Temporal lobe interictal epileptic discharges affect cerebral activity in “default mode” brain regions

A cerebral network comprising precuneus, medial frontal, and temporoparietal cortices is less active both during goal‐directed behavior and states of reduced consciousness than during conscious rest. We tested the hypothesis that the interictal epileptic discharges affect activity in these brain regions in patients with temporal lobe epilepsy who have complex partial seizures. At the group level, using electroencephalography‐correlated functional magnetic resonance imaging in 19 consecutive patients with focal epilepsy, we found common decreases of resting state activity in 9 patients with temporal lobe epilepsy (TLE) but not in 10 patients with extra‐TLE. We infer that the functional consequences of TLE interictal epileptic discharges are different from those in extra‐TLE and affect ongoing brain function. Activity increases were detected in the ipsilateral hippocampus in patients with TLE, and in subthalamic, bilateral superior temporal and medial frontal brain regions in patients with extra‐TLE, possibly indicating effects of different interictal epileptic discharge propagation. Hum Brain Mapp 2006. © 2006 Wiley‐Liss, Inc.

[1]  J. Duncan,et al.  Seizure characteristics, pathology, and outcome after temporal lobectomy , 1987, Neurology.

[2]  R. Erwin,et al.  Focal spike‐induced cerebral dysfunction is related to the after‐coming slow wave , 1988, Annals of neurology.

[3]  A. Wyler,et al.  Results of reoperation for failed epilepsy surgery. , 1989, Journal of neurosurgery.

[4]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[5]  J. Ebersole,et al.  Intracranial EEG Substrates of Scalp Ictal Patterns from Temporal Lobe Foci , 1997, Epilepsia.

[6]  Karl J. Friston,et al.  Human Brain Function , 1997 .

[7]  C D Binnie,et al.  Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy. , 1997, Brain : a journal of neurology.

[8]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[9]  Louis Lemieux,et al.  Identification of EEG Events in the MR Scanner: The Problem of Pulse Artifact and a Method for Its Subtraction , 1998, NeuroImage.

[10]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[11]  M R Symms,et al.  Methodology: EEG-correlated fMRI. , 2000, Advances in neurology.

[12]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[13]  H. Lüders,et al.  Presurgical evaluation of epilepsy. , 2001, Brain : a journal of neurology.

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

[15]  W T Blume,et al.  Frontal Lobe Seizure Propagation: Scalp and Subdural EEG Studies , 2001, Epilepsia.

[16]  B. Mazoyer,et al.  Cortical networks for working memory and executive functions sustain the conscious resting state in man , 2001, Brain Research Bulletin.

[17]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[18]  Hal Blumenfeld,et al.  The role of subcortical structures in human epilepsy , 2002, Epilepsy & Behavior.

[19]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  W. Penny,et al.  Random-Effects Analysis , 2002 .

[21]  Anthony B Waites,et al.  fMRI “deactivation” of the posterior cingulate during generalized spike and wave , 2003, NeuroImage.

[22]  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.

[23]  Karl J. Friston,et al.  Functional magnetic resonance imaging of human absence seizures , 2003, Annals of neurology.

[24]  P Dupont,et al.  SPECT perfusion changes during complex partial seizures in patients with hippocampal sclerosis. , 2003, Brain : a journal of neurology.

[25]  Karl J. Friston,et al.  Studying spontaneous EEG activity with fMRI , 2003, Brain Research Reviews.

[26]  C. Binnie,et al.  Cognitive impairment during epileptiform discharges: is it ever justifiable to treat the EEG? , 2003, The Lancet Neurology.

[27]  Steven Laureys,et al.  Brain function in coma, vegetative state, and related disorders , 2004, The Lancet Neurology.

[28]  Jean Gotman,et al.  EEG‐fMRI of focal epileptic spikes: Analysis with multiple haemodynamic functions and comparison with gadolinium‐enhanced MR angiograms , 2004, Human brain mapping.

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

[30]  M. Greicius,et al.  Default-Mode Activity during a Passive Sensory Task: Uncoupled from Deactivation but Impacting Activation , 2004, Journal of Cognitive Neuroscience.

[31]  Alan Connelly,et al.  Cortical lateralization during verb generation: a combined ERP and fMRI study , 2004, NeuroImage.

[32]  H Burton,et al.  Default brain functionality in blind people. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[33]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[34]  Karl J. Friston,et al.  Mixed-effects and fMRI studies , 2005, NeuroImage.

[35]  M. Steriade.  Sleep, epilepsy and thalamic reticular inhibitory neurons , 2005, Trends in Neurosciences.

[36]  J. Gotman,et al.  Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  P. Fransson.  Spontaneous low‐frequency BOLD signal fluctuations: An fMRI investigation of the resting‐state default mode of brain function hypothesis , 2005, Human brain mapping.

[38]  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.

[39]  Maria Thom,et al.  Quantitative post-mortem study of the hippocampus in chronic epilepsy: seizures do not inevitably cause neuronal loss. , 2005, Brain : a journal of neurology.

[40]  G. Jackson,et al.  Functional connectivity networks are disrupted in left temporal lobe epilepsy , 2006, Annals of neurology.

[41]  J. Gotman,et al.  Cortical and thalamic fMRI responses in partial epilepsy with focal and bilateral synchronous spikes , 2006, Clinical Neurophysiology.

[42]  Jean Gotman,et al.  Negative BOLD responses to epileptic spikes , 2006, Human brain mapping.

[43]  Tianzi Jiang,et al.  Changes in hippocampal connectivity in the early stages of Alzheimer's disease: Evidence from resting state fMRI , 2006, NeuroImage.

[44]  A. Kleinschmidt,et al.  Linking Generalized Spike‐and‐Wave Discharges and Resting State Brain Activity by Using EEG/fMRI in a Patient with Absence Seizures , 2006, Epilepsia.

[45]  Karl J. Friston,et al.  EEG–fMRI of idiopathic and secondarily generalized epilepsies , 2006, NeuroImage.

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

[47]  Karl J. Friston,et al.  Hemodynamic correlates of epileptiform discharges: An EEG-fMRI study of 63 patients with focal epilepsy , 2006, Brain Research.

[48]  W. D. Penny,et al.  Random-Effects Analysis , 2002 .