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      Evidence and implications of abnormal predictive coding in dementia

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          Abstract

          The diversity of cognitive deficits and neuropathological processes associated with dementias has encouraged divergence in pathophysiological explanations of disease. Here, we review an alternative framework that emphasizes convergent critical features of cognitive pathophysiology. Rather than the loss of ‘memory centres’ or ‘language centres’, or singular neurotransmitter systems, cognitive deficits are interpreted in terms of aberrant predictive coding in hierarchical neural networks. This builds on advances in normative accounts of brain function, specifically the Bayesian integration of beliefs and sensory evidence in which hierarchical predictions and prediction errors underlie memory, perception, speech and behaviour. We describe how analogous impairments in predictive coding in parallel neurocognitive systems can generate diverse clinical phenomena, including the characteristics of dementias. The review presents evidence from behavioural and neurophysiological studies of perception, language, memory and decision-making. The reformulation of cognitive deficits in terms of predictive coding has several advantages. It brings diverse clinical phenomena into a common framework; it aligns cognitive and movement disorders; and it makes specific predictions on cognitive physiology that support translational and experimental medicine studies. The insights into complex human cognitive disorders from the predictive coding framework may therefore also inform future therapeutic strategies.

          Abstract

          Kocagoncu et al. propose an alternative framework for interpreting the cognitive deficits observed in dementia. They argue that deficits should be considered in terms of aberrant predictive coding in hierarchical neural networks, rather than as reflecting the loss of functional hubs or singular neurotransmitter systems.

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          Most cited references201

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          Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects.

          We describe a model of visual processing in which feedback connections from a higher- to a lower-order visual cortical area carry predictions of lower-level neural activities, whereas the feedforward connections carry the residual errors between the predictions and the actual lower-level activities. When exposed to natural images, a hierarchical network of model neurons implementing such a model developed simple-cell-like receptive fields. A subset of neurons responsible for carrying the residual errors showed endstopping and other extra-classical receptive-field effects. These results suggest that rather than being exclusively feedforward phenomena, nonclassical surround effects in the visual cortex may also result from cortico-cortical feedback as a consequence of the visual system using an efficient hierarchical strategy for encoding natural images.
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            Event-related EEG/MEG synchronization and desynchronization: basic principles.

            An internally or externally paced event results not only in the generation of an event-related potential (ERP) but also in a change in the ongoing EEG/MEG in form of an event-related desynchronization (ERD) or event-related synchronization (ERS). The ERP on the one side and the ERD/ERS on the other side are different responses of neuronal structures in the brain. While the former is phase-locked, the latter is not phase-locked to the event. The most important difference between both phenomena is that the ERD/ERS is highly frequency band-specific, whereby either the same or different locations on the scalp can display ERD and ERS simultaneously. Quantification of ERD/ERS in time and space is demonstrated on data from a number of movement experiments.
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              Whatever next? Predictive brains, situated agents, and the future of cognitive science.

              Andy Clark (2013)
              Brains, it has recently been argued, are essentially prediction machines. They are bundles of cells that support perception and action by constantly attempting to match incoming sensory inputs with top-down expectations or predictions. This is achieved using a hierarchical generative model that aims to minimize prediction error within a bidirectional cascade of cortical processing. Such accounts offer a unifying model of perception and action, illuminate the functional role of attention, and may neatly capture the special contribution of cortical processing to adaptive success. This target article critically examines this "hierarchical prediction machine" approach, concluding that it offers the best clue yet to the shape of a unified science of mind and action. Sections 1 and 2 lay out the key elements and implications of the approach. Section 3 explores a variety of pitfalls and challenges, spanning the evidential, the methodological, and the more properly conceptual. The paper ends (sections 4 and 5) by asking how such approaches might impact our more general vision of mind, experience, and agency.
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                Author and article information

                Journal
                Brain
                Brain
                brainj
                Brain
                Oxford University Press
                0006-8950
                1460-2156
                November 2021
                08 July 2021
                08 July 2021
                : 144
                : 11
                : 3311-3321
                Affiliations
                [1 ] Cambridge Centre for Frontotemporal Dementia, Department of Clinical Neurosciences, University of Cambridge , Cambridge CB2 0SZ, UK
                [2 ] Medical Research Council Cognition and Brain Sciences Unit, University of Cambridge , Cambridge CB2 7EF, UK
                [3 ] Cambridge University Hospital NHS Foundation Trust, University of Cambridge , Cambridge, CB2 2QQ, UK
                [4 ] Basque Centre on Cognition, Brain and Language , San Sebastian 20009, Spain
                Author notes
                Correspondence to: Ece Kocagoncu, PhD MRC Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, UK E-mail: ece.kocagoncu@ 123456cantab.net
                Author information
                https://orcid.org/0000-0002-6292-7472
                Article
                awab254
                10.1093/brain/awab254
                8677549
                34240109
                412b223a-b022-4fa7-978a-7a96b7e8e7f0
                © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 06 December 2020
                : 15 March 2021
                : 17 June 2021
                : 13 December 2021
                Page count
                Pages: 11
                Funding
                Funded by: Dementias Platform UK and Alzheimer’s Research UK;
                Award ID: RG94383
                Award ID: RG89702
                Funded by: Wellcome Trust, DOI 10.13039/100010269;
                Award ID: 103838
                Funded by: Medical Research Council, DOI 10.13039/501100000265;
                Award ID: SUAG/051 G101400
                Funded by: National Institute for Health Research Cambridge Biomedical Research Centre, DOI 10.13039/501100018956;
                Funded by: Wellcome Trust, DOI 10.13039/100010269;
                Award ID: 103838
                Funded by: European Union’s Horizon 2020 Research and Innovation Programme;
                Funded by: Marie Skłodowska-Curie;
                Award ID: 798971
                Categories
                Update
                AcademicSubjects/MED00310
                AcademicSubjects/SCI01870

                Neurosciences
                predictive coding,dementia,top-down processing,prediction,neurodegeneration
                Neurosciences
                predictive coding, dementia, top-down processing, prediction, neurodegeneration

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