The Impact of Neurodegeneration on Network Connectivity: A Study of Change Detection in Frontotemporal Dementia

The neural response to unpredictable auditory events is suggested to depend on frontotemporal interactions. We used magnetoencephalography in patients with behavioral variant frontotemporal dementia to study change detection and to examine the impact of disease on macroscopic network connectivity underlying this core cognitive function. In patients, the amplitudes of auditory cortical responses to predictable standard tones were normal but were reduced for unpredictable deviant tones. Network connectivity, in terms of coherence among frontal, temporal, and parietal sources, was also abnormal in patients. In the beta frequency range, left frontotemporal coherence was reduced. In the gamma frequency range, frontal interhemispheric coherence was reduced whereas parietal interhemispheric coherence was enhanced. These results suggest impaired change detection resulting from dysfunctional frontotemporal interactions. They also provide evidence of a rostro-caudal reorganization of brain networks in disease. The sensitivity of magnetoencephalography to cortical network changes in behavioral variant frontotemporal dementia enriches the understanding of neurocognitive systems as well as showing potential for studies of experimental therapies for neurodegenerative disease.

[1]  I. Winkler,et al.  Memory-based or afferent processes in mismatch negativity (MMN): a review of the evidence. , 2005, Psychophysiology.

[2]  G. Frisoni,et al.  Functional network disruption in the degenerative dementias , 2011, The Lancet Neurology.

[3]  Sébastien Ourselin,et al.  Distinct profiles of brain atrophy in frontotemporal lobar degeneration caused by progranulin and tau mutations☆ , 2010, NeuroImage.

[4]  S. Rossi,et al.  Clinical neurophysiology of aging brain: From normal aging to neurodegeneration , 2007, Progress in Neurobiology.

[5]  Erich Schröger,et al.  Prefrontal cortex involvement in preattentive auditory deviance detection: neuroimaging and electrophysiological evidence , 2003, NeuroImage.

[6]  James B. Rowe,et al.  Magnetoencephalography of frontotemporal dementia: spatiotemporally localized changes during semantic decisions. , 2011, Brain : a journal of neurology.

[7]  R. Faber,et al.  Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. , 1999, Neurology.

[8]  Yung-Yang Lin,et al.  Cortico-cortical phase synchrony in auditory mismatch processing , 2010, Biological Psychology.

[9]  Karl J. Friston,et al.  A Dual Role for Prediction Error in Associative Learning , 2008, Cerebral cortex.

[10]  Karsten Hoechstetter,et al.  BESA Source Coherence: A New Method to Study Cortical Oscillatory Coupling , 2003, Brain Topography.

[11]  R. Thatcher,et al.  Cortico-cortical associations and EEG coherence: a two-compartmental model. , 1986, Electroencephalography and clinical neurophysiology.

[12]  Karl J. Friston,et al.  Action and behavior: a free-energy formulation , 2010, Biological Cybernetics.

[13]  Guy B. Williams,et al.  Neural correlates of semantic and behavioural deficits in frontotemporal dementia , 2005, NeuroImage.

[14]  S. Moratti,et al.  Dysfunctional and compensatory duality in mild cognitive impairment during a continuous recognition memory task. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  Karl J. Friston,et al.  Preserved Feedforward But Impaired Top-Down Processes in the Vegetative State , 2011, Science.

[16]  R. Näätänen,et al.  The mismatch negativity (MMN) – A unique window to disturbed central auditory processing in ageing and different clinical conditions , 2012, Clinical Neurophysiology.

[17]  James B. Rowe,et al.  Reorganisation of brain networks in frontotemporal dementia and progressive supranuclear palsy☆ , 2013, NeuroImage: Clinical.

[18]  B. Bilican,et al.  Cell-Mediated Neuroprotection in a Mouse Model of Human Tauopathy , 2010, The Journal of Neuroscience.

[19]  J. Ahveninen,et al.  Serotonergic modulation of mismatch negativity , 2005, Psychiatry Research: Neuroimaging.

