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The history of invasive EEG evaluation in epilepsy patients
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The history of invasive EEG evaluation in epilepsy patients Philipp S. Reif a,*, Adam Strzelczyk a,b, Felix Rosenow a,b a b
Epilepsy Center Frankfurt Rhine-Main, Department of Neurology, Johann Wolfgang Goethe University, Frankfurt am Main, Germany Epilepsy Center Hessen and Department of Neurology, Philipps-University, Marburg, Germany
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 April 2016 Accepted 13 April 2016
Modern invasive EEG recording techniques are the result of an interdisciplinary research process between neurologists and neurosurgeons that began in the 19th century. In the beginning, stimulation studies were the basis of our understanding of cortical functions. After the introduction of EEG in humans by Hans Berger and its implementation in diagnostic procedures in epilepsy patients, a new era began when Forster and Altenburger performed the first invasive EEG recording five years later. The fruitful work of Wilder Penfield and Herbert Jasper was the basis of a new understanding of epilepsy and influenced the investigations of the next generation of researchers. The development of stereotactic devices advanced by Jean Talairach and Jean Bancaud was fundamental to the understanding of deep brain functions and pathophysiological processes in epilepsy patients. In subsequent decades, new recording techniques were established and long-term video-EEG-recordings became the gold standard in presurgical evaluation. The development of imaging techniques allowed a combination of structural and electrophysiological data and restricted the indications for invasive evaluations, but also led to new concepts in the diagnostic process, including the epileptogenic network and the pathophysiological understanding of epileptogenic tissue. The following article provides an overview of the history of invasive EEG evaluation in epilepsy from the 19th century until today. ß 2016 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.
Keywords: Cortical stimulation sEEG Subdural grids Epileptogenic zone
1. Characterization of the brain cortex: early stimulation studies and their transfer to humans In the first half of the 19th century, the assumption of the brain as a single unit was challenged by observations that a focal cerebral lesion can lead to a focal deficit [1]. Based on the hypothesis of Jean Baptiste Bouillaud that speech is localized in both frontal lobes, Pierre Paul Broca was the first to describe a man with frontal lobe lesions and an expressive aphasia in 1861 [2]. His observations resulted in the localization of the speech area in the left frontal lobe, the so-called ‘‘Broca Area’’ (BA 44 and 45). In the following years, Hughlings Jackson’s investigations of epileptic patients assumed that focal seizures are induced by local cortical discharges [3]. This was supported by the results of stimulation studies in
Abbreviations: BA, brodmann area; ECoG, electrocorticography; ETLE, extra temporal lobe epilepsy; MNI, Montreal Neurological Institute; mTLE, mesial temporal lobe epilepsy; TLE, temporal lobe epilepsy; DC, direct current. * Corresponding author at: Epilepsy Center Frankfurt Rhine-Main, Department of Neurology, Johann Wolfgang Goethe University, Schleusenweg 2-16, 60528 Frankfurt, Germany. Tel.: +49 69 6301 7466; fax: +49 69 6301 84466. E-mail address: [email protected] (P.S. Reif).
animals by Theodore Fritsch and Eduard Hitzig showing focal motor activity after galvanic stimulation of the cerebral cortex [4]. Influenced by these findings and their confirmation three years later by David Ferrier, Robert Barthlow conducted the first electrical stimulation in a human brain in 1874 [5,6]. In the first years of the 20th century, more detailed results of cortical stimulation in the human brain were published. Using the technique of faradic stimulation, Harvey Cushing reported on two cases of patients with focal epilepsy in 1909 [7]: Stimulation of the postcentral gyrus intraoperatively resulted in sensory sensations of the contralateral hand. In 1911, Fedor Krause published the first detailed cortical map of the motor area of the brain [8]. During the First World War, traumatic brain injuries and the resulting epilepsy increased dramatically. Otfrid Foerster, a German neurologist from Breslau, was frustrated by the results of neurosurgical procedures conducted by his surgical colleague and started to operate himself [1]. He had already used intraoperative electrical stimulation during local anaesthesia to identify the epileptogenic focus in traumatic brain injuries. Driven by Foerster’s success, Wilder Penfield, a Canadian neurosurgeon, joined him. As a result of their work, they published an expanded map of the human cortex in 1930 [9]. The so-called ‘‘epileptogenic
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Please cite this article in press as: Reif PS, et al. The history of invasive EEG evaluation in epilepsy patients. Seizure: Eur J Epilepsy (2016), http://dx.doi.org/10.1016/j.seizure.2016.04.006
