Epilepsy surgery at the MNI:. From Archibald to the creation of the Shirley and Mark Rayport fellowship in surgery of epilepsy

The thread of history of epilepsy surgery has been followed on numerous occasions (Feindel et al., 2009). Our purpose is to recall some aspects of the role played by the Montreal Neurological Institute (MNI) with emphasis on the period covering the last 30 years. The discovery of the primary motor area in the dog by Fritsch and Hitzig (1870), its confirmation in primate and its extrapolation to the human by Ferrier (1876) led Horsley (1886) to apply these discoveries to treat lateralized convulsions by central resections. By the time Fedor Krause published his extensive somatotopical map of the motor cortex (Krause, 1911), the precentral gyrus had long been recognized as the primary motor center (Sebileau, 1898). Cushing (1909) demonstrated in awake patients that the primary sensory area was located within the postcentral gyrus. Archibald (1908) working at McGill published a book on neurosurgery in 1908, which emphasized the status of cerebral localization. Recognized as Canada’s first neurosurgeon, he was the key person in eventually bringing Penfield to Montreal. In 1928 the center of epilepsy surgery was in Breslau, Germany, in the clinic of Otfried Foerster. Foerster himself had studied neurology with Jules Dejerine in Paris and Carl Wernicke in Germany, two neurologists–neuroanatomists interested in cerebral localization and speech mechanisms. He also kept a working relationship with the anatomists Oskar and Cecile Vogt, themselves very involved in cortical mapping. During World War I, Foerster became a surgeon and treated peripheral nerves and spinal cord injuries and eventually posttraumatic epilepsy. Surgery for epilepsy was carried out under local anesthesia and all operative findings were plotted over a modified Vogt map of cortical regions (Foerster, 1936a,b). Foerster was the first with Altenburger to perform direct electrograms from the surface of the exposed brain (Foerster & Altenburger, 1935). Prior to coming to Montreal in 1928, Penfield spent 6 months with Foerster in Breslau and carried out histologic studies on the posttraumatic scars resected at surgery, which led to publications on posttraumatic epilepsy (Foerster & Penfield, 1930; Penfield, 1930). Penfield brought Foerster’s concepts and techniques to Montreal and in his turn developed a systematic and global approach to the surgical treatment of epilepsy, strongly reinforced with the founding of the MNI in 1934. The arrival of Herbert Jasper in 1937 led to a most successful integration of basic and clinical approach in the study of epilepsy, which had a major worldwide impact. Among the numerous early MNI contributions a few can be mentioned: that of Penfield and Boldrey (1937) on sensorimotor representation illustrated with the famous homunculus, that of Penfield and Flanigin (1950) on the surgical therapy of temporal lobe seizures, and the seminal book by Penfield and Jasper (1954): Epilepsy and the Functional Anatomy of the Human Brain. Numerous fellows and surgeons came to the MNI and later went on to establish surgical epilepsy programs abroad among others. Ed Broldrey went to the University of San Francisco; T.C. Erickson to University of Wisconsin; Guy Odom and Blaine Nashold to Duke University; Jack Handberry to Stanford University; Arthur Ward to University of Washington; Kesley Welsh to Colorado and Harvard Universities; Maitland Baldwin and John Van Buren to National Institutes of Health (NIH); Mark Rayport to Albert Einstein and Ohio Medical College; Lamar Robert to University of Florida; and Herman Flanigin to Universities of Arkansas and Georgia. Theodore Rasmussen succeeded Penfield as the epilepsy surgeon and was largely responsible for maintaining the MNI at the forefront during the 25-year period spanning from the early 1960s to the mid-1980s. His surgical techniques were impeccable and his sense of organization astonishing. As recalled by Feindel (2003) in his 25 years (1955–1980) of active surgery at the MNI, Rasmussen probably performed more operations for epilepsy than any other neurosurgeon of his time and became the foremost authority in this field. Among other achievements, he coauthored with Penfield in 1950, The Cerebral Cortex of Man. A Clinical Study of Localization of Function (Penfield & Rasmussen, 1950). In 1958 with Jasper he wrote on the role of temporomesial structures (Jasper & Rasmussen, 1958) and in 1960 with June Wada introduced the intracarotid amytal test for lateralization of speech dominance (Wada & Rasmussen, 1960). In 1962 with Brenda Milner and Charles Branch he extended the application of the amytal test for evaluation of short-term memory (Milner et al., 1962). In 1983, Rasmussen described the procedure of functional hemispherectomy, which he had applied to the treatment of focal chronic encephalitis, now recognized as Rasmussen encephalitis (Rasmussen, 1983). His teaching had a major impact on surgeons such as Falah Maroun, John Girvin, Bryce Weir, Raoul Marino, Frank LeBlanc, Terry Myles, Jean-Guy Villemure, and Richard Leblanc. Over the last 30 years the author, who also had the privilege of training and working with this giant of