[20]  C. Stam Use of magnetoencephalography (MEG) to study functional brain networks in neurodegenerative disorders , 2010, Journal of the Neurological Sciences.

[21]  Efstathios D. Gennatas,et al.  Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. , 2010, Brain : a journal of neurology.

[22]  Chia-Hsiung Cheng,et al.  Inadequate inhibition of redundant auditory inputs in Alzheimer's disease: An MEG study , 2012, Biological Psychology.

[23]  Karl J. Friston,et al.  The functional anatomy of the MMN: A DCM study of the roving paradigm , 2008, NeuroImage.

[24]  Nick C Fox,et al.  Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. , 2011, Brain : a journal of neurology.

[25]  Ulrich Schall,et al.  Functional neuroanatomy of auditory mismatch processing: an event-related fMRI study of duration-deviant oddballs , 2003, NeuroImage.

[26]  D L Woods,et al.  Lesions of frontal cortex diminish the auditory mismatch negativity. , 1994, Electroencephalography and clinical neurophysiology.

[27]  J. Rowe Frontiers in Systems Neuroscience Systems Neuroscience , 2010 .

[28]  J R Hodges,et al.  Atrophy patterns in histologic vs clinical groupings of frontotemporal lobar degeneration , 2009, Neurology.

[29]  Cornelis J. Stam,et al.  Magnetoencephalographic evaluation of resting-state functional connectivity in Alzheimer's disease , 2006, NeuroImage.

[30]  J. Hodges,et al.  Nonprogressive behavioural frontotemporal dementia: recent developments and clinical implications of the 'bvFTD phenocopy syndrome'. , 2010, Current opinion in neurology.

[31]  F. Boers,et al.  Optimized mismatch negativity paradigm reflects deficits in schizophrenia patients A combined EEG and MEG study , 2008, Biological Psychology.

[32]  Karl J. Friston,et al.  Selecting forward models for MEG source-reconstruction using model-evidence , 2009, NeuroImage.

[33]  Fernando Maestú,et al.  Functional connectivity in mild cognitive impairment during a memory task: implications for the disconnection hypothesis. , 2010, Journal of Alzheimer's disease : JAD.

[34]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[35]  M. Hämäläinen,et al.  Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data , 1989, IEEE Transactions on Biomedical Engineering.

[36]  William D. Marslen-Wilson,et al.  The Cambridge Centre for Ageing and Neuroscience (Cam-CAN) study protocol: a cross-sectional, lifespan, multidisciplinary examination of healthy cognitive ageing , 2014, BMC Neurology.

[37]  R. Barker,et al.  The utility of the Cambridge Behavioural Inventory in neurodegenerative disease , 2007, Journal of Neurology Neurosurgery & Psychiatry.

[38]  J. Changeux,et al.  A Neuronal Model of Predictive Coding Accounting for the Mismatch Negativity , 2012, The Journal of Neuroscience.

[39]  C R Jack,et al.  Voxel-based morphometry patterns of atrophy in FTLD with mutations in MAPT or PGRN , 2009, Neurology.

[40]  Raymond J. Dolan,et al.  Computational and dynamic models in neuroimaging , 2010, NeuroImage.

[41]  R. Näätänen,et al.  The mismatch negativity: an index of cognitive decline in neuropsychiatric and neurological diseases and in ageing. , 2011, Brain : a journal of neurology.

[42]  D. Mumford On the computational architecture of the neocortex , 2004, Biological Cybernetics.

[43]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[44]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[45]  Karl J. Friston,et al.  The mismatch negativity: A review of underlying mechanisms , 2009, Clinical Neurophysiology.

[46]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[47]  R. Knight,et al.  A distributed cortical network for auditory sensory memory in humans , 1998, Brain Research.

[48]  Razumov An,et al.  [The modern approaches to the prognostication of rehabilitation of the patients after stroke on an individual basis: a review of the literature and the results of original investigations]. , 2015 .

[49]  Guy B. Williams,et al.  Atrophy, hypometabolism and white matter abnormalities in semantic dementia tell a coherent story. , 2011, Brain : a journal of neurology.

