Altered hemodynamic oscillations of resting-state networks in mesial temporal lobe epilepsy

Mesial-temporal lobe epilepsy (mTLE), a neurological disorder characterized by abnormal synchronous discharges in a large cell population, affects the hemodynamic activities of functional networks remote from the epileptogenic zone and causes widespread deficits in brain functions. Although a number of resting-state fMRI studies have found altered spatial patterns in the canonical resting-state networks (RSNs) in patients with mTLE, including the default mode network (DMN), dorsal lateral attention network (DAN), auditory network (AUN), somatosensory network (SMN) and visual network (VIN), none of these studies has addressed the question whether the frequencies of hemodynamic oscillations in these RSNs were altered. In the present study, we have proposed a network-based temporal clustering analysis (TCA) method to characterize the resting hemodynamic activity of a large-scale functional network. First, the RSNs were identified in healthy controls as well in the left mTLE patients using independent component analysis (ICA). Then, a time course representing the hemodynamic activity of each RSN was extracted by counting the number of the voxels that were activated simultaneously at each time point within the network. Finally, the power spectral density (PSD) of the time course was estimated. Our results have demonstrated significant differences in the frequency profiles of the SMN, VIN and left DAN between the patients and controls: the peaks of these spectra shifted toward a lower frequency in the patients, while more power was distributed over higher frequency bands in the healthy controls. However, no significant difference has been found in the AUN, DMN and right DAN. These features might serve as biomarkers to differentiate the patients from controls.

[1]  Simon B Eickhoff,et al.  Investigating the Functional Heterogeneity of the Default Mode Network Using Coordinate-Based Meta-Analytic Modeling , 2009, The Journal of Neuroscience.

[2]  W. Liao,et al.  Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI , 2009, Journal of Neurology.

[3]  Huafu Chen,et al.  Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy , 2010, Brain Research.

[4]  Peter T. Fox,et al.  The temporal response of the brain after eating revealed by functional MRI , 2000, Nature.

[5]  W. Liao,et al.  Impaired attention network in temporal lobe epilepsy: A resting FMRI study , 2009, Neuroscience Letters.

[6]  Jeong Hyun Lee,et al.  Central auditory processing impairment in patients with temporal lobe epilepsy , 2011, Epilepsy & Behavior.

[7]  S. Spencer Neural Networks in Human Epilepsy: Evidence of and Implications for Treatment , 2002, Epilepsia.

[8]  S. Strogatz,et al.  Synchronization of pulse-coupled biological oscillators , 1990 .

[9]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[10]  A. Kleinschmidt,et al.  Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. Baulac,et al.  Processing of rapid auditory information in epileptic patients with left temporal lobe damage , 2001, Neuropsychologia.

[12]  B. Jabbari,et al.  Somatosensory Auras in Refractory Temporal Lobe Epilepsy , 2006, Epilepsia.

[13]  P. Welch The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

[14]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[15]  Seung Bong Hong,et al.  Cerebral perfusion changes in mesial temporal lobe epilepsy: SPM analysis of ictal and interictal SPECT , 2005, NeuroImage.

[16]  R. Goodman,et al.  Distribution of Auditory and Visual Naming Sites in Nonlesional Temporal Lobe Epilepsy Patients and Patients with Space‐Occupying Temporal Lobe Lesions , 2007, Epilepsia.

[17]  V. Haughton,et al.  Frequencies contributing to functional connectivity in the cerebral cortex in "resting-state" data. , 2001, AJNR. American journal of neuroradiology.

[18]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[19]  K. Sathian,et al.  Somatosensory Processing Is Impaired in Temporal Lobe Epilepsy , 2005, Epilepsia.

[20]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[21]  M. Young,et al.  Neuronal population activity and functional imaging , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[22]  P. Uvebrant,et al.  Motor and Sensory Impairments in Children with Intractable Epilepsy , 1993, Epilepsia.

[23]  H. Wieser,et al.  Mesial Temporal Lobe Epilepsy with Hippocampal Sclerosis , 2004 .

[24]  Tülay Adali,et al.  Estimating the number of independent components for functional magnetic resonance imaging data , 2007, Human brain mapping.

[25]  M. Piccirilli,et al.  Attention Problems in Epilepsy: Possible Significance of the Epileptogenic Focus , 1994, Epilepsia.

[26]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[27]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[28]  A. Villringer,et al.  Spontaneous Low Frequency Oscillations of Cerebral Hemodynamics and Metabolism in Human Adults , 2000, NeuroImage.

[29]  S. Graham,et al.  An fMRI study of the Trail Making Test , 2005, Neuropsychologia.

[30]  M. Raichle Functional Brain Imaging and Human Brain Function , 2003, The Journal of Neuroscience.

[31]  Colin Studholme,et al.  Positive and negative network correlations in temporal lobe epilepsy. , 2004, Cerebral cortex.

[32]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[33]  T. Grunwald,et al.  Hippocampal function and visual object processing in temporal lobe epilepsy , 2003, Neuroreport.

[34]  Stephen M. Smith,et al.  fMRI resting state networks define distinct modes of long-distance interactions in the human brain , 2006, NeuroImage.

[35]  V. Calhoun,et al.  Modulation of temporally coherent brain networks estimated using ICA at rest and during cognitive tasks , 2008, Human brain mapping.

[36]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Ivanei E. Bramati,et al.  The cerebral correlates of set-shifting: an fMRI study of the trail making test. , 2002, Arquivos de neuro-psiquiatria.

[38]  P. Fox,et al.  Temporal dissociation of parallel processing in the human subcortical outputs , 1999, Nature.

[39]  Stephen M Smith,et al.  Correspondence of the brain's functional architecture during activation and rest , 2009, Proceedings of the National Academy of Sciences.

[40]  H. Jokeit,et al.  Long term effects of refractory temporal lobe epilepsy on cognitive abilities: a cross sectional study , 1999, Journal of neurology, neurosurgery, and psychiatry.

[41]  Huafu Chen,et al.  fMRI study of mesial temporal lobe epilepsy using amplitude of low‐frequency fluctuation analysis , 2010, Human brain mapping.

[42]  Arthur C. Grant,et al.  Interictal perceptual function in epilepsy , 2005, Epilepsy & Behavior.

[43]  B. Harrison,et al.  Consistency and functional specialization in the default mode brain network , 2008, Proceedings of the National Academy of Sciences.

[44]  Patrick Dupont,et al.  Correlations of interictal FDG-PET metabolism and ictal SPECT perfusion changes in human temporal lobe epilepsy with hippocampal sclerosis , 2006, NeuroImage.

[45]  L. Lemieux,et al.  Combined EEG-fMRI and tractography to visualise propagation of epileptic activity , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[46]  Stephen M. Smith,et al.  Investigations into resting-state connectivity using independent component analysis , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[47]  D J Mikulis,et al.  Functional MRI of phonological and semantic processing in temporal lobe epilepsy. , 2001, Brain : a journal of neurology.