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cortical areas’’ showed detailed information about motor, sensory, acoustic and visual representations of the brain surface [9]. 2. EEG recordings in humans and their implementation in neurosurgical procedures With studies of the EEG in humans by Hans Berger in 1929, a new technique for functional analysis of the brain was introduced [10]. Inspired by Berger’s results, Otfrid Foerster and Hans Altenburger postulated the necessity of intracranial recordings for further investigations. In 1934, they published results from 30 intraoperative EEG recordings in different regions of the brain [11]. The localizing value of EEG in cases of brain tumour was stressed and an ictal seizure pattern during invasive recording was described for the first time [11]. As a consequence of the Second World War and the initial lack of notice of Berger’s discovery, the impact of epilepsy research in Europe, and especially in Germany, declined. Adrian and Matthews reported on Berger‘s discovery in the English-speaking community in 1934 [12]. Meanwhile, Gibbs and Lennox systematically demonstrated the importance of EEG in the characterization of epileptic patients [13]. In 1940, Schwartz and Kerr confirmed the results obtained by Foerster and Altenburger as they showed characteristic EEG changes in the cortex adjacent to brain tumours [14]. They demonstrated the electrical silence of intratumoral tissue and the importance of the superficial brain cortex in the generation of electrical potentials measured by EEG [14]. In 1937, the successful cooperation between Wilder Penfield and the neurologist Herbert Jasper in the Montreal Neurological Institute (MNI) began [15]. They combined cortical stimulation with EEG recording technique and established an interdisciplinary approach at the institute [16]. Influenced by his earlier work with Foerster, Penfield advanced his studies on the mapping of cortical functions and used them to better understand seizure semiology. During that time, not only the concept of the ‘‘Homunculus’’ but also precise characterizations of the insular cortex and its integrative function of frontal, parietal and temporal input were described. Intraoperative stimulation studies demonstrated the representations of gastric, motor and sensory functions by insular tissue, but also their variable representation [17–21]. A first serial invasive EEG recording over several days using epidural electrodes was performed in 1939 at the MNI and showed the importance of invasive EEG techniques in the delineation of the epileptogenic area [16]. Between 1939 and 1944, epilepsy surgery was performed in 76 cases at the MNI. Pre- and postoperative EEG were established routinely to identify the epileptogenic area as ‘‘the surgeon’s best guide’’ and the relevance of the EEG in localizing cerebral lesions started to surpass that of the pneumencephalogram [22]. Provoking procedures such as hyperventilation, hydration and metrazol were used to activate the epileptogenic focus during extraoperative recordings [23]. In a next step, acute intraoperative ECoG was routinely executed during awake surgery. According to this interictal approach and the rare recordings of seizure patterns during ECoG, Jasper proclaimed that ‘‘random spikes’’ generated by local epileptogenic lesions of the brain had the highest probability of identifying the epileptogenic focus [24]. Other epileptiform discharges, such as sharp and slow waves, had a lower localization value because they were typically found more distant from the epileptogenic lesion. Jasper used the term ‘‘primary and secondary foci’’ to describe these phenomena. He characterized the affected tissue as ‘‘normal cortex in which the epileptic discharge is conducted from a distant buried focus’’ and pointed out the dilemma to differentiate the primary from secondary epileptogenic foci, especially in deep and inaccessible brain structures [25]. Also, after-discharges or seizure patterns induced by electrical stimulation were recognized as useful to detect
epileptogenic tissue [26]. Even though their distribution did not completely correspond with the expansion of interictal spikes [24], stimulation-induced phenomena resembling the patients’ initial seizure signs were applied to define the resection area intraoperatively [27]. Penfield and Jasper confirmed that epilepsy was not produced by the cortical lesion itself but by the surrounding, partially destroyed tissue, a notion initially proposed by Jackson. In cases of epilepsy surgery, Penfield and Steelman summarized that ‘‘the epileptogenic focus in the marginal partly involved gyri must also (be) removed’’ by cortical excision [23]. 3. Investigation of deep structures and the beginnings of sEEG Over the course of time, it became clear that not only surface grey matter was involved in the generation of epileptic seizures. Subcortical and deep brain lesions like the thalamus, basal ganglia and other regions were identified as sources of slow EEG and epileptiform activity [28]. Furthermore, the influence of thalamocortical circuits was discussed as a result of stimulation studies in animals and their impact on generalized epilepsies [29]. In temporal lobe epilepsy (TLE) the importance of the resection of mesial TL structures was recognized [25,26]. Jasper discovered the phenomena of initial EEG suppression, especially in seizures with a deep anterior or mesial focus [25]. Additionally, the interhemispheric connectivity between homologue regions and the observation of a fast shift of pathological EEG patterns in TLE highlighted the necessity of a better understanding of subcortical regions and tracts and their function in seizure generation and propagation [25]. Robert Hayne and Russel Meyers published the first report about stereotactically implanted EEG electrodes in humans with epilepsy in 1949 [30]. They described combined and independent seizure activity in cortical and subcortical structures and advanced the importance of expanded simultaneous investigations of superficial and deep brain tissue. However, at that time, the implantation system was not individualized enough, resulting in inaccuracy in investigations of small nuclear structures [31]. At the same time, Jean Talairach, a French neurosurgeon, gained his first experience with stereotactic procedures. He improved the implantation technique and used the pneumencephalogram to adapt the implantation coordinates with