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The Journal of Neuroscience, September 3, 2008, 28(36):9066-9081; doi:10.1523/JNEUROSCI.2014-08.2008

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Neurobiology of Disease
Remote Effects of Focal Hippocampal Seizures on the Rat Neocortex

Dario J. Englot,¹ Asht M. Mishra,¹ Peter K. Mansuripur,¹ Peter Herman,^2,6,7 Fahmeed Hyder,^2,3,6,7 and Hal Blumenfeld^1,4,5,6

Departments of ¹Neurology, ²Diagnostic Radiology, ³Biomedical Engineering, ⁴Neurobiology, and ⁵Neurosurgery, ⁶Program for Quantitative Neuroscience with Magnetic Resonance (QNMR), and ⁷Magnetic Resonance Research Center (MRRC), Yale University School of Medicine, New Haven, Connecticut 06520

Correspondence should be addressed to Dr. Hal Blumenfeld, Department of Neurology, Yale University, 333 Cedar Street, New Haven, CT 06520. Email: hal.blumenfeld{at}yale.edu

Seizures have both local and remote effects on nervous system function. Whereas propagated seizures are known to disrupt cerebral activity, little work has been done on remote network effects of seizures that do not propagate. Human focal temporal lobe seizures demonstrate remote changes including slow waves on electroencephalography (EEG) and decreased cerebral blood flow (CBF) in the neocortex. Ictal neocortical slow waves have been interpreted as seizure propagation; however, we hypothesize that they reflect a depressed cortical state resembling sleep or coma. To investigate this hypothesis, we performed multimodal studies of partial and secondarily generalized limbic seizures in rats. Video/EEG monitoring of spontaneous seizures revealed slow waves in the frontal cortex during behaviorally mild partial seizures, contrasted with fast polyspike activity during convulsive generalized seizures. Seizures induced by hippocampal stimulation produced a similar pattern, and were used to perform functional magnetic resonance imaging weighted for blood oxygenation and blood volume, demonstrating increased signals in hippocampus, thalamus and septum, but decreases in orbitofrontal, cingulate, and retrosplenial cortex during partial seizures, and increases in all of these regions during propagated seizures. Combining these results with neuronal recordings and CBF measurements, we related neocortical slow waves to reduced neuronal activity and cerebral metabolism during partial seizures, but found increased neuronal activity and metabolism during propagated seizures. These findings suggest that ictal neocortical slow waves represent an altered cortical state of depressed function, not propagated seizure activity. This remote effect of partial seizures may cause impaired cerebral functions, including loss of consciousness.

Key words: consciousness; BOLD decreases; cortex; fMRI; slow oscillations; temporal lobe epilepsy

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Received May 1, 2008; revised July 1, 2008; accepted July 31, 2008.

Correspondence should be addressed to Dr. Hal Blumenfeld, Department of Neurology, Yale University, 333 Cedar Street, New Haven, CT 06520. Email: hal.blumenfeld{at}yale.edu

This article has been cited by other articles:

				D. J. Englot, B. Modi, A. M. Mishra, M. DeSalvo, F. Hyder, and H. Blumenfeld Cortical Deactivation Induced by Subcortical Network Dysfunction in Limbic Seizures J. Neurosci., October 14, 2009; 29(41): 13006 - 13018. [Abstract] [Full Text] [PDF]

				H. Blumenfeld, G. I. Varghese, M.J. Purcaro, J.E. Motelow, M. Enev, K. A. McNally, A.R. Levin, L. J. Hirsch, R. Tikofsky, I. G. Zubal, et al. Cortical and subcortical networks in human secondarily generalized tonic-clonic seizures Brain, April 1, 2009; (2009) awp028v1. [Abstract] [Full Text] [PDF]

				B. G. Sanganahalli, P. Herman, H. Blumenfeld, and F. Hyder Oxidative Neuroenergetics in Event-Related Paradigms J. Neurosci., February 11, 2009; 29(6): 1707 - 1718. [Abstract] [Full Text] [PDF]

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