[50]  J. Schneider,et al.  Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration , 2007, Acta Neuropathologica.

[51]  S. D. Penna,et al.  Cortical rhythms reactivity in AD, LBD and normal subjects: A quantitative MEG study , 2006, Neurobiology of Aging.

[52]  R. Näätänen,et al.  The adaptive brain: A neurophysiological perspective , 2010, Progress in Neurobiology.

[53]  Aniruddh D. Patel,et al.  Top‐Down Control of Rhythm Perception Modulates Early Auditory Responses , 2009, Annals of the New York Academy of Sciences.

[54]  Karl J. Friston,et al.  Predictive coding under the free-energy principle , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[55]  John R Hodges,et al.  The Addenbrooke's Cognitive Examination Revised (ACE‐R): a brief cognitive test battery for dementia screening , 2006, International journal of geriatric psychiatry.

[56]  R. Johansson,et al.  Prediction Precedes Control in Motor Learning , 2003, Current Biology.

[57]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[58]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[59]  M. Corbetta,et al.  Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke , 2009, Annals of neurology.

[60]  V. Knott,et al.  Nicotine and sensory memory in Alzheimer's disease: an event-related potential study. , 2002, Brain and cognition.

[61]  I. Mackenzie The Neuropathology of FTD Associated With ALS , 2007, Alzheimer disease and associated disorders.

[62]  F. Perrin,et al.  Brain generators implicated in the processing of auditory stimulus deviance: a topographic event-related potential study. , 1990, Psychophysiology.

[63]  Luc H. Arnal,et al.  Transitions in neural oscillations reflect prediction errors generated in audiovisual speech , 2011, Nature Neuroscience.

[64]  Tobias Egner,et al.  Cerebral Cortex doi:10.1093/cercor/bhi129 Mistaking a House for a Face: Neural Correlates of Misperception in Healthy Humans , 2005 .

[65]  R. Näätänen,et al.  The mismatch negativity (MMN): towards the optimal paradigm , 2004, Clinical Neurophysiology.

[66]  B. Boeve,et al.  Frontotemporal Dementia Treatment: Current Symptomatic Therapies and Implications of Recent Genetic, Biochemical, and Neuroimaging Studies , 2007, Alzheimer disease and associated disorders.

[67]  R Salmelin,et al.  The 3D topography of MEG source localization accuracy: effects of conductor model and noise , 2003, Clinical Neurophysiology.

[68]  James T. Becker,et al.  Magnetoencephalography as a Putative Biomarker for Alzheimer's Disease , 2011, International journal of Alzheimer's disease.

[69]  Yan Yang Schmitt Frontotemporal dementia : evidence for impairment of ascending serotoninergic but not noradrenergic innervation Immunocytochemical and quantitative study using a graph method , 2022 .

[70]  Karl J. Friston,et al.  A Hierarchy of Time-Scales and the Brain , 2008, PLoS Comput. Biol..

[71]  Maria Luisa Gorno-Tempini,et al.  Frontal paralimbic network atrophy in very mild behavioral variant frontotemporal dementia. , 2008, Archives of neurology.

[72]  B. Miller,et al.  Neurodegenerative Diseases Target Large-Scale Human Brain Networks , 2009, Neuron.

[73]  D Mumford,et al.  On the computational architecture of the neocortex. II. The role of cortico-cortical loops. , 1992, Biological cybernetics.

[74]  Jean-Claude Baron,et al.  Decomposition of metabolic brain clusters in the frontal variant of frontotemporal dementia , 2006, NeuroImage.

[75]  Yury Shtyrov,et al.  Fast reconfiguration of high-frequency brain networks in response to surprising changes in auditory input. , 2012, Journal of neurophysiology.

[76]  E. Pekkonen,et al.  Auditory Sensory Memory and the Cholinergic System: Implications for Alzheimer's Disease , 2001, NeuroImage.

[77]  E. Pekkonen Mismatch Negativity in Aging and in Alzheimer’s and Parkinson’s Diseases , 2000, Audiology and Neurotology.

