Positive and negative network correlations in temporal lobe epilepsy.

Temporal lobe seizures are accompanied by complex behavioral phenomena including loss of consciousness, dystonic movements and neuroendocrine changes. These phenomena may arise from extended neural networks beyond the temporal lobe. To investigate this, we imaged cerebral blood flow (CBF) changes during human temporal lobe seizures with single photon emission computed tomography (SPECT) while performing continuous video/EEG monitoring. We found that temporal lobe seizures associated with loss of consciousness produced CBF increases in the temporal lobe, followed by increases in bilateral midline subcortical structures. These changes were accompanied by marked bilateral CBF decreases in the frontal and parietal association cortex. In contrast, temporal lobe seizures in which consciousness was spared were not accompanied by these widespread CBF changes. The CBF decreases in frontal and parietal association cortex were strongly correlated with increases in midline structures such as the mediodorsal thalamus. These results suggest that impaired consciousness in temporal lobe seizures may result from focal abnormal activity in temporal and subcortical networks linked to widespread impaired function of the association cortex.

[1]  J. Bauer Interactions Between Hormones and Epilepsy in Female Patients , 2001, Epilepsia.

[2]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[3]  Jerome Engel,et al.  Role of the Frontal Lobes in the Propagation of Mesial Temporal Lobe Seizures , 1991, Epilepsia.

[4]  D. Chalmers The conscious mind: in search of a fundamental theory , 1996 .

[5]  A. Handforth,et al.  Functional [14C]2-deoxyglucose mapping of progressive states of status epilepticus induced by amygdala stimulation in rat , 1988, Brain Research.

[6]  Hal Blumenfeld,et al.  Why do Seizures Cause Loss of Consciousness? , 2003, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[7]  D. Spencer,et al.  Ictal neocortical slowing in temporal lobe epilepsy , 2004, Neurology.

[8]  K. Gale,et al.  Mediodorsal Thalamus Plays a Critical Role in the Development of Limbic Motor Seizures , 1998, The Journal of Neuroscience.

[9]  E. Lothman,et al.  Self‐sustaining limbic status epilepticus. , 1991, Neurology.

[10]  E. Bertram,et al.  Interictal and postictal alterations of pulsatile secretions of luteinizing hormone in temporal lobe epilepsy in men , 2002, Annals of neurology.

[11]  K. Heo,et al.  Ictal Automatisms with Preserved Responsiveness in a Patient with Left Mesial Temporal Lobe Epilepsy , 2001, Epilepsia.

[12]  C. Jack,et al.  Subtraction ictal SPECT co‐registered to MRI improves clinical usefulness of SPECT in localizing the surgical seizure focus , 1998, Neurology.

[13]  Geraint Rees,et al.  What can functional imaging reveal about the role of attention in visual awareness? , 2001, Neuropsychologia.

[14]  Eileen O. Smith,et al.  Difference images calculated from ictal and interictal technetium-99m-HMPAO SPECT scans of epilepsy. , 1995, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[15]  Ivanei E. Bramati,et al.  The Neural Correlates of Moral Sensitivity: A Functional Magnetic Resonance Imaging Investigation of Basic and Moral Emotions , 2002, The Journal of Neuroscience.

[16]  B. Tabachnick,et al.  Using Multivariate Statistics , 1983 .

[17]  Theodore H. Schwartz,et al.  In vivo optical mapping of epileptic foci and surround inhibition in ferret cerebral cortex , 2001, Nature Medicine.

[18]  R. M. Cooper,et al.  [14C]2‐Deoxyglucose Autoradiographic Technique Provides a Metabolic Signature of Cobalt‐Induced Focal Epileptogenesis , 1994, Epilepsia.

[19]  R. Mattson,et al.  Characteristics of medial temporal lobe epilepsy: II. Interictal and ictal scalp electroencephalography, neuropsychological testing, neuroimaging, surgical results, and pathology , 1993, Annals of neurology.

[20]  G. Hagemann,et al.  Coupling of cortical and thalamic metabolism in experimentally induced visual and somatosensory focal epilepsy , 1997, Epilepsy Research.

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

[22]  J. Gray Consciousness on the scientific agenda , 1992, Nature.

