Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-19T12:27:35.934Z Has data issue: false hasContentIssue false

Psychiatric consequences of temporal lobectomy for intractable seizures: a 20–30-year follow-up of 14 cases

Published online by Cambridge University Press:  09 July 2009

Janice R. Stevens
Affiliation:
National Institute of Mental Health, Saint Elizabeth's Hospital, Washington, DC, Oregon Health Sciences University, Portland, Oregon, USA

Synopsis

Between 1958 and 1968, 14 patients from the epilepsy clinic at the University of Oregon Hospitals and Clinics with a diagnosis of temporal lobe epilepsy (TLE) had a temporal lobectomy for medically intractable seizures. Nine of the 14 patients operated on remained seizure-free over the 20–30-year period of follow-up. Between 6 months and one year following temporal lobectomy, two women, previously healthy from a psychiatric standpoint, developed psychoses, and the previous psychiatric problems of four other patients worsened. Two patients, one with incapacitating paranoid personality disorder and the other with explosive rage attacks preoperatively, had marked improvement in their psychiatric status following temporal lobectomy. The remaining six patients, all psychiatrically healthy prior to surgery, have had no change in psychiatric status following surgery. Development of psychosis or deterioration in psychiatric status after surgery was more common in patients with later age of onset, unreality or déjà vu rather than epigastric aura, pre-operative evidence of bilateral brain damage, and persistence of EEG or clinical seizure activity. Development of a chronic psychosis in psychiatrically healthy individuals many months after temporal lobectomy, even when seizures are arrested or ameliorated, suggests that anomalous synaptic regeneration may follow the surgery in these cases. Careful analysis of histories and outcomes may contribute to better understanding of the pathophysiology and anatomical substrates of psychoses.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 1990

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bailey, P., Green, J. R., Amador, L. & Gibbs, F. A. (1953). Treatment of psychomotor states by anterior temporal lobectomy, a report of progress. Research Publications in Nervous and Mental Disease 31, 341346.Google Scholar
Bartlet, J. E. A. (1957). Chronic psychosis following epilepsy. American Journal of Psychiatry 114, 338343.CrossRefGoogle ScholarPubMed
Ben-Ari, Y., Lagowska, Y., Gal La Salle, G., Tremblay, E., Ottersen, O. P. & Naquet, R. (1978). Diazepam pretreatment reduces distant hippocampal damage induced by intra-amygdaloid injections of kainic acid. European Journal of Pharmacology 52, 419420.CrossRefGoogle ScholarPubMed
Bogerts, B., Meertz, E. & Schofeldt-Bausch, R. (1985). Basal ganglia and limbic system pathology in schizophrenia. Archives of General Psychiatry 42, 784791.CrossRefGoogle ScholarPubMed
Bruton, C. J. (1988). The Neuropathology of Temporal Lobe Epilepsy. Oxford University Press: Oxford.Google Scholar
Bunney, B. S. & Aghajanian, G. K. (1976). Dopamine and norepinephrine innervated cells in the rat prefrontal cortex: pharmacological differentiation using microiontophoretic techniques. Life Sciences 19, 17831792.CrossRefGoogle ScholarPubMed
Chiodo, L. A. & Antelman, S. M. (1980). Electroconvulsive shock: progressive dopamine autoreceptor subsensitivity independent of repeated treatment. Science 210, 799801.CrossRefGoogle ScholarPubMed
Cotman, C. W. & Nadler, J. V. (1978). Reactive synaptogenesis in the hippocampus. In Neuronal Plasticity (ed. Cotman, C. W.), pp. 227272. Raven Press: New York.Google Scholar
Csernansky, J. G., Holman, C. A., Bonnet, K. A., Grabowsky, K., King, R. & Hollister, L. E. (1983). Dopaminergic supersensitivity at distant sites following induced epileptic foci. Life Sciences 32. 385390.Google Scholar