respect to ventricular position and size [32]. He defined a system of reference lines and structures that allowed an individualized and optimized approach for investigations of deep brain structures and their anatomical localization. His work culminated in the publication of the first atlas of stereotactically defined brain structures in 1957, followed by a second edition 10 years later [33,34]. Working in the St. Anne Hospital in France, he met Jean Bancaud, a neurologist and neurophysiologist interested in EEG and influenced by the French pioneer on epileptology, Henri He´caen, who had previously worked with Wilder Penfield at the MNI [35]. Comparable to the MNI, the interdisciplinary approach to the investigations in epilepsy and epilepsy surgery at St. Anne Hospital was the basis of successful work over the next decades. Together with Jean Bancaud, he advanced stereotactic techniques in epilepsy patients. The application of depth electrodes allowed not only the recording of deep brain structures; it also offered the possibility of a threedimensional analysis of seizure patterns, their distribution and propagation and correlation to clinical features. The technique allowed longer and serial terms of recordings as well as the separation of diagnostic and surgical procedures [36]. Due to the good tolerance of intracranial stereo-EEG (sEEG), ‘‘chronic’’ investigations with a duration of days up to weeks became possible. Talairach and Bancaud developed new concepts in the definition of seizure-relevant tissue. The resections of Penfield initially were, in most cases, guided by interictal spikes and
Please cite this article in press as: Reif PS, et al. The history of invasive EEG evaluation in epilepsy patients. Seizure: Eur J Epilepsy (2016), http://dx.doi.org/10.1016/j.seizure.2016.04.006
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stimulation phenomena [24,26]. Ictal recordings were unusual due to the acute recording technique during awake surgery under local anaesthesia. Using prolonged sEEG, Talairach and Bancaud now had the opportunity to capture seizure patterns during the diagnostic process. They conceptualized the relationship between a cerebral lesion, the irritative zone and the epileptogenic focus [37]. In contrast to Jasper, they stated that spikes were not likely to localize the epileptogenic focus. The so-called ‘‘irritative zone’’ was considered solely an interictal phenomenon and more an expression of a functional rather than a structural lesion. Seizures could be recorded very distant to a potential lesion. They proposed that it was indispensable to analyze serial seizure patterns under various conditions to understand the extension of the potential epileptogenic focus. Their depiction of an epileptogenic focus was a combined definition using electrical and clinical features including the site of origin, its primary organization and relation to clinical features considering the spatio-temporal characteristics of epileptic seizures [37,38]. This concept provided a so-called anatomoelectro-clinical correlate for the definition of the epileptogenic zone, the ‘‘epileptogenic network’’. Several essential publications followed over the next years. Penfield and Jasper’s centrencephalic concept of generalized seizure pattern was extended by the observation that mesial frontal structures were involved in their generation [39]. The pivotal role of the anterior cingulate gyrus in epileptic automatism was also proposed [40,41]. Angiographic studies, together with Gabor Szikla, essentially improved the anatomical understanding of vascularization and localization of brain structures prior to the imaging area of CT and MRI [42]. Until the beginning of the 1980s, sEEG was the gold standard for investigations in epilepsy patients. 4. Further applications: subdural grids and sphenoidal and foramen ovale electrodes The use of subdural grids was relatively rare during the first decades of invasive EEG diagnostics. Marsan and van Buren combined as one of the first subdural, epidural and depth electrodes for their investigations in temporal lobe epilepsy and established a standardized implantation plan for temporal lobe epilepsies [43]. Additionally, Fisher-Wiliams demonstrated the safe and successful use of subdural grids in epilepsy patients [44]. Since the 1980s, subdural grids have become more popular, especially outside of Europe. High technical requirements, costs and expertise when using sEEG were some of the reasons for the growing utilization of subdural recordings. Allen Wyler and colleagues were one of the first groups to use subdural electrodes again [45]. They proved their safety and emphasized their power in exploring the mesial temporal lobe structures through a subtemporal access. Various models concerning different sizes and extents allowed a sufficient coverage of the convexity of the cortex. Eloquent areas, especially in the perirolandic region, could be sufficiently delineated and more precisely so than when sEEG was used. Furthermore, functional analysis and cortical evoked potentials were implemented in subdural electrodes [46]. From the beginning, invasive recordings were a time-consuming and expensive procedure. Several techniques were developed to simplify the diagnostic process. Sphenoidal electrodes were introduced, but could not replace the necessity of more invasive investigations [47]. Later in Zurich, Heinz Gregor Wieser and Gazi Yas¸argil developed the technique of foramen ovale electrodes and propagated it for investigations in mTL [48]. The observation that a high number of TLE were solely produced by mesial structures led to the more limited resection strategy of selective amygdalohippocampectomy, now a widely used technique in addition to the classical technique of lobectomy in mTL patients [49,50].
