Vascular steal model of human temporal lobe epileptogenicity: the relationship between electrocorticographic interhemispheric propagation time and cerebral blood flow

doi:10.1054/mehy.1999.0937

Medical Hypotheses

Volume 54, Issue 5, May 2000, Pages 717-720

https://doi.org/10.1054/mehy.1999.0937 Get rights and content

Abstract

Human temporal lobe epileptogenicity (i.e. seizure frequency) depends on epileptic and non-epileptic cerebral blood flow (CBF). Increasing non-epileptic cortical CBF is associated with reduction in epileptic cortical CBF. Seizure frequency increases logarithmically with non-epileptic cortical CBF increase and epileptic cortical CBF reduction. A model of human temporal lobe epileptogenicity is derived from the mathematical equivalence to the logarithmic function of seizure frequency of (a) epileptic and non-epileptic CBF differential and (b) electrocorticographic (ECoG) interhemispheric propagation time (IHPT). The vascular steal model of human temporal lobe epileptogenicity suggests that a small CBF redistribution from non-epileptic to epileptic cortex should produce substantial reduction in temporal lobe seizure frequency in association with prolongation of IHPT. The equivalence of these CBF and ECoG parameters to the logarithmic function of seizure frequency suggests that the interhemispheric temporal lobe perfusion gradient and ECoG propagation time may be involved in the fundamental perturbation responsible for human temporal lobe epileptogenicity.

References (21)

NIH Consens Dev Conf Consens Statement
(1990)
M. LaManna et al.
Initial experience with SPECT imaging of the brain using I-123 p-iodoamphetamine in focal epilepsy
Clin Nucl Med
(1989)
H. Stefan et al.
Regional cerebral blood flow during focal seizures of temporal and frontocentral onset
Ann Neurol
(1990)
M.E. Weinand et al.
Cerebral blood flow and temporal lobe epileptogenicity
J Neurosurg
(1997)
M.E. Weinand et al.
Temporal lobe ischemia and epileptogenicity: Long-term cortical cerebral blood flow analysis of sequential seizures
Surgical Forum
(1995)
U.W. Baluenstein et al.
¹³³Xenon inhalation method: Analysis of reproducibility: Some of its physiological implications
Stroke
(1977)
A. Dahl et al.
A comparison of transcranial doppler and cerebral blood flow studies to assess cerebral vasoreactivity
Stroke
(1992)
W. Penfield
Remarks on incomplete hypotheses for the control of cerebral circulation
J Neurosurg
(1971)
W. Penfield
The evidence for a cerebral vascular mechanism in epilepsy
Ann Int Med
(1933)
S. Bernardi et al.
An interictal study of partial epilepsy using positron emission tomography and the oxygen-15 inhalation technique
J Neurol Neurosurg Psychiatry
(1983)

There are more references available in the full text version of this article.

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Regular ArticleVascular steal model of human temporal lobe epileptogenicity: the relationship between electrocorticographic interhemispheric propagation time and cerebral blood flow

Abstract

NIH Consens Dev Conf Consens Statement

Initial experience with SPECT imaging of the brain using I-123 p-iodoamphetamine in focal epilepsy

Clin Nucl Med

Regional cerebral blood flow during focal seizures of temporal and frontocentral onset

Ann Neurol

Cerebral blood flow and temporal lobe epileptogenicity

J Neurosurg

Temporal lobe ischemia and epileptogenicity: Long-term cortical cerebral blood flow analysis of sequential seizures

Surgical Forum

133Xenon inhalation method: Analysis of reproducibility: Some of its physiological implications

Stroke

A comparison of transcranial doppler and cerebral blood flow studies to assess cerebral vasoreactivity

Stroke

Remarks on incomplete hypotheses for the control of cerebral circulation

J Neurosurg

The evidence for a cerebral vascular mechanism in epilepsy

Ann Int Med

An interictal study of partial epilepsy using positron emission tomography and the oxygen-15 inhalation technique

J Neurol Neurosurg Psychiatry

Regular Article
Vascular steal model of human temporal lobe epileptogenicity: the relationship between electrocorticographic interhemispheric propagation time and cerebral blood flow

¹³³Xenon inhalation method: Analysis of reproducibility: Some of its physiological implications