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      Diminished Posterior Precuneus Connectivity with the Default Mode Network Differentiates Normal Aging from Alzheimer's Disease

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          Abstract

          Both normal aging and Alzheimer's disease (AD) have been associated with a reduction in functional brain connectivity. It is unknown how connectivity patterns due to aging and AD compare. Here, we investigate functional brain connectivity in 12 young adults (mean age 22.8 ± 2.8), 12 older adults (mean age 73.1 ± 5.2) and 12 AD patients (mean age 74.0 ± 5.2; mean MMSE 22.3 ± 2.5). Participants were scanned during 6 different sessions with resting state functional magnetic resonance imaging (RS-fMRI), resulting in 72 scans per group. Voxelwise connectivity with 10 functional networks was compared between groups ( p < 0.05, corrected). Normal aging was characterized by widespread decreases in connectivity with multiple brain networks, whereas AD only affected connectivity between the default mode network (DMN) and precuneus. The preponderance of effects was associated with regional gray matter volume. Our findings indicate that aging has a major effect on functional brain interactions throughout the entire brain, whereas AD is distinguished by additional diminished posterior DMN-precuneus coherence.

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          Searching for a baseline: functional imaging and the resting human brain.

          Functional brain imaging in humans has revealed task-specific increases in brain activity that are associated with various mental activities. In the same studies, mysterious, task-independent decreases have also frequently been encountered, especially when the tasks of interest have been compared with a passive state, such as simple fixation or eyes closed. These decreases have raised the possibility that there might be a baseline or resting state of brain function involving a specific set of mental operations. We explore this possibility, including the manner in which we might define a baseline and the implications of such a baseline for our understanding of brain function.
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            From sensation to cognition.

            M. Mesulam (1998)
            Sensory information undergoes extensive associative elaboration and attentional modulation as it becomes incorporated into the texture of cognition. This process occurs along a core synaptic hierarchy which includes the primary sensory, upstream unimodal, downstream unimodal, heteromodal, paralimbic and limbic zones of the cerebral cortex. Connections from one zone to another are reciprocal and allow higher synaptic levels to exert a feedback (top-down) influence upon earlier levels of processing. Each cortical area provides a nexus for the convergence of afferents and divergence of efferents. The resultant synaptic organization supports parallel as well as serial processing, and allows each sensory event to initiate multiple cognitive and behavioural outcomes. Upstream sectors of unimodal association areas encode basic features of sensation such as colour, motion, form and pitch. More complex contents of sensory experience such as objects, faces, word-forms, spatial locations and sound sequences become encoded within downstream sectors of unimodal areas by groups of coarsely tuned neurons. The highest synaptic levels of sensory-fugal processing are occupied by heteromodal, paralimbic and limbic cortices, collectively known as transmodal areas. The unique role of these areas is to bind multiple unimodal and other transmodal areas into distributed but integrated multimodal representations. Transmodal areas in the midtemporal cortex, Wernicke's area, the hippocampal-entorhinal complex and the posterior parietal cortex provide critical gateways for transforming perception into recognition, word-forms into meaning, scenes and events into experiences, and spatial locations into targets for exploration. All cognitive processes arise from analogous associative transformations of similar sets of sensory inputs. The differences in the resultant cognitive operation are determined by the anatomical and physiological properties of the transmodal node that acts as the critical gateway for the dominant transformation. Interconnected sets of transmodal nodes provide anatomical and computational epicentres for large-scale neurocognitive networks. In keeping with the principles of selectively distributed processing, each epicentre of a large-scale network displays a relative specialization for a specific behavioural component of its principal neurospychological domain. The destruction of transmodal epicentres causes global impairments such as multimodal anomia, neglect and amnesia, whereas their selective disconnection from relevant unimodal areas elicits modality-specific impairments such as prosopagnosia, pure word blindness and category-specific anomias. The human brain contains at least five anatomically distinct networks. The network for spatial awareness is based on transmodal epicentres in the posterior parietal cortex and the frontal eye fields; the language network on epicentres in Wernicke's and Broca's areas; the explicit memory/emotion network on epicentres in the hippocampal-entorhinal complex and the amygdala; the face-object recognition network on epicentres in the midtemporal and temporopolar cortices; and the working memory-executive function network on epicentres in the lateral prefrontal cortex and perhaps the posterior parietal cortex. Individual sensory modalities give rise to streams of processing directed to transmodal nodes belonging to each of these networks. The fidelity of sensory channels is actively protected through approximately four synaptic levels of sensory-fugal processing. The modality-specific cortices at these four synaptic levels encode the most veridical representations of experience. Attentional, motivational and emotional modulations, including those related to working memory, novelty-seeking and mental imagery, become increasingly more pronounced within downstream components of unimodal areas, where they help to create a highly edited subjective version of the world. (ABSTRACT TRUNCATED)
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              Changes in hippocampal connectivity in the early stages of Alzheimer's disease: evidence from resting state fMRI.