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5. CT and MRI imaging techniques and their influence on invasive EEG recordings With the invention of CT and MRI scans in the 1980s, the use of invasive recordings declined. The indication for invasive monitoring was progressively limited to patients with MR-negative epilepsies, epilepsies with potential epileptogenic lesion but non-concordant EEG or epilepsies with an assumed epileptogenic focus in eloquent cortex areas. It was the time when closed circuit television and cable telemetry systems allowed more prolonged seizure monitoring [51]. Retrospective and recurrent seizure observations allowed a more detailed analysis of their correlation with the epileptogenic area [52]. Functional techniques, such as PET and ictal SPECT, were also established in the early 1980s [53]. As a consequence, new concepts were implemented for the definition of epilepsy-relevant brain areas [54]. The zone concept by Hans Luders defined six cortical zones as a result of seizure semiology, electroencephalographic analysis, neurological and neurophysiological examination and imaging techniques. His concept defined the epileptogenic zone as the ‘‘cortical region (which is) indispensable for the generation of epileptic seizures’’ and resulted in a more restricted definition than the complex neuronal network hypothesis proposed by Talairach and Bancaud [55,56]. Today, different invasive recording techniques are widely used. Whereas sEEG is the favourable technique for investigations of deep brain structures, subdural electrodes are predominantly used in neocortical and cortical located epilepsies of the convexity of the brain. In addition to the original technique of Talairach, which was predominantly practiced in the French and Italian community, the development of new and simplified insertion techniques of sEEG have gained increasing popularity in the past 10 years in the rest of Europe and North America [57]. Frameless and robot-assisted implantation techniques were developed and allowed an easier, safe, accurate and timesaving insertion of sEEG [58]. Also, the combined use of both techniques was shown to be a reasonable technique in some cases of TLE and ETLE [59]. 6. Slow and fast activity in invasive EEG Over the last 20 years, fast and slow frequency potentials have received more attention as they were found to be useful in the definition of epileptogenic area. Direct current (DC)-shift recordings have been known experimentally since the 1950s and were first reported in penicillin-induced seizures. Ikeda observed that ictal DC shift corresponded with epileptogenic areas in patients with subdural electrodes [60]. Additionally, investigations in infraslow activity led to the assumption that additional tools would be established to characterize the epileptogenic tissue [61]. Already in early studies by Bragin in patients with epilepsy, it was noticed that fast ripples occurred in the epileptogenic area during intracranial recordings and thus were proposed as a biomarker for the epileptogenic zone [62]. This technique is not yet implemented in routine diagnostics, but rather adds to the definition and better understanding of epileptogenic actions in the epileptic human brain. 7. Conclusion Starting from the early observations by Foerster and Altenburger, invasive EEG recordings were established in clinical diagnostics. Both techniques, sEEG and subdural grids, were widely used and could also be combined [59]. Regardless of the success of imaging techniques and their combination with electroencephalography and independent of their definition, the delineation of the
Please cite this article in press as: Reif PS, et al. The history of invasive EEG evaluation in epilepsy patients. Seizure: Eur J Epilepsy (2016), http://dx.doi.org/10.1016/j.seizure.2016.04.006
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epileptogenic zone still remains a challenge during invasive EEG examinations. Different concepts of their definitions have been successfully implemented in the diagnostics of epilepsy. An interdisciplinary approach was the key to revolutionary steps in the history of invasive EEG recordings and the development of new techniques. This potential should be utilized for further investigations in epilepsy patients. Conflicts of interest Dr. Reif has received research support from the Stiftung P.E. Kempkes, Marburg. Dr. Strzelczyk reports personal fees and grants from Bayer HealthCare, Boehringer Ingelheim, Desitin Arzneimittel, Eisai, Pfizer, Sage Therapeutics, and UCB Pharma, outside of the submitted work. Dr. Rosenow has received honoraria for services as advisor from UCB, EISAI, Shire, Viropharma, Desitin, Cerbomed and for presentations from UCB, EISAI, Desitin, Hexal, Bayer-Vital, Cerbomed, Novartis, LMU-Mu¨nchen, Scho¨nklinik Schwabing, American Hospital Tirana. FR also received research support from the EU (within FP6 and FP7), the European Science-Foundation, the DFG and the Klaus-Dieter Scharf Forschungsprojekt. Acknowledgement We thank Dr. A. M. Hermsen for reading and critically discussing the manuscript. References [1] Lueders JC, Lueders HO. Contributions of Fedor Krause and Otfrid Foerster to epilepsy surgery. In: Lueders HO, Comair YG, editors. Epilepsy surgery. Philadelphia: Lippincott Wiliams & Wilkins; 2001. p. 23–33. [2] Berker EA, Berker AH, Smith A. Translation of Broca’s 1865 report. Localization of speech in the third left frontal convolution. Arch Neurol 1986;43:1065–72. [3] York 3rd GK, Steinberg DA. Hughlings Jackson’s neurological ideas. Brain 2011;134:3106–13. [4] Fritsch G, Hitzig E. Electric excitability of the cerebrum Uber die elektrische Erregbarkeit des Grosshirns Epilepsy Behav 2009;15:123–30. [5] Ferrier D. Experimental researches in cerebral physiology and pathology. J Anat Physiol 1873;8:152–5. [6] Bartholow R. Experimental investigations into the functions of the human brain. Am J Med Sci 1874;66:305–13. [7] Cushing III H. Partial hypophysectomy for acromegaly: with remarks on the function of the hypophysis. Ann Surg 1909;50:1002–17. [8] Krause F. Chirurgie des Gehirns und Ru¨ckenmarks nach eigenen Erfahrungen. Berlin: Urban und Schwarzenberg; 1911. [9] Foerster O, Penfield W. The structural basis of traumatic epilepsy and results of radical operation. Brain 1930;53:99–119. [10] Berger H. Uber das Elektrenkephalogramm des Menschen. Arch Psychiatr Nervenkr 1929;87:527–70. [11] Foerster O, Altenburger H. Elektrobiologische Vorga¨nge an der menschlichen Hirnrinde. Dtsch Z Nervenheilk 1934;135:277–88. [12] Adrian ED, Matthews BHC. The Berger Rhythm: potential changes from the occipital lobes in man. Brain 1934;57:355–85. [13] Gibbs FA, Gibbs EL, Lennox WG. The electro-encephalogram in diagnosis and in localization of epileptic seizures. AMA Arch Neurol Psychiatry 1936;36: 1225–35. [14] Schwartz HG, Kerr AS. Electrical activity of the exposed human brain. AMA Arch Neurol Psychiatry 1940;43:547–59. [15] Feindel W. Epilepsy surgery in Canada. In: Lueders HO, editor. Textbook of epilepsy surgery. London: Informa Healthcare; 2008. p. 103–15. [16] Almeida AN, Martinez V, Feindel W. The first case of invasive EEG monitoring for the surgical treatment of epilepsy: historical significance and context. Epilepsia 2005;46:1082–5. [17] Rasmussen T, Penfield W. The human sensorimotor cortex as studied by electrical stimulation. Fed Proc 1947;6:184. [18] Rasmussen T, Penfield W. Further studies of the sensory and motor cerebral cortex of man. Fed Proc 1947;6:452–60. [19] Schott GD. Penfield’s homunculus: a note on cerebral cartography. J Neurol Neurosurg Psychiatry 1993;56:329–33. [20] Penfield W, Boldrey E. Somatic motor and sensory representations in the cerebral cortex of man as studied by electrical stimulation. Brain 1937;60: 389–443. [21] Penfield W, Faulk Jr ME. The insula; further observations on its function. Brain 1955;78:445–70. [22] Jasper H. Electrical activity of the brain. Annu Rev Physiol 1941;3:377–98.
