Wilder Penfield and the vascular hypothesis of focal epilepsy.

The vascular hypothesis held that posttraumatic epilepsy results from reflex vasoconstriction of cortical arteries around a cerebral scar. Penfield’s initial support and eventual refutation of the vascular hypothesis is the subject of this paper, which is based on a review of his clinical charts, operative and electrocorticographic reports, and brain maps held in the Montreal Neurological Institute archives. Penfield and his collaborators discovered that posttraumatic cortical scars are composed of astro-glial fibers, collagen fibrils, and a neo-vascular plexus that anastomoses with the surrounding cortical arteries. He hypothesized that the contracting scar applied traction to these arteries, which caused epileptic seizures. This was supported by his observations that cortical arteries constrict during an epileptic seizure. Penfield’s subsequent investigations led to the discovery that parasympathetic nerves innervate the intracranial arteries, that experimental vasospasm can produce cortical infarction, and that cerebral blood flow (CBF) is coupled to cerebral metabolism. In fact, Penfield found that CBF increases in the epileptogenic zone around a cortical scar, contrary to what the hypothesis had predicted. Despite this, Penfield’s investigations shed new light on the dynamics of the cerebral circulation that were not fully understood until decades later.