neurosurgery, has carried out more than 2,500 procedures for the surgical treatment of epilepsy at the MNI. Here are some of the highlights during that period. The systematic use of stereoencephalography (SEEG) was introduced in early 1972. The very first patient benefited from the technique of automatic computer seizure detection, which was being developed at the MNI by John Ives using software designed by Chris Thompson (Ives et al., 1974). The computer spike detection and quantification of interictal activity program also developed at the MNI by Jean Gotman (Gotman & Gloor, 1976) was rapidly integrated in the automatic recording system. The MNI SEEG technique based on Talairach and Bancaud’s concept evolved rapidly over the years to integrate in the stereotaxic approach various imaging modalities including stereoscopic angiography in 1972, computed tomography (CT) scanning in 1979, digital angiography in 1984, magnetic resonance imaging (MRI) in 1985, and the first anatomic integration of positron emission tomography (PET) and MRI scans in the plane of electrode insertion in 1986 (Olivier et al., 1987). A special stereotactic apparatus and later a frameless system were also designed to facilitate percutaneous insertion of electrodes and avoid blood vessels (Olivier et al., 1985). The intracranial electrodes were designed according to our specifications in the MNI neuro-electronic laboratory by Eddie Puodziunas. They are still used regularly and provide high-quality recording. The main indication for SEEG has been the syndrome of bitemporal epilepsy, which we helped to further define. The recordings of spontaneous seizures showed that the main generators of ictal events in temporal lobe epilepsy were the limbic structures, both the amygdala and the hippocampus. (Olivier et al., 1977) Patients implanted with intracranial electrodes were meticulously studied by Peter Gloor and later by Felipe Quesney and François Dubeau. Depth electrode stimulations have provided invaluable insight into function of limbic structures (Gloor et al., 1982). They have confirmed the important role played by the periamygdaloid area, first demonstrated by Feindel in the human (Feindel & Rasmussen, 1991), but also that of the hippocampus in temporal lobe epilepsy (Gloor et al., 1982). A major technical advance in the surgery of epilepsy at the MNI was the advent of the ultrasound dissector (CUSA) in 1981. With setting at very low parameters of frequency and suction that left the pia and blood vessels undisturbed, it was used routinely for all cortical resections and also for callosotomy (Olivier, 1987). Callosotomy was introduced at the MNI in 1981 and led to significant publications (Olivier et al., 1988; Tanriverdi et al., 2009c). The advent of MRI in 1984 created a tremendous resurgence of interest in the surgery of epilepsy. In 1986, Berkovic et al. (2004) from the MNI demonstrated that hippocampal sclerosis could be well demonstrated on coronal MRI. Fred Andermann and colleagues developed an interest and expertise in cortical development disorders, which led to the publication of the first large series by Palmini et al. (1991). Neuronavigation was introduced at the MNI in March 1992 and, from the very beginning, was applied systematically to all surgical procedures for epilepsy including placement of intracranial electrodes, callosotomy, selective resections, and brain tumors (Olivier et al., 1996). The use of the Allegro software provided by the ISG Technologies (Missisaugh, Ontario, Canada) enabled three-dimensional (3D) global reconstructions of the brain, which until today have remained almost unequaled. These images revealed with astonishing clarity the pre- and postcentral gyri and the central sulcus, which brought a new and more practical perspective to the concept of cerebral localization. The Allegro reconstruction software rejuvenated the long-forgotten concept of the gyral continuum put forward by Paul Broca, which was applied for ultrasound endopial navigation and resections. One of the major impacts of neuronavigation was in the field of migration disorders by helping prior to surgery to evaluate the epileptogenic nature of cortical and subcortical lesions and during surgery, to locate their position and extent. Although the traditional MRI brain map was not abandoned it was supplemented by the more precise and more specific patient’s own 3D brain map, where the exact locations of a lesion, of the stimulation data, and of the electrocorticography (ECoG) findings could be archived. The technique of local anesthesia that had been used systematically until 1992 became reserved for cases in critical zones involving speech and sensory motor area. There was a drastic reduction of the use of local anesthesia to perform temporal lobe surgery, since there was no longer a need for perioperative physiological identification of the sensory motor area by stimulation. This also led to the reduction of the use of ECoG for the routine cases of temporal lobe epilepsy and to a greater use of navigation SEEG to study the more complex ones. The advent of MRI and neuronavigation also led to a marked reduction in the size of the average craniotomy for epilepsy. However, the expertise of operating under local