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Seizure journal homepage: www.elsevier.com/locate/yseiz
The history of invasive EEG evaluation in epilepsy patients Philipp S. Reif a,*, Adam Strzelczyk a,b, Felix Rosenow a,b a b
Epilepsy Center Frankfurt Rhine-Main, Department of Neurology, Johann Wolfgang Goethe University, Frankfurt am Main, Germany Epilepsy Center Hessen and Department of Neurology, Philipps-University, Marburg, Germany
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 April 2016 Accepted 13 April 2016
Modern invasive EEG recording techniques are the result of an interdisciplinary research process between neurologists and neurosurgeons that began in the 19th century. In the beginning, stimulation studies were the basis of our understanding of cortical functions. After the introduction of EEG in humans by Hans Berger and its implementation in diagnostic procedures in epilepsy patients, a new era began when Forster and Altenburger performed the first invasive EEG recording five years later. The fruitful work of Wilder Penfield and Herbert Jasper was the basis of a new understanding of epilepsy and influenced the investigations of the next generation of researchers. The development of stereotactic devices advanced by Jean Talairach and Jean Bancaud was fundamental to the understanding of deep brain functions and pathophysiological processes in epilepsy patients. In subsequent decades, new recording techniques were established and long-term video-EEG-recordings became the gold standard in presurgical evaluation. The development of imaging techniques allowed a combination of structural and electrophysiological data and restricted the indications for invasive evaluations, but also led to new concepts in the diagnostic process, including the epileptogenic network and the pathophysiological understanding of epileptogenic tissue. The following article provides an overview of the history of invasive EEG evaluation in epilepsy from the 19th century until today. ß 2016 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.
Keywords: Cortical stimulation sEEG Subdural grids Epileptogenic zone
1. Characterization of the brain cortex: early stimulation studies and their transfer to humans In the first half of the 19th century, the assumption of the brain as a single unit was challenged by observations that a focal cerebral lesion can lead to a focal deficit [1]. Based on the hypothesis of Jean Baptiste Bouillaud that speech is localized in both frontal lobes, Pierre Paul Broca was the first to describe a man with frontal lobe lesions and an expressive aphasia in 1861 [2]. His observations resulted in the localization of the speech area in the left frontal lobe, the so-called ‘‘Broca Area’’ (BA 44 and 45). In the following years, Hughlings Jackson’s investigations of epileptic patients assumed that focal seizures are induced by local cortical discharges [3]. This was supported by the results of stimulation studies in
Abbreviations: BA, brodmann area; ECoG, electrocorticography; ETLE, extra temporal lobe epilepsy; MNI, Montreal Neurological Institute; mTLE, mesial temporal lobe epilepsy; TLE, temporal lobe epilepsy; DC, direct current. * Corresponding author at: Epilepsy Center Frankfurt Rhine-Main, Department of Neurology, Johann Wolfgang Goethe University, Schleusenweg 2-16, 60528 Frankfurt, Germany. Tel.: +49 69 6301 7466; fax: +49 69 6301 84466. E-mail address: [email protected] (P.S. Reif).
