and (2) based on the spatial topography of amyloid and tau effects on ALFF (Figure 1 bottom), there is likely a differential effect of of the two on ALFF that needs to be further explored.
Abstract INTRODUCTION Variability in relationship of tau‐based neurofibrillary tangles (T) and neurodegeneration (N) in Alzheimer's disease (AD) arises from non‐specific nature of N, modulated by non‐AD co‐pathologies, age‐related changes, and resilience factors. METHODS We used regional T‐N residual patterns to partition 184 patients within the Alzheimer's continuum into data‐driven groups. These were compared with groups from 159 non‐AD (amyloid “negative”) patients partitioned using cortical thickness, and groups in 98 patients with ante mortem MRI and post mortem tissue for measuring N and T, respectively. We applied the initial T‐N residual model to classify 71 patients in an independent cohort into predefined groups. RESULTS AD groups displayed spatial T‐N mismatch patterns resembling neurodegeneration patterns in non‐AD groups, similarly associated with non‐AD factors and diverging cognitive outcomes. In the autopsy cohort, limbic T‐N mismatch correlated with TDP‐43 co‐pathology. DISCUSSION T‐N mismatch may provide a personalized approach for determining non‐AD factors associated with resilience/vulnerability in AD.
Abstract Background The extent to which pathological processes in aging and Alzheimer’s disease (AD) relate to functional disruption of the medial temporal lobe (MTL)‐dependent brain networks is poorly understood. To address this knowledge gap, we examined functional connectivity (FC) alterations between anterior and posterior regions of the MTL and in MTL‐associated functional communities – the Anterior‐Temporal (AT) and Posterior‐Medial (PM) networks – in normal agers, individuals with preclinical AD, and patients with Mild Cognitive Impairment or mild dementia due to AD. Method In this cross‐sectional study, we analyzed data from 179 individuals from the Aging Brain Cohort study of the Penn ADRC. Detailed information about participants is provided in Table 1. For intra‐MTL FC comparisons, the MTL subregions were segmented using the automated segmentation of hippocampal subfields‐T1 (ASHS‐T1) pipeline (Fig. 1a). When modeling the MTL’s interactions with the rest of the cortex, we employed four MTL ROIs (left/right × anterior/posterior) derived from an ex vivo atlas of tau accumulation in the MTL. Our functional datasets were preprocessed using a customized fMRIprep pipeline. Sparse network estimations and modularity‐based consensus clustering were used to reconstruct the AT and PM network systems (Fig. 1b). Age effect analyses and group comparisons along the AD continuum were performed using the General Linear Model within the network‐based statistical framework. Result The preclinical stage of AD was characterized by increased FC between the perirhinal cortex and other regions of the MTL, as well as between the anterior MTL and its direct neighbors in the AT network (Fig. 1c‐d). This effect was not present in symptomatic AD. Instead, symptomatic patients displayed reduced hippocampal and intra‐PM connectivity. For normal aging, our results led to three main conclusions (for visuals, see Fig. 2). First, intra‐network connectivity of both the AT and PM networks decreases with age. Second, FC between the anterior and posterior segments of the MTL declines with age. Finally, within the MTL, we observed greater vulnerability of the posterior MTL subregions, particularly the parahippocampal cortex, to age‐associated FC decline. Conclusion Together, the current results provide evidence for aberrant connectivity in the preclinical stage of AD that may have implications for early AD pathophysiology.
Objective: Mobile, valid, and engaging cognitive assessments are essential for detecting and tracking change in research participants and patients at risk for Alzheimer’s Disease and Related Dementias (ADRDs). The mobile cognitive app performance platform (mCAPP) includes memory and executive functioning tasks to remotely detect cognitive changes associated with aging and preclinical Alzheimer’s disease. This study assesses participants’ comfort and subjective experiences with mCAPP as the potential utility and advantage of mobile app-based assessments for remote monitoring among older adults will depend upon usability and adoptability of such technology. Participants and Methods: The mCAPP includes three gamified tasks: (1) a memory task involving learning and matching hidden card pairs (“Concentration”) (2) a stroop-like task (“Brick Drop”), and (3) a digit-symbol coding-like task (“Space Imposters”). Participants included 37 older adults (60% female; age=72±4.4; years of education=17±2.5; 67% White) with normal cognition enrolled in the Penn ADRC cohort. Participants completed one baseline session of mCAPP in-person, followed by two weeks of at-home use with eight scheduled sessions. Information on prior experience with mobile technology and games was collected, and usability of mCAPP was measured at baseline and after 2-weeks of use with the IBM Computer Usability Satisfaction Questionnaire and the mHeath App Usability Questionnaire (MAUQ) respectively. Feedback on perceived difficulty, enjoyment, and likelihood to play mCAPP games again on their own was collected. Results: Participants completed on average 11±4.9 sessions over 2 weeks, with each session lasting 11.5±2.5 minutes. 59% of participants reported using their mobile device to play games (“mobile game players”). Performance on mCAPP tasks was slower at baseline for non-players, with trend-level differences on higher-load blocks of Space Imposters (p=.057 and .059). No differences in game performance were seen between groups after playing 8 sessions at-home. There were no differences in usability of mCAPP between groups, with average usability 8.2±1.5 (IBM, 0-9 scale) at T1 and 6.2±0.8 (MAUQ, 1-7 scale) after completion of two weeks of at-home use (TLast). Reported enjoyment was moderate to high for both groups at baseline and increased over time. Likelihood to play Concentration and Brick Drop again trended lower among nonplayers at T1 (p=.061 and .054), but not at TLast. Further, change in likelihood to play mCAPP from T1 to TLast was positive among non-players, with change for Concentration significantly higher for non-players than for players (p=.037). Conclusions: Participants were willing and able to complete at-home cognitive testing and most completed more than the assigned sessions. While participants who do not play games on their own mobile device were slower on some tasks at baseline, these differences dissipated with further play at-home. Usability and enjoyment of mCAPP games were high regardless of mobile game-playing status, and non-players demonstrated increased willingness to play mCAPP games again at the end of participation compared to baseline. This pilot study shows preliminary feasibility and adoptability of mobile app-based assessment regardless of prior experience with mobile games.
