Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms

A better understanding of interstructure relationship sustaining drug‐resistant epileptogenic networks is crucial for surgical perspective and to better understand the consequences of epileptic processes on cognitive functions. We used resting‐state fMRI to study basal functional connectivity within temporal lobes in medial temporal lobe epilepsy (MTLE) during interictal period. Two hundred consecutive single‐shot GE‐EPI acquisitions were acquired in 37 right‐handed subjects (26 controls, eight patients presenting with left and three patients with right MTLE). For each hemisphere, normalized correlation coefficients were computed between pairs of time‐course signals extracted from five regions involved in MTLE epileptogenic networks (Brodmann area 38, amygdala, entorhinal cortex (EC), anterior hippocampus (AntHip), and posterior hippocampus (PostHip)). In controls, an asymmetry was present with a global higher connectivity in the left temporal lobe. Relative to controls, the left MTLE group showed disruption of the left EC‐AntHip link, and a trend of decreased connectivity of the left AntHip‐PostHip link. In contrast, a trend of increased connectivity of the right AntHip‐PostHip link was observed and was positively correlated to memory performance. At the individual level, seven out of the eight left MTLE patients showed decreased or disrupted functional connectivity. In this group, four patients with left TLE showed increased basal functional connectivity restricted to the right temporal lobe spared by seizures onset. A reverse pattern was observed at the individual level for patients with right TLE. This is the first demonstration of decreased basal functional connectivity within epileptogenic networks with concomitant contralateral increased connectivity possibly reflecting compensatory mechanisms. Hum Brain Mapp 2009. © 2008 Wiley‐Liss, Inc.

[1]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

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

[3]  Richard S. J. Frackowiak,et al.  Learning to find your way: a role for the human hippocampal formation , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[4]  M. Lowe,et al.  Functional Connectivity in Single and Multislice Echoplanar Imaging Using Resting-State Fluctuations , 1998, NeuroImage.

[5]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[6]  C. Gross,et al.  Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. , 1998, Journal of neurophysiology.

[7]  N. Fountain,et al.  Functional anatomy of limbic epilepsy: a proposal for central synchronization of a diffusely hyperexcitable network , 1998, Epilepsy Research.

[8]  D. Amaral,et al.  Entorhinal cortex of the rat: Organization of intrinsic connections , 1998, The Journal of comparative neurology.

[9]  Charles L. Wilson,et al.  High‐frequency oscillations in human brain , 1999, Hippocampus.

[10]  John A. King,et al.  Memory for events and their spatial context: models and experiments. , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[11]  J. Bellanger,et al.  Neural networks involving the medial temporal structures in temporal lobe epilepsy , 2001, Clinical Neurophysiology.

[12]  M. Mishkin,et al.  The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. , 2001, Brain : a journal of neurology.

[13]  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.

[14]  Fabrice Bartolomei,et al.  Metabolic and Electrophysiological Alterations in Subtypes of Temporal Lobe Epilepsy: A Combined Proton Magnetic Resonance Spectroscopic Imaging and Depth Electrodes Study , 2002, Epilepsia.

[15]  J. Bellanger,et al.  Epileptic fast intracerebral EEG activity: evidence for spatial decorrelation at seizure onset. , 2003, Brain : a journal of neurology.

[16]  J. Gray,et al.  Allocentric spatial memory activation of the hippocampal formation measured with fMRI. , 2004, Neuropsychology.

[17]  R. Kahn,et al.  Lateralization of amygdala activation: a systematic review of functional neuroimaging studies , 2004, Brain Research Reviews.

[18]  Fabrice Bartolomei,et al.  Semiologic and Electrophysiologic Correlations in Temporal Lobe Seizure Subtypes , 2004, Epilepsia.

[19]  Maija Pihlajamäki,et al.  Visual presentation of novel objects and new spatial arrangements of objects differentially activates the medial temporal lobe subareas in humans , 2004, The European journal of neuroscience.

[20]  F. Wendling,et al.  Temporal lobe epilepsy , 2019, Radiopaedia.org.

[21]  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.

[22]  Christine Delmaire,et al.  Productive and perceptive language reorganization in temporal lobe epilepsy , 2005, NeuroImage.

[23]  S. Zeki,et al.  The chronoarchitecture of the cerebral cortex , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  Jean Régis,et al.  1H-MRS imaging in intractable frontal lobe epilepsies characterized by depth electrode recording , 2005, NeuroImage.

[25]  R. Gur,et al.  Leftward asymmetry in relative fiber density of the arcuate fasciculus , 2005, Neuroreport.

[26]  G. Jackson,et al.  Effect of prior cognitive state on resting state networks measured with functional connectivity , 2005, Human brain mapping.

[27]  Ravi S. Menon,et al.  Novelty responses to relational and non‐relational information in the hippocampus and the parahippocampal region: A comparison based on event‐related fMRI , 2005, Hippocampus.

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

[29]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

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

[31]  Christian Schwarzbauer,et al.  Perirhinal cortex activity during visual object discrimination: An event-related fMRI study , 2006, NeuroImage.

[32]  Benjamin J. Shannon,et al.  Coherent spontaneous activity identifies a hippocampal-parietal memory network. , 2006, Journal of neurophysiology.

[33]  J. Régis,et al.  The role of corticothalamic coupling in human temporal lobe epilepsy. , 2006, Brain : a journal of neurology.

[34]  Morris Moscovitch,et al.  Consequences of hippocampal damage across the autobiographical memory network in left temporal lobe epilepsy. , 2007, Brain : a journal of neurology.

[35]  John S Duncan,et al.  Reorganization of Verbal and Nonverbal Memory in Temporal Lobe Epilepsy Due to Unilateral Hippocampal Sclerosis , 2007, Epilepsia.

[36]  R. Goodman,et al.  Cortical abnormalities in epilepsy revealed by local EEG synchrony , 2007, NeuroImage.

[37]  M. Walker,et al.  Noncanonical spike‐related BOLD responses in focal epilepsy , 2007, Human brain mapping.

[38]  J. Régis,et al.  Enhanced EEG functional connectivity in mesial temporal lobe epilepsy , 2008, Epilepsy Research.