animals by Theodore Fritsch and Eduard Hitzig showing focal motor activity after galvanic stimulation of the cerebral cortex [4]. Influenced by these findings and their confirmation three years later by David Ferrier, Robert Barthlow conducted the first electrical stimulation in a human brain in 1874 [5,6]. In the first years of the 20th century, more detailed results of cortical stimulation in the human brain were published. Using the technique of faradic stimulation, Harvey Cushing reported on two cases of patients with focal epilepsy in 1909 [7]: Stimulation of the postcentral gyrus intraoperatively resulted in sensory sensations of the contralateral hand. In 1911, Fedor Krause published the first detailed cortical map of the motor area of the brain [8]. During the First World War, traumatic brain injuries and the resulting epilepsy increased dramatically. Otfrid Foerster, a German neurologist from Breslau, was frustrated by the results of neurosurgical procedures conducted by his surgical colleague and started to operate himself [1]. He had already used intraoperative electrical stimulation during local anaesthesia to identify the epileptogenic focus in traumatic brain injuries. Driven by Foerster’s success, Wilder Penfield, a Canadian neurosurgeon, joined him. As a result of their work, they published an expanded map of the human cortex in 1930 [9]. The so-called ‘‘epileptogenic
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Please cite this article in press as: Reif PS, et al. The history of invasive EEG evaluation in epilepsy patients. Seizure: Eur J Epilepsy (2016), http://dx.doi.org/10.1016/j.seizure.2016.04.006
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cortical areas’’ showed detailed information about motor, sensory, acoustic and visual representations of the brain surface [9]. 2. EEG recordings in humans and their implementation in neurosurgical procedures With studies of the EEG in humans by Hans Berger in 1929, a new technique for functional analysis of the brain was introduced [10]. Inspired by Berger’s results, Otfrid Foerster and Hans Altenburger postulated the necessity of intracranial recordings for further investigations. In 1934, they published results from 30 intraoperative EEG recordings in different regions of the brain [11]. The localizing value of EEG in cases of brain tumour was stressed and an ictal seizure pattern during invasive recording was described for the first time [11]. As a consequence of the Second World War and the initial lack of notice of Berger’s discovery, the impact of epilepsy research in Europe, and especially in Germany, declined. Adrian and Matthews reported on Berger‘s discovery in the English-speaking community in 1934 [12]. Meanwhile, Gibbs and Lennox systematically demonstrated the importance of EEG in the characterization of epileptic patients [13]. In 1940, Schwartz and Kerr confirmed the results obtained by Foerster and Altenburger as they showed characteristic EEG changes in the cortex adjacent to brain tumours [14]. They demonstrated the electrical silence of intratumoral tissue and the importance of the superficial brain cortex in the generation of electrical potentials measured by EEG [14]. In 1937, the successful cooperation between Wilder Penfield and the neurologist Herbert Jasper in the Montreal Neurological Institute (MNI) began [15]. They combined cortical stimulation with EEG recording technique and established an interdisciplinary approach at the institute [16]. Influenced by his earlier work with Foerster, Penfield advanced his studies on the mapping of cortical functions and used them to better understand seizure semiology. During that time, not only the concept of the ‘‘Homunculus’’ but also precise characterizations of the insular cortex and its integrative function of frontal, parietal and temporal input were described. Intraoperative stimulation studies demonstrated the representations of gastric, motor and sensory functions by insular tissue, but also their variable representation [17–21]. A first serial invasive EEG recording over several days using epidural electrodes was performed in 1939 at the MNI and showed the importance of invasive EEG techniques in the delineation of the epileptogenic area [16]. Between 1939 and 1944, epilepsy surgery was performed in 76 cases at the MNI. Pre- and postoperative EEG were established routinely to identify the epileptogenic area as ‘‘the surgeon’s best guide’’ and the relevance of the EEG in localizing cerebral lesions started to surpass that of the pneumencephalogram [22]. Provoking procedures such as hyperventilation, hydration and metrazol were used to activate the epileptogenic focus during extraoperative recordings [23]. In a next step, acute intraoperative ECoG was routinely executed during awake surgery. According to this interictal approach and the rare recordings of seizure patterns during ECoG, Jasper proclaimed that ‘‘random spikes’’ generated by local epileptogenic lesions of the brain had the highest probability of identifying the epileptogenic focus [24]. Other epileptiform discharges, such as sharp and slow waves, had a lower localization value because they were typically found more distant from the epileptogenic lesion. Jasper used the term ‘‘primary and secondary foci’’ to describe these phenomena. He characterized the affected tissue as ‘‘normal cortex in which the epileptic discharge is conducted from a distant buried focus’’ and pointed out the dilemma to differentiate the primary from secondary epileptogenic foci, especially in deep and inaccessible brain structures [25]. Also, after-discharges or seizure patterns induced by electrical stimulation were recognized as useful to detect
epileptogenic tissue [26]. Even though their distribution did not completely correspond with the expansion of interictal spikes [24], stimulation-induced phenomena resembling the patients’ initial seizure signs were applied to define the resection area intraoperatively [27]. Penfield and Jasper confirmed that epilepsy was not produced by the cortical lesion itself but by the surrounding, partially destroyed tissue, a notion initially proposed by Jackson. In cases of epilepsy surgery, Penfield and Steelman summarized that ‘‘the epileptogenic focus in the marginal partly involved gyri must also (be) removed’’ by cortical excision [23]. 