anesthesia was maintained, which provided the opportunity to pursue studies on cerebral localization. Work from our institution demonstrated the correlation of preoperative PET activation with peroperative stimulation studies of the sensorimotor area (Bittar et al., 1999) and of the speech areas (Olivier et al., 2001). Demonstration of seizure onset in the limbic structures with depth electrodes and hippocampal sclerosis on the MRI led to the acceptance of selective amygdalectomy as an alternative for the treatment of temporal lobe epilepsy (Wieser & Yasergil, 1982). The image-guided selective amygdalohippocampectomy was developed and introduced at the Montreal Neurological Hospital in 1992 and became one of the most frequently performed procedures in the treatment of temporal lobe epilepsy (Olivier, 2000). Using neuronavigation, a small incision and trephination are centered over the second temporal gyrus. The temporal horn is approached through a transcortical corridor, and an intraventricular resection of the amygdala and hippocampus is performed as first described by Niemeyer (1958). Recent studies of fiber impact in the so-called selective amygdalohippocampectomy using diffusion tensor imaging techniques have shown that the procedure, whatever the approach, is not so specific and encroaches on a large number of fiber tract systems (Colnat-Coulbois et al., 2009). In 1983 in a series of 214 resections for temporal lobe epilepsy, we stressed the fact that these operations imply the destruction or deafferentation of several anatomic structures that contributed to the manifestations of seizures when present or to their decrease or disappearance when resected (Olivier, 1983). The debate has continued and has often centered on the question of how much hippocampus needs to be removed (Feindel & Rasmussen, 1991; Rasmussen & Feindel, 1991). Our recent studies on fiber tract involvement in “selective” amygdalohippocampectomy confirm that we are dealing with a bewildering network, among which the hippocampus and amygdala are two important stations. It is likely that in all cases of focal epilepsies, a critical network mass needs to be disrupted in order to obtain good results. So far this has been best achieved by resective surgery. The main challenge of epilepsy surgery remains the determination of the exact focus of the seizures. Several researchers at the MNI continue working toward that goal, including Andrea and Neda Bernasconi who are refining the imaging techniques; Jean Gotman, François Dubeau, and Eliane Kobayashi, who are exploring functional MRI (fMRI); and Christophe Grova and Eliane Kobayashi who are on the forefront of magnetoencephalography (MEG) research. A major event in the surgery of epilepsy at the MNI was the creation in 2007 of the Shirley and Mark Rayport Fellowship in the Surgery of Epilepsy. Mark Rayport a former fellow at the MNI was much inspired by the work of Penfield and Talairach and developed epilepsy programs at Albert Einstein College of Medicine and at the Medical College of Ohio. He and his wife Shirley Ferguson have written extensively on psychiatric aspects and quality of life related to surgery of epilepsy. The first recipient of this fellowship was Dr Taner Tanriverdi from Istanbul, Turkey. In a span of 2 years, Dr Tanriverdi has reviewed some of our material and has been able to publish a total of 15 peer-reviewed articles in major journals including completing the first long-term prospective study on quality of life initiated some 14 years ago by Nicole Poulin (Tanriverdi et al., 2008b,c). Other topics studied included the anatomy of the central artery (Tanriverdi et al., 2008d), long-term outcome of standard versus selective temporal resections (Tanriverdi et al., 2008a), cognitive changes after a surgery (Tanriverdı & Olivier, 2007), morbidity in epilepsy based on 2,449 consecutive procedures (Tanriverdi et al., 2009a), PET findings of atypical speech representation in left hemisphere epilepsy (Tanriverdi et al., 2009b), and callosotomy (Tanriverdi et al., 2009a). In conclusion it can be said that over the last 30 years the MNI has continued to influence the field of epilepsy surgery not only by continuing to develop it at home in Montreal, with clinicians and basic scientists working under the same roof, but also by training neurosurgeons who went on to become important figures in the field such as Tanaka in Japan; Lévesque and Comair in Cleveland and Houston; Villemure at the University of Montreal; Clark in Halifax, Mascott in Dublin, Ireland; Boling in West Virginia; Baltuch in Philadelphia; Cosgrove in Boston; Lacerte and Picard in Quebec City; Wheatley in Edmonton; Steven in London, Ontario; Abosch in Minneapolis; Germano and Goodman in New York; Kim in Korea; Cukiert and Centeno in Brazil; and Jeff Hall in Montreal. As a final note I would like to underscore the paramount role played by my colleague Frederick Andermann in our epilepsy surgical program. More than any other neurologist, he has been an unbiased supporter of the surgery of epilepsy and the ideal coworker. His contribution has been enormous and his support essential. The author has no conflict of interest to disclose.

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