BOLD signal changes preceding negative responses in EEG‐fMRI in patients with focal epilepsy

Purpose:  In simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI), increased neuronal activity from epileptiform spikes commonly elicits positive blood oxygenation level–dependent (BOLD) responses. Negative responses are also occasionally seen and have not been explained. Recent studies describe BOLD signal changes before focal EEG spikes. We aimed to systematically study if the undershoot of a preceding positive response might explain the negative BOLD seen in the focus.

[1]  J. Gotman,et al.  Quality of EEG in simultaneous EEG-fMRI for epilepsy , 2003, Clinical Neurophysiology.

[2]  M. D’Esposito,et al.  The variability of human BOLD hemodynamic responses , 1998, NeuroImage.

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

[4]  Reinhard Grebe,et al.  NIRS‐measured oxy‐ and deoxyhemoglobin changes associated with EEG spike‐and‐wave discharges in children , 2008, Epilepsia.

[5]  Jean Gotman,et al.  Using patient-specific hemodynamic response functions in combined EEG-fMRI studies in epilepsy , 2003, NeuroImage.

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

[7]  Jean Gotman,et al.  Analysis of the EEG–fMRI response to prolonged bursts of interictal epileptiform activity , 2005, NeuroImage.

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

[9]  Karl J. Friston,et al.  Event‐related f MRI , 1997, Human brain mapping.

[10]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[11]  H. Laufs,et al.  Electroencephalography/functional MRI in human epilepsy: what it currently can and cannot do , 2007, Current opinion in neurology.

[12]  Mark D'Esposito,et al.  Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses , 2004, NeuroImage.

[13]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[14]  J Gotman,et al.  Intrinsic epileptogenicity in polymicrogyric cortex suggested by EEG-fMRI BOLD responses , 2005, Neurology.

[15]  Tapio Seppänen,et al.  BOLD signal increase preceeds EEG spike activity—a dynamic penicillin induced focal epilepsy in deep anesthesia , 2005, NeuroImage.

[16]  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.

[17]  J. Gotman,et al.  Combining EEG and fMRI: A multimodal tool for epilepsy research , 2006, Journal of magnetic resonance imaging : JMRI.

[18]  J. Gotman Epileptic networks studied with EEG‐fMRI , 2008, Epilepsia.

[19]  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.

[20]  J. Ebersole,et al.  Intracranial EEG Substrates of Scalp EEG Interictal Spikes , 2005, Epilepsia.

[21]  A. Shmuel,et al.  Sustained Negative BOLD, Blood Flow and Oxygen Consumption Response and Its Coupling to the Positive Response in the Human Brain , 2002, Neuron.

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

[23]  G. Glover Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[24]  M Wj DANIEL G. BRINTON. , 1899 .

[25]  J. Gotman,et al.  fMRI activation during spike and wave discharges in idiopathic generalized epilepsy. , 2004, Brain : a journal of neurology.

[26]  Dae-Shik Kim,et al.  Origin of Negative Blood Oxygenation Level—Dependent fMRI Signals , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[27]  Joshua E. Motelow,et al.  Negative BOLD with large increases in neuronal activity. , 2008, Cerebral cortex.

[28]  Silvia Mangia,et al.  Metabolic and Hemodynamic Events after Changes in Neuronal Activity: Current Hypotheses, Theoretical Predictions and in vivo NMR Experimental Findings , 2009, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[29]  Yingli Lu,et al.  BOLD changes occur prior to epileptic spikes seen on scalp EEG , 2007, NeuroImage.

[30]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[31]  J. Gotman,et al.  fMRI Activation in Continuous and Spike‐triggered EEG–fMRI Studies of Epileptic Spikes , 2003, Epilepsia.

[32]  C. A. Marsan,et al.  Cellular Mechanisms in Experimental Epileptic Seizures , 1964, Science.

[33]  Alan C. Evans,et al.  A General Statistical Analysis for fMRI Data , 2000, NeuroImage.

[34]  Jean Gotman,et al.  The BOLD Response to Interictal Epileptiform Discharges , 2002, NeuroImage.

[35]  Kaoru Sakatani,et al.  Comparison of blood-oxygen-level-dependent functional magnetic resonance imaging and near-infrared spectroscopy recording during functional brain activation in patients with stroke and brain tumors. , 2007, Journal of biomedical optics.

[36]  M R Symms,et al.  Spatio-temporal imaging of focal interictal epileptiform activity using EEG-triggered functional MRI. , 2001, Epileptic disorders : international epilepsy journal with videotape.

[37]  Jean Gotman,et al.  Hemodynamic Responses to Interictal Epileptiform Discharges in Children with Symptomatic Epilepsy , 2007, Epilepsia.

[38]  Jane Neumann,et al.  Variability of the BOLD response over time: An examination of within-session differences , 2006, NeuroImage.

[39]  Praveen Kulkarni,et al.  Imaging the Neural Substrates Involved in the Genesis of Pentylenetetrazol‐induced Seizures , 2006, Epilepsia.

[40]  Reinhard Grebe,et al.  NIRS‐measured oxy‐ and deoxyhemoglobin changes associated with EEG spike‐and‐wave discharges in a genetic model of absence epilepsy: The GAERS , 2010, Epilepsia.

[41]  Robert G. Shulman,et al.  A BOLD search for baseline , 2007, NeuroImage.

[42]  Oliver Granert,et al.  Changes in activity of striato–thalamo–cortical network precede generalized spike wave discharges , 2008, NeuroImage.

[43]  Pierre J Magistretti,et al.  GABA uptake into astrocytes is not associated with significant metabolic cost: Implications for brain imaging of inhibitory transmission , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  A. Kleinschmidt,et al.  Temporal lobe interictal epileptic discharges affect cerebral activity in “default mode” brain regions , 2006, Human brain mapping.

[45]  Jean Gotman,et al.  Hemodynamic changes preceding the interictal EEG spike in patients with focal epilepsy investigated using simultaneous EEG-fMRI , 2009, NeuroImage.

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