Wilder Penfield and the vascular hypothesis of focal epilepsy

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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.

ABBREVIATIONS CBF = cerebral blood flow; MNI = Montreal Neurological Institute.
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Contributor Notes

Correspondence Richard Leblanc: Montreal Neurological Institute, Montreal, QC, Canada. richard.leblanc@mcgill.ca.INCLUDE WHEN CITING Published online January 4, 2019; DOI: 10.3171/2018.8.JNS181990.Disclosures The author reports no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.
  • 1

    Alexander W: The Treatment of Epilepsy. Edinburgh: YJ Pentland1889

  • 2

    Bernard C: Influence du grand sympathique sur la sensibilité et sur la calorification. C R Memoires Soc Biol 3:1631641852

  • 3

    Bernard C: Leçons sur la physiologie et la pathologie du système nerveux. Paris: JB Bailliere et Fils1858Vol 2 pp 491495

    • Export Citation
  • 4

    Bernard C: Recherches expérimentales sur les nerfs vasculaires et calorifiques du grand sympathique. C R Acad Sci 55:228–2363053121862

    • Search Google Scholar
    • Export Citation
  • 5

    Bernard C: Sur les effets de la section de la portion encéphalique du grand sympathique. C R Memoires Soc Biol 4:1681701853

  • 6

    Choróbski J: Part 1: A Vasodilator Nervous Pathway to the Cerebral Vessels from the Central Nervous System. Part 2: On the Occurrence of Afferent Nerve Fibers in the Internal Carotid Plexus [master’s thesis]. Montreal: McGill University1931/1932

    • Search Google Scholar
    • Export Citation
  • 7

    Choróbski JPenfield W: Cerebral vasodilator nerves and their pathway from the medulla oblongata with observations on the pial and intracerebral vascular plexus. Arch Neurol Psychiatry 28:125712891932

    • Search Google Scholar
    • Export Citation
  • 8

    del Río-Hortega PPenfield WG: Cerebral cicatrix: the reaction of neuroglia and microglia to brain wounds. Bull Johns Hopkins Hosp 41:2783031927

    • Search Google Scholar
    • Export Citation
  • 9

    Echeverria MG: On Epilepsy. New York: William Wood & Company1870

  • 10

    Echlin FA: Cerebral Ischemia and Its Relationship to Epilepsy [master’s thesis]. Montreal: McGill University1939

  • 11

    Feindel WYamamoto YL: Luxury-perfusion syndrome. Lancet 1:48491967

  • 12

    Feindel WYamamoto YLHodge CP: Red cerebral veins as an index of cerebral steal. Presented at the International Symposium on ‘CSF and CBF’, Lund and Copenhagen, May 9–11, 1968. Scand J Lab Clin Invest 21 (Suppl 102):X:C 1968

    • Search Google Scholar
    • Export Citation
  • 13

    Foerster OPenfield W: The structural basis of traumatic epilepsy and results of radical operation. Brain 53:991191930

  • 14

    Forbes SH: The cerebral circulation. 1. Observation and measurement of pial vessels. Arch Neurol Psychiatry 19:7517611928

  • 15

    Gage EL: The Effects of Vasomotor Nerve Section on Experimental Epilepsy [master’s thesis]. Montreal: McGill University1931

  • 16

    Gibbs FA: Cerebral blood flow preceding and accompanying experimental convulsions. Arch Neurol Psychiatry 30:100310101933

  • 17

    Gibbs FA: A thermoelectric blood flow recorder in the form of a needle. Exp Biol Med 31:1411933

  • 18

    Gibbs FALennox WGGibbs EL: Cerebral blood flow preceding and accompanying epileptic seizures in man. Arch Neurol Psychiatry 32:2572721934

    • Search Google Scholar
    • Export Citation
  • 19

    Jackson H: Unilateral epileptiform seizures beginning by a disagreeable smell. Medical Times and Gazette. August 13 1864; 168

  • 20

    Jackson JH: On the anatomical, physiological, and pathological investigation of epilepsies. West Riding Lunatic Asylum Med Rep 3:3153391873

    • Search Google Scholar
    • Export Citation
  • 21

    Jackson JH: A study of convulsions. Trans Saint Andrews Graduate Assoc 3:1621941870

  • 22

    Kussmaul ATenner A: On the Nature and Origin of Epileptiform Convulsions Caused by Profuse Bleeding and Also Those of True Epilepsy. Bonner E trans. London: New Sydenham Society1859

    • Search Google Scholar
    • Export Citation
  • 23

    Leblanc RLittle JR: Hemodynamics of arteriovenous malformations. Clin Neurosurg 36:2993171990

  • 24

    Leblanc RMeyer E: Functional PET scanning in the assessment of cerebral arteriovenous malformations. Case report. J Neurosurg 73:6156191990

    • Search Google Scholar
    • Export Citation
  • 25

    Norcross NC: Studies in Cerebral Circulation [master’s thesis]. Montreal: McGill University1936

  • 26

    Penfield W: Meningocerebral adhesions: a historical study of the results of cerebral incision and cranioplasty. Surg Gynecol Obstet 39:8038101924

    • Search Google Scholar
    • Export Citation
  • 27

    Penfield W: The circulation of the epileptic brain. Res Publ Assoc Nerv Ment Dis 18:6056371937

  • 28

    Penfield W: Epilepsy and surgical therapy. Arch Neurol Psychiatry 36:4494841936

  • 29

    Penfield W: The evidence for a cerebral vascular mechanism in epilepsy. Ann Intern Med 7:3033101933

  • 30

    Penfield W: Intracerebral vascular nerves. Arch Neurol Psychiatry 27:30441932

  • 31

    Penfield W: The mechanism of cicatricial contraction in the brain. Brain 50:4995171927

  • 32

    Penfield W: Obituary: Sir Percy Sargent, 1873–1933. Arch Neurol Psychiatry 30:4134141933

  • 33

    Penfield WBuckley RC: Punctures of the brain: the factors concerned in gliosis and in cicatricial contraction. Arch Neurol Psychiatry 20:1131928

    • Search Google Scholar
    • Export Citation
  • 34

    Penfield Wvon Santha KCipriani A: Cerebral blood flow during induced epileptiform seizures in animals and man. J Neurophysiol 2:2572671939

    • Search Google Scholar
    • Export Citation
  • 35

    Popper KR: The Logic of Scientific Discovery. New York: Harper Torchbooks1968

  • 36

    Reynolds JR: Epilepsy: Its Symptoms Treatment and Relation to Other Chronic Convulsive Diseases. London: John Churchill1861

  • 37

    Sargent P: Some observations on epilepsy: presidential address. Brain 44:3123281921

  • 38

    Smith RRRobertson JT: Subarachnoid Hemorrhage and Cerebrovascular Spasm. Springfield, IL: Charles C. Thomas1975

  • 39

    Spielmeyer W: The anatomic substratum of the convulsive state. Arch Neurol Psychiatry 23:8698751930

  • 40

    Temkin O: The reflex theory in: The Falling Sickness: A History of Epilepsy from the Greeks to the Beginnings of Modern Neurology. Baltimore: Johns Hopkins Press1945 pp 267274

    • Search Google Scholar
    • Export Citation
  • 41

    von Santha KCipriani A: Focal alterations in subcortical circulation resulting from stimulation of the cerebra1 cortex. Res Publ Assoc Nerv Ment Dis 18:3463621938

    • Search Google Scholar
    • Export Citation


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