Currie, S., Heathfield, K. W. G., Henson, R. A. & Scott, D. F. (1971). Clinical course and prognosis of temporal lobe epilepsy. Brain 94, 173190.Google Scholar
Deakin, J. F. W., Slater, P., Simpson, M. D. C., Gilchrist, A. C., Skan, W., Royston, M. C., Reynolds, G. P. & Cross, A. J. (1989). Frontal-cortical and left temporal glutamatergic dysfunction in schizophrenia. Journal of Neurochemislry 52, 17811786.CrossRefGoogle ScholarPubMed
Delgado-Escueto, A. V. & Walsh, G. O. (1985). Type I complex partial seizures of hippocampal origin: excellent results of anterior temporal lobectomy. Neurology 35, 143154.CrossRefGoogle Scholar
Duncan, J. S. & Sagar, H. J. (1987). Seizure characteristics, pathology, and outcome after temporal lobectomy. Neurology 37, 405409.Google Scholar
Engel, J. (1987). Surgical Treatment of Epilepsies. Raven Press: New York.Google Scholar
Falconer, M. A. & Serafetinides, E. A. (1963). A follow-up study of surgery in temporal lobe epilepsy. Journal of Neurology, Neurosurgery and Psychiatry 26, 154165.Google Scholar
Farley, I. J., Price, K. S., McCullough, E., Deck, J. H. N., Hordynski, W. & Hornykiewicz, O. (1978). Norepinephrine in chronic paranoid schizophrenia: above-normal levels in limbic forebrain. Science 200, 456458.CrossRefGoogle ScholarPubMed
Flor-Henry, P. (1969). Psychosis and temporal lobe epilepsy: a controlled investigation. Epilepsia 1, 117142.Google Scholar
Gallhofer, B., Trimble, M. R., Frackiowiak, R., Gibbs, J. & Jones, T. (1985). A study of cerebral blood flow and metabolism in epileptic psychosis using positron emission tomography and oxygen., Journal of Neurology, Neurosurgery and Psychiatry 48, 201206.Google Scholar
Geinisman, Y., Morrell, F. & de Toledo-Morrell, L. (1989). Perforated synapses on double-headed dendritic spines: a possible structural substrate of synaptic plasticity. Brain Research 480, 326329.Google Scholar
Gibbs, F. A. & Gibbs, E. L. (1952). Atlas of Eleelroencephalography, vol. II. Addison-Wesley: Reading, Mass.Google Scholar
Heath, R. G. & Guerrero-Figueroa, R. (1965). Psychotic behavior with evoked septal dysrhythmia: effects of intracerebral acetylcholine and gamma aminobutyric acid. American Journal of Psychiatry 121, 10801086.CrossRefGoogle ScholarPubMed
Jensen, I. & Larsen, J. K. (1979). Mental aspects of temporal lobe epilepsy. Journal of Neurology, Neurosurgery and Psychiatry 42, 256265.Google Scholar
Kleinman, J. E., Karoum, F., Rosenblatt, J. E., Gillin, J. C., Hong, J., Bridge, T. P., Zalcman, S., Storch, F., del Carmen, R. & Wyatt, R. J. (1982). Postmortem neurochemical studies in chronic schizophrenia. In Biological Markers in Psychiatry and Neurology (ed. Usdin, E. and Hanin, I.), pp. 6775. Pergamon Press: Oxford.CrossRefGoogle Scholar
Koch-Weser, M., Garron, D. C., Gilley, D. W., Bergen, D., Bleck, T. P., Morrell, F., Ristanovic, R. & Whistler, W. W. (1988). Prevalence of psychologic disorders after surgical treatment of seizures. Archives of Neurology 45, 13081311.CrossRefGoogle ScholarPubMed
Kristcnsen, O. & Sindrup, E. H. (1978). Psychomotor epilepsy and psychosis. Parts I and II. Ada Neurologica Scandinavica 57, 361379.CrossRefGoogle Scholar
Landolt, H. (1958). Serial electroencephalographic investigations during psychotic episodes in epileptic patients and during schizophrenic attacks. In Lectures on Epilepsy. (ed. de Haas, L.), pp. 91133. Elsevier Science Publishing: New York.Google Scholar
Levine, D. N. & Finklestein, S. (1982). Delayed psychosis after right temporoparietal stroke and seizures or trauma: relation to epilepsy. Neurology 32, 267273.CrossRefGoogle ScholarPubMed
Manallack, D. T., Beart, P. M. & Gundlach, A. L. (1986). Psychotomimetic 6-opiates and PCP. Trends in Neuroscience 9, 448451.Google Scholar