[78]  Michael A. DiSano,et al.  Intracranial EEG Reveals a Time- and Frequency-Specific Role for the Right Inferior Frontal Gyrus and Primary Motor Cortex in Stopping Initiated Responses , 2009, The Journal of Neuroscience.

[79]  E. Miller,et al.  Serial, Covert Shifts of Attention during Visual Search Are Reflected by the Frontal Eye Fields and Correlated with Population Oscillations , 2009, Neuron.

[80]  Barry Horwitz,et al.  Functional biomarkers for neurodegenerative disorders based on the network paradigm , 2011, Progress in Neurobiology.

[81]  Iiro P. Jääskeläinen,et al.  Tryptophan Depletion Effects on EEG and MEG Responses Suggest Serotonergic Modulation of Auditory Involuntary Attention in Humans , 2002, NeuroImage.

[82]  Karl J. Friston,et al.  Dynamic Causal Modeling of the Response to Frequency Deviants , 2009, Journal of neurophysiology.

[83]  Nick C Fox,et al.  Measuring disease progression in frontotemporal lobar degeneration , 2010, Neurology.

[84]  Risto Näätänen,et al.  Central auditory dysfunction in schizophrenia as revealed by the mismatch negativity (MMN) and its magnetic equivalent MMNm: a review. , 2009, The international journal of neuropsychopharmacology.

[85]  K. Alho,et al.  Intracranial identification of an electric frontal-cortex response to auditory stimulus change: a case study. , 2001, Brain research. Cognitive brain research.

[86]  C. Gray,et al.  Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[87]  R. Näätänen,et al.  The mismatch negativity (MMN) in basic research of central auditory processing: A review , 2007, Clinical Neurophysiology.

[88]  C R Jack,et al.  Gray and white matter water diffusion in the syndromic variants of frontotemporal dementia , 2010, Neurology.

[89]  Efstathios D. Gennatas,et al.  TDP-43 subtypes are associated with distinct atrophy patterns in frontotemporal dementia , 2010, Neurology.

[90]  W. M. van der Flier,et al.  Functional neural network analysis in frontotemporal dementia and Alzheimer's disease using EEG and graph theory , 2009, BMC Neuroscience.

[91]  Klaus Linkenkaer-Hansen,et al.  Flexible spike timing of layer 5 neurons during dynamic beta oscillation shifts in rat prefrontal cortex , 2009, The Journal of physiology.

[92]  Efstathios D. Gennatas,et al.  Predicting Regional Neurodegeneration from the Healthy Brain Functional Connectome , 2012, Neuron.

[93]  J R Hodges,et al.  Combined magnetic resonance imaging and positron emission tomography brain imaging in behavioural variant frontotemporal degeneration: refining the clinical phenotype. , 2009, Brain : a journal of neurology.

[94]  A. Engel,et al.  Cognitive functions of gamma-band activity: memory match and utilization , 2004, Trends in Cognitive Sciences.

[95]  Jordan Grafman,et al.  A systematic review of neurotransmitter deficits and treatments in frontotemporal dementia , 2006, Neurology.

[96]  C. Elger,et al.  Subdural recordings of the mismatch negativity (MMN) in patients with focal epilepsy. , 2005, Brain : a journal of neurology.

[97]  K. Alho,et al.  Generators of electrical and magnetic mismatch responses in humans , 2005, Brain Topography.

[98]  Dag Aarsland,et al.  Disturbance of automatic auditory change detection in dementia associated with Parkinson's disease: A mismatch negativity study , 2010, Neurobiology of Aging.

[99]  Piet Van Mieghem,et al.  Disruption of Functional Brain Networks in Alzheimer's Disease: What Can We Learn from Graph Spectral Analysis of Resting-State Magnetoencephalography? , 2012, Brain Connect..

[100]  S. Dehaene,et al.  Evidence for a hierarchy of predictions and prediction errors in human cortex , 2011, Proceedings of the National Academy of Sciences.