Mobile, valid and engaging cognitive assessments are essential for detecting and tracking change in research participants and patients at risk for Alzheimer's Disease and Related Dementias (ADRDs). This pilot study aims to determine the feasibility and psychometric properties of app-based memory and executive functioning tasks included in the mobile cognitive app performance platform (mCAPP), to detect cognitive changes associated with aging and preclinical Alzheimer's Disease (AD).The mCAPP includes three gamified tasks: (1) a memory task that includes learning and matching hidden card pairs and incorporates increasing memory load, pattern separation features (lure vs. non-lure), and spatial memory (2) a stroop-like task ("brick drop") with speeded word and color identification and response inhibition components and (3) a digit-symbol coding-like task ("space imposters") with increasing pairs and incidental learning components. The cohort is also assessed with the NACC UDS3 or T-Cog neuropsychological battery within six months of the mCAPP testing. Participants included nine older adults (44% female; age=73.9±5.4, years of education=16.6±2.3; 77% Caucasian) with normal cognition who are enrolled in the Penn ADRC cohort. In addition to in-lab testing, a cohort of participants will also use the mCAPP at home for two weeks and remotely collected data will be presented.On the brick drop task, performance was significantly slower and less accurate on the inhibition task compared to the word and color identification tasks (p<.05). On the space imposters task, increased reaction time and decreased accuracy was observed as the number of digit-symbol pairs increased, but the difference was not significant. Correlations with UDS 3.0 measures showed significant relationships between the brick drop word/color identification and trail making test A (TMTA) and category fluency (p<.05) as well as between the response inhibition task and category fluency and olfactory function (p<.05). The space imposters task correlated with the TMTA (p<.05). Data will also be presented on home-based collection of all three mCAPP tasks.This pilot study shows feasibility and validity of app-based tests of executive functioning and will also examine detection of subtle cognitive differences associated with preclinical AD through burst testing, home-based data collection and on all three mCAPP measures.
Abstract Background In previous work (Das et al., 2021), we exploited the non‐specific nature of neurodegeneration by investigating the amount and spatial pattern of deviation from the level of neurodegeneration (N) expected for a given level of tau (T). Using a data‐driven clustering approach based on T‐N mismatch , we found phenotypes that had greater N than expected for T (“vulnerable”) and phenotypes with less N than expected for T (“resilient”) in specific patterns. Here we extend this work to include amyloid positive (A+) and negative (A‐) participants. The logic of inclusion of A‐ individuals is that areas of mismatch in A+ individuals is likely driven by factors outside of AD pathology, which can be present in the absence of AD pathology. Method We employed cortical thickness to represent N and 18 F‐flortaucipir tracer uptake as T for 104 bilateral cortical regions of interest (ROI) in 343 symptomatic individuals including both A+ and A‐ from ADNI. We established T‐N robust regression and partitioned participants based on thresholded residuals. Longitudinal trajectories of cognitive scores were assessed with linear mixed‐effects model effect models using CDRSB as the dependent variable. Result We replicated prior work and obtained clusters with distinct T‐N mismatch patterns. We defined the largest group as “canonical”, as it displayed typical T‐N relationships (N∼T, low residuals). The limbic vulnerable cluster displayed N>T (negative residuals) in limbic regions, while diffuse vulnerable group displayed N>T throughout the cortex. Alternatively, the resilient (N<T, positive residuals) clusters were classified as limbic resilient or prefrontal resilient based on the pattern of this relationship. Note the highly similar regional patterns of the A+ and A‐ subgroups, supporting our hypothesis that this residual reflects non‐AD related phenomenology which could be present irrespective of amyloid status. Phenotypes differed in longitudinal cognitive trajectories. The vulnerable clusters declined significantly faster than the canonical cluster regardless of amyloid status likely attributable to the presence of non‐AD pathologies. The resilient groups tended to progress less than the canonical group. Conclusion Our findings suggest T‐N mismatch depicts vulnerability and resilience likely attributable to non‐AD factors. This may provide an approach for detecting co‐pathologies in AD continuum and benefiting therapeutic management.
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