Margerison, J. H. & Corsellis, J. A. N. (1966). Epilepsy and the temporal lobes: clinical electroencephalographic and neuropalhological study of the brain in epilepsy with particular reference to the temporal lobes. Brain 89, 499530.CrossRefGoogle Scholar
Marques-Assis, L. (1976). Discussion. In Epileptic Seizures-Behavior-Pain (ed. Birkmayer, W.), pp. 8990. University Park Press: Baltimore.Google Scholar
Meduna, L. von (1937). Konvulsionstherapie der Schizophrenia, pp. 510529. Carl Marhold: Halle.Google Scholar
Meldrum, B. S. & Brierly, J. B. (1973). Prolonged epileptic seizure in primates. Archives of Neurology 28, 1017.Google Scholar
Moore, R. Y., Bjorklund, A. & Stenevui, U. (1971). Plastic changes in the adrenergic innervation of the rat septal area in response to denervation. Brain Research 33, 1315.Google Scholar
Morrell, F. (1969). Physiology and histochemistry of the mirror focus. In Basic Mechanisms of the Epilepsies (ed. Jasper, H. H., Ward, A. A. and Pope, A.), pp. 357370. Little, Brown Co.: BostonGoogle Scholar
Nieto-Sampedro, M., HofT, S. F. & Cotman, C. W. (1982). Perforated postsynaptic densities: probably intermediates in synapse turnover. Proceedings of the National Academy of Sciences USA 79, 57185722.Google Scholar
Novelly, R. A., Augustine, A., Mattson, R. H., Glaser, G. H., Williamson, P. D., Spencer, D. D. & Spencer, S. S. (1984). Selective memory improvement and impairment in temporal lobectomy for epilepsy. Annals of Neurology 15, 6467.CrossRefGoogle ScholarPubMed
Olney, J. W., Collins, R. C. & Sloviter, R. S. (1986). Excitotoxic mechanisms of epileptic brain damage. In Advances in Neurology, Vol. 44 (ed. Delgado-Escueta, A. V., Ward, A. A. Jr., Woodbury, D. M. and Porter, R. J.), pp. 857877. Raven Press, New York.Google Scholar
Ounsted, C. & Lindsay, J. (1981). The long-term outcome of temporal lobe epilepsy in childhood. In Epilepsy and Psychiatry (ed. Reynolds, E. H. and Trimble, M. R.), pp. 185215. Churchill Livingstone: Edinburgh.Google Scholar
Pakalnis, A., Drake, E., John, K. & Kellum, J. B. (1987). Forced normalization: acute psychosis after seizure control in seven patients. Archives of Neurology 44, 289292.Google Scholar
Penfield, W. P. & Flanigan, H. (1950). Surgical therapy of temporal lobe seizures. Archives of Neurology and Psychiatry 64, 491500.CrossRefGoogle ScholarPubMed
Peters, J. G. (1979). Dopamine, noradrenaline and serotonin spinal fluid metabolites in temporal lobe epileptic patients with schizophrenic symptomatology. European Neurology 18, 1518.CrossRefGoogle ScholarPubMed
Polkey, C. E. (1983). Effects of anterior temporal lobectomy apart from the relief of seizures: a study of 40 patients. Journal of the Royal Society of Medicine (London) 76, 354358.Google Scholar
Prince, D. A. & Wilder, B. J. (1967). Control mechanisms in cortical cpileptogenic foci. Archives of Neurology 16, 194202.Google Scholar
Raisman, G. (1969). Neuronal plasticity in the septal nuclei of the adult rat. Brain Research 14, 2548.CrossRefGoogle ScholarPubMed
Rasmussen, T. B. (1983). Surgical treatment of complex partial seizures: results, lessons and problems. Epilepsiu 1, S65S76.Google Scholar
Reier, P. J. & Houle, J. D. (1988). The glial scar: its bearing on axonal elongation and transplantation approaches to CNS repair. In Advances in Neurology, Vol. 47: Functional Recovery in Neurological Disease (ed. Waxman, S. G.), pp. 87138. Raven Press: New York.Google Scholar
Reynolds, G. P. (1983). Increased concentrations and lateral asymmetry of amygdala dopamine in schizophrenia. Nature 305, 527529.Google Scholar
Rowe, C. C., Berkovic, B., Sia, B., Austin, M., Bladin, P. F. & McKuy, W. J. (1988). Localization of epileptic foci by postictal single photon computed tomography (SPECT) and 99mTc-HMPAO: comparison with ictal EEG in 22 patients. Neurology 38, 158.Google Scholar