3. Investigation of deep structures and the beginnings of sEEG Over the course of time, it became clear that not only surface grey matter was involved in the generation of epileptic seizures. Subcortical and deep brain lesions like the thalamus, basal ganglia and other regions were identified as sources of slow EEG and epileptiform activity [28]. Furthermore, the influence of thalamocortical circuits was discussed as a result of stimulation studies in animals and their impact on generalized epilepsies [29]. In temporal lobe epilepsy (TLE) the importance of the resection of mesial TL structures was recognized [25,26]. Jasper discovered the phenomena of initial EEG suppression, especially in seizures with a deep anterior or mesial focus [25]. Additionally, the interhemispheric connectivity between homologue regions and the observation of a fast shift of pathological EEG patterns in TLE highlighted the necessity of a better understanding of subcortical regions and tracts and their function in seizure generation and propagation [25]. Robert Hayne and Russel Meyers published the first report about stereotactically implanted EEG electrodes in humans with epilepsy in 1949 [30]. They described combined and independent seizure activity in cortical and subcortical structures and advanced the importance of expanded simultaneous investigations of superficial and deep brain tissue. However, at that time, the implantation system was not individualized enough, resulting in inaccuracy in investigations of small nuclear structures [31]. At the same time, Jean Talairach, a French neurosurgeon, gained his first experience with stereotactic procedures. He improved the implantation technique and used the pneumencephalogram to adapt the implantation coordinates with respect to ventricular position and size [32]. He defined a system of reference lines and structures that allowed an individualized and optimized approach for investigations of deep brain structures and their anatomical localization. His work culminated in the publication of the first atlas of stereotactically defined brain structures in 1957, followed by a second edition 10 years later [33,34]. Working in the St. Anne Hospital in France, he met Jean Bancaud, a neurologist and neurophysiologist interested in EEG and influenced by the French pioneer on epileptology, Henri He´caen, who had previously worked with Wilder Penfield at the MNI [35]. Comparable to the MNI, the interdisciplinary approach to the investigations in epilepsy and epilepsy surgery at St. Anne Hospital was the basis of successful work over the next decades. Together with Jean Bancaud, he advanced stereotactic techniques in epilepsy patients. The application of depth electrodes allowed not only the recording of deep brain structures; it also offered the possibility of a threedimensional analysis of seizure patterns, their distribution and propagation and correlation to clinical features. The technique allowed longer and serial terms of recordings as well as the separation of diagnostic and surgical procedures [36]. Due to the good tolerance of intracranial stereo-EEG (sEEG), ‘‘chronic’’ investigations with a duration of days up to weeks became possible. Talairach and Bancaud developed new concepts in the definition of seizure-relevant tissue. The resections of Penfield initially were, in most cases, guided by interictal spikes and
Please cite this article in press as: Reif PS, et al. The history of invasive EEG evaluation in epilepsy patients. Seizure: Eur J Epilepsy (2016), http://dx.doi.org/10.1016/j.seizure.2016.04.006
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stimulation phenomena [24,26]. Ictal recordings were unusual due to the acute recording technique during awake surgery under local anaesthesia. Using prolonged sEEG, Talairach and Bancaud now had the opportunity to capture seizure patterns during the diagnostic process. They conceptualized the relationship between a cerebral lesion, the irritative zone and the epileptogenic focus [37]. In contrast to Jasper, they stated that spikes were not likely to localize the epileptogenic focus. The so-called ‘‘irritative zone’’ was considered solely an interictal phenomenon and more an expression of a functional rather than a structural lesion. Seizures could be recorded very distant to a potential lesion. They proposed that it was indispensable to analyze serial seizure patterns under various conditions to understand the extension of the potential epileptogenic focus. Their depiction of an epileptogenic focus was a combined definition using electrical and clinical features including the site of origin, its primary organization and relation to clinical features considering the spatio-temporal characteristics of epileptic seizures [37,38]. This concept provided a so-called anatomoelectro-clinical correlate for the definition of the epileptogenic zone, the ‘‘epileptogenic network’’. Several essential publications followed over the next years. Penfield and Jasper’s centrencephalic concept of generalized seizure pattern was extended by the observation that mesial frontal structures were involved in their generation [39]. The pivotal role of the anterior cingulate gyrus in epileptic automatism was also proposed [40,41]. Angiographic studies, together with Gabor Szikla, essentially improved the anatomical understanding of vascularization and localization of brain structures prior to the imaging area of CT and MRI [42]. Until the beginning of the 1980s, sEEG was the gold standard for investigations in epilepsy patients. 4. Further applications: subdural grids and sphenoidal and foramen ovale electrodes The use of subdural grids was relatively rare during the first decades of invasive EEG diagnostics. Marsan and van Buren combined as one of the first subdural, epidural and depth electrodes for their investigations in temporal lobe epilepsy and established a standardized implantation plan for temporal lobe epilepsies [43]. Additionally, Fisher-Wiliams demonstrated the safe and successful use of subdural grids in epilepsy patients [44]. Since the 1980s, subdural grids have become more popular, especially outside of Europe. High technical requirements, costs and expertise when using sEEG were some of the reasons for the growing utilization of subdural recordings. Allen Wyler and colleagues were one of the first groups to use subdural electrodes again [45]. They proved their safety and emphasized their power in exploring the mesial temporal lobe structures through a subtemporal access. Various models concerning different sizes and extents allowed a sufficient coverage of the convexity of the cortex. Eloquent areas, especially in the perirolandic region, could be sufficiently delineated and more precisely so than when sEEG was used. Furthermore, functional analysis and cortical evoked potentials were implemented in subdural electrodes [46]. From the beginning, invasive recordings were a time-consuming and expensive procedure. Several techniques were developed to simplify the diagnostic process. Sphenoidal electrodes were introduced, but could not replace the necessity of more invasive investigations [47]. Later in Zurich, Heinz Gregor Wieser and Gazi Yas¸argil developed the technique of foramen ovale electrodes and propagated it for investigations in mTL [48]. The observation that a high number of TLE were solely produced by mesial structures led to the more limited resection strategy of selective amygdalohippocampectomy, now a widely used technique in addition to the classical technique of lobectomy in mTL patients [49,50].