[23]  W. Marks,et al.  Semiology of Temporal Lobe Seizures: Value in Lateralizing the Seizure Focus , 1998, Epilepsia.

[24]  D. Kuhl,et al.  Local cerebral metabolism during partial seizures , 1983, Neurology.

[25]  B. Gulyás,et al.  Activation by Attention of the Human Reticular Formation and Thalamic Intralaminar Nuclei , 1996, Science.

[26]  C. Studholme,et al.  Estimating Tissue Deformation between Functional Images Induced by Intracranial Electrode Implantation Using Anatomical MRI , 2001, NeuroImage.

[27]  Tae Joo Jeon,et al.  Evaluation of ictal brain SPET using statistical parametric mapping in temporal lobe epilepsy , 2000, European Journal of Nuclear Medicine.

[28]  M E Phelps,et al.  Patterns of human local cerebral glucose metabolism during epileptic seizures. , 1982, Science.

[29]  Jason Freeman,et al.  Selective frontal, parietal, and temporal networks in generalized seizures , 2003, NeuroImage.

[30]  Karl J. Friston,et al.  Statistical parametric mapping in functional neuroimaging: beyond PET and fMRI activation studies. , 1998, European journal of nuclear medicine.

[31]  Jacqueline A. French,et al.  Characteristics of medial temporal lobe epilepsy , 1993 .

[32]  O. Witte,et al.  Thalamocortical circuits causing remote hypometabolism during focal interictal epilepsy , 1998, Epilepsy Research.

[33]  R. C. Collins Use of cortical circuits during focal penicillin seizures: An autoradiographic study with [14C]deoxyglucose , 1978, Brain Research.

[34]  Andersen Ar,et al.  99mTc-D,L-hexamethylene-propyleneamine oxime (99mTc-HMPAO): basic kinetic studies of a tracer of cerebral blood flow. , 1989 .

[35]  A. Szűcs,et al.  Automatisms with preserved responsiveness and ictal aphasia: contradictory lateralising signs during a dominant temporal lobe seizure , 2003, Seizure.

[36]  Geraint Rees,et al.  Neural correlates of consciousness in humans , 2002, Nature Reviews Neuroscience.

[37]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[38]  VanLandingham Ke,et al.  Self-sustaining limbic status epilepticus. I. Acute and chronic cerebral metabolic studies: limbic hypermetabolism and neocortical hypometabolism. , 1991 .

[39]  D C Reutens,et al.  Dystonia, clinical lateralization, and regional blood flow changes in temporal lobe seizures , 1992, Neurology.

[40]  D. Prince,et al.  Control mechanisms in cortical epileptogenic foci. "Surround" inhibition. , 1967, Archives of neurology.

[41]  E. Bertram,et al.  Midline Thalamic Region: Widespread Excitatory Input to the Entorhinal Cortex and Amygdala , 2002, The Journal of Neuroscience.

[42]  Colin Studholme,et al.  Comparison of Statistical Parametric Mapping and SPECT Difference Imaging in Patients with Temporal Lobe Epilepsy , 2002, Epilepsia.

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

[44]  Jerome Engel,et al.  Outcome with respect to epileptic seizures. , 1993 .

[45]  G. Rees,et al.  Neural correlates of perceptual rivalry in the human brain. , 1998, Science.

[46]  K. Meador,et al.  Pathophysiology of altered consciousness during seizures: Subtraction SPECT study , 2002, Neurology.

[47]  C. Elger,et al.  Inhibitory effects of mesial temporal partial seizures onto frontal neocortical structures. , 1998, Acta neurologica Belgica.

[48]  Y Mayanagi,et al.  Mesial Temporal Lobe Epilepsy: Clinical Features and Seizure Mechanism , 1996, Epilepsia.

[49]  A. Rabinowicz,et al.  Changes in Regional Cerebral Blood Flow Beyond the Temporal Lobe in Unilateral Temporal Lobe Epilepsy , 1997, Epilepsia.

[50]  I G Zubal,et al.  Sensitivity and specificity of quantitative difference SPECT analysis in seizure localization. , 1999, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[51]  D. Seo,et al.  Ictal hyperperfusion of cerebellum and basal ganglia in temporal lobe epilepsy: SPECT subtraction with MRI coregistration. , 2001, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.