              A selective distribution of Alzheimer's disease (AD) pathological lesions in specific cortical layers isolates the hippocampus from the rest of the brain. However, functional connectivity between the hippocampus and other brain regions remains unclear in AD. Here, we employ a resting state functional MRI (fMRI) to examine changes in hippocampal connectivity comparing 13 patients with mild AD versus 13 healthy age-matched controls. Hippocampal connectivity was investigated by examination of the correlation between low frequency fMRI signal fluctuations in the hippocampus and those in all other brain regions. We found that functional connectivity between the right hippocampus and a set of regions was disrupted in AD; these regions are: medial prefrontal cortex (MPFC), ventral anterior cingulate cortex (vACC), right inferotemporal cortex, right cuneus extending into precuneus, left cuneus, right superior and middle temporal gyrus and posterior cingulate cortex (PCC). We also found increased functional connectivity between the left hippocampus and the right lateral prefrontal cortex in AD. In addition, rightward asymmetry of hippocampal connectivity observed in elderly controls was diminished in AD patients. The disrupted hippocampal connectivity to the MPFC, vACC and PCC provides further support for decreased activity in "default mode network" previously shown in AD. The decreased connectivity between the hippocampus and the visual cortices might indicate reduced integrity of hippocampus-related cortical networks in AD. Moreover, these findings suggest that resting-state fMRI might be an appropriate approach for studying pathophysiological changes in early AD.
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                Author and article information

                Contributors
                Journal
                Front Aging Neurosci
                Front Aging Neurosci
                Front. Aging Neurosci.
                Frontiers in Aging Neuroscience
                Frontiers Media S.A.
                1663-4365
                19 April 2017
                2017
                : 9
                : 97
                Affiliations
                [1] 1Institute of Psychology, Leiden University Leiden, Netherlands
                [2] 2Department of Radiology, Leiden University Medical Center Leiden, Netherlands
                [3] 3Leiden Institute for Brain and Cognition, Leiden University Leiden, Netherlands
                [4] 4Centre for Human Drug Research Leiden, Netherlands
                Author notes

                Edited by: Pedro Rosa-Neto, McGill University, Canada

                Reviewed by: Blas Couto, Institute of Cognitive Neurology, Argentina; Arnaud Charil, Australian Nuclear Science and Technology Organisation, Australia

                *Correspondence: Bernadet L. Klaassens b.l.klaassens@ 123456fsw.leidenuniv.nl
                Article
                10.3389/fnagi.2017.00097
                5395570
                28469571
                bcf4e3ec-ccd2-4457-a8ae-6e7e06654821
                Copyright © 2017 Klaassens, van Gerven, van der Grond, de Vos, Möller and Rombouts.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 29 November 2016
                : 28 March 2017
                Page count
                Figures: 3, Tables: 3, Equations: 0, References: 89, Pages: 13, Words: 9009
                Categories
                Neuroscience
                Original Research

                Neurosciences
                alzheimer's disease,dementia,aging,brain connectivity,functional network,resting state fmri,functional connectivity

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