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5. CT and MRI imaging techniques and their influence on invasive EEG recordings With the invention of CT and MRI scans in the 1980s, the use of invasive recordings declined. The indication for invasive monitoring was progressively limited to patients with MR-negative epilepsies, epilepsies with potential epileptogenic lesion but non-concordant EEG or epilepsies with an assumed epileptogenic focus in eloquent cortex areas. It was the time when closed circuit television and cable telemetry systems allowed more prolonged seizure monitoring [51]. Retrospective and recurrent seizure observations allowed a more detailed analysis of their correlation with the epileptogenic area [52]. Functional techniques, such as PET and ictal SPECT, were also established in the early 1980s [53]. As a consequence, new concepts were implemented for the definition of epilepsy-relevant brain areas [54]. The zone concept by Hans Luders defined six cortical zones as a result of seizure semiology, electroencephalographic analysis, neurological and neurophysiological examination and imaging techniques. His concept defined the epileptogenic zone as the ‘‘cortical region (which is) indispensable for the generation of epileptic seizures’’ and resulted in a more restricted definition than the complex neuronal network hypothesis proposed by Talairach and Bancaud [55,56]. Today, different invasive recording techniques are widely used. Whereas sEEG is the favourable technique for investigations of deep brain structures, subdural electrodes are predominantly used in neocortical and cortical located epilepsies of the convexity of the brain. In addition to the original technique of Talairach, which was predominantly practiced in the French and Italian community, the development of new and simplified insertion techniques of sEEG have gained increasing popularity in the past 10 years in the rest of Europe and North America [57]. Frameless and robot-assisted implantation techniques were developed and allowed an easier, safe, accurate and timesaving insertion of sEEG [58]. Also, the combined use of both techniques was shown to be a reasonable technique in some cases of TLE and ETLE [59]. 6. Slow and fast activity in invasive EEG Over the last 20 years, fast and slow frequency potentials have received more attention as they were found to be useful in the definition of epileptogenic area. Direct current (DC)-shift recordings have been known experimentally since the 1950s and were first reported in penicillin-induced seizures. Ikeda observed that ictal DC shift corresponded with epileptogenic areas in patients with subdural electrodes [60]. Additionally, investigations in infraslow activity led to the assumption that additional tools would be established to characterize the epileptogenic tissue [61]. Already in early studies by Bragin in patients with epilepsy, it was noticed that fast ripples occurred in the epileptogenic area during intracranial recordings and thus were proposed as a biomarker for the epileptogenic zone [62]. This technique is not yet implemented in routine diagnostics, but rather adds to the definition and better understanding of epileptogenic actions in the epileptic human brain. 7. Conclusion Starting from the early observations by Foerster and Altenburger, invasive EEG recordings were established in clinical diagnostics. Both techniques, sEEG and subdural grids, were widely used and could also be combined [59]. Regardless of the success of imaging techniques and their combination with electroencephalography and independent of their definition, the delineation of the
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epileptogenic zone still remains a challenge during invasive EEG examinations. Different concepts of their definitions have been successfully implemented in the diagnostics of epilepsy. An interdisciplinary approach was the key to revolutionary steps in the history of invasive EEG recordings and the development of new techniques. This potential should be utilized for further investigations in epilepsy patients. Conflicts of interest Dr. Reif has received research support from the Stiftung P.E. Kempkes, Marburg. Dr. Strzelczyk reports personal fees and grants from Bayer HealthCare, Boehringer Ingelheim, Desitin Arzneimittel, Eisai, Pfizer, Sage Therapeutics, and UCB Pharma, outside of the submitted work. Dr. Rosenow has received honoraria for services as advisor from UCB, EISAI, Shire, Viropharma, Desitin, Cerbomed and for presentations from UCB, EISAI, Desitin, Hexal, Bayer-Vital, Cerbomed, Novartis, LMU-Mu¨nchen, Scho¨nklinik Schwabing, American Hospital Tirana. FR also received research support from the EU (within FP6 and FP7), the European Science-Foundation, the DFG and the Klaus-Dieter Scharf Forschungsprojekt. Acknowledgement We thank Dr. A. M. Hermsen for reading and critically discussing the manuscript. References [1] Lueders JC, Lueders HO. Contributions of Fedor Krause and Otfrid Foerster to epilepsy surgery. In: Lueders HO, Comair YG, editors. Epilepsy surgery. Philadelphia: Lippincott Wiliams & Wilkins; 2001. p. 23–33. [2] Berker EA, Berker AH, Smith A. Translation of Broca’s 1865 report. Localization of speech in the third left frontal convolution. Arch Neurol 1986;43:1065–72. [3] York 3rd GK, Steinberg DA. Hughlings Jackson’s neurological ideas. Brain 2011;134:3106–13. [4] Fritsch G, Hitzig E. Electric excitability of the cerebrum Uber die