Sato, M. (1976). A study on psychomotor epilepsy with ‘kindled’ cat preparations. Folia Psychialrica el Neurologica Japoniea 30, 425434.Google Scholar
Sato, M. (1977). Functional changes in the caudate and accumbens nuclei during amygdaloid and hippocampal seizure development in kindled cats. Folia Psychialrica el Neurologica Japoniea 31, 501512.Google ScholarPubMed
Schwarcz, R., Foster, A. C., French, E. D., Whetsell, W. O. Jr. & Kohler, C. (1984). Excitotoxic models for neurodegenerative disorders., Life Sciences 35, 1932.Google Scholar
Segal, M. & Bloom, F. E. (1974). The action of norepinephrine in the rat hippocampus. I. iontophoretic studies. Brain Research 72, 7997.CrossRefGoogle ScholarPubMed
Shcrwin, I. (1984). Psychiatric outcomes following surgery for temporal lobe epilepsy. In Advances in Epileptology: XVth Epilepsy International Symposium (ed. Porter, R. J., Mattson, R. H., Ward, A. Jr. and Dam, M.), pp. 497501. Raven Press: New York.Google Scholar
Simmel, M. L. & Counts, S. (1957). Clinical and psychological results of anterior temporal lobectomy in patients with psychomotor epilepsy. In Temporal Lobe Epilepsy (ed. Baldwin, M. and Bailey, P.), pp. 530550. C. C. Thomas: Springfield.Google Scholar
Slater, F., Beard, A. W. & Glithero, E. (1963). The schizophrenia-like psychoses of epilepsy. British Journal of Psychiatry 109, 95150.Google Scholar
Sloviter, R. s. (1987). Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235, 7376.CrossRefGoogle Scholar
Spielmeyer, W. (1927). Die Pathogenese des epileptischen Krampfes. Zeitschrift für die gesamte Neurologie und Psychialrie 109, 501520.Google Scholar
Stevens, J. R. (1966). Psychiatric implications of temporal lobe epilepsy. Archives of General Psychiatry 14, 461471.Google Scholar
Stevens, J. R. (1982). Neuropathology of schizophrenia. Archives of General Psychiatry 39, 11311139.Google Scholar
Stevens, J. R. (1986). Epilepsy and psychosis: neuropathologic studies of six cases. In Aspects of Epilepsy and Psychiatry (ed. Bolwig, T. and Trimble, M.), pp. 117146. John Wiley & Sons: London.Google Scholar
Stevens, J. R. & Livermore, A. Jr. (1978). Kindling of the mesolimbic dopamine system: animal model of psychosis. Neurology 28, 3646.CrossRefGoogle ScholarPubMed
Stevens, J. R. & Lonsbury-Martin, B. (1985). Limbic system, epilepsy and psychosis: experimental studies and clinical correlations. Psychiatric Journal of the University of Ottawa 10, 193204.Google ScholarPubMed
Steward, O. (1986). Lesion induced synapse growth in the hippocampus: in search of cellular and molecular mechanisms. In The Hippocampus, vol. 3 (ed. Isaacson, R.L. and Pribram, K. H.), pp. 65111. Plenum Press: New York.Google Scholar
Sutula, T., Xiao-Xian, H., Cavazos, J. & Scott, G. (1988). Synaptic reorganization in the hippocampus induced by abnormal functional activity. Science 239, 11471150.CrossRefGoogle ScholarPubMed
Taylor, D. C. (1972). Mental slate and temporal lobe epilepsy, A correlative account of 100 patients treated surgically. Epilepsia 13, 727765.CrossRefGoogle Scholar
Van Buren, J. M. & Yakovlev, P.I. (1959). Connections of the temporal lobe in man. Acta Anatomica 39, 150.CrossRefGoogle ScholarPubMed
Wada, J. & Rasmussen, T. (1960). Intracarotid injection of sodium amytal for the liberalization of cerebral speech dominance. Experimental and clinical observations. Journal of Neurosurgery 17, 266282.CrossRefGoogle Scholar
Walker, A. E. & Blumer, D. (1984). Behavioral effects of temporal lobe epilepsy. In Psychiatric Aspects of Epilepsy (ed. Blumer, D.), pp. 295323. American Psychiatric Press: Washington, D.C.Google Scholar
Weiser, H. G. & Elger, C. G. (1987). Presurgical Evaluation of Epileptics. Springer-Verlag: Berlin.Google Scholar
Whitman, S., Hermann, B. P., Black, R. B. & Chabria, S. (1982). Psychopathology and seizure type in children with epilepsy. Psychological Medicine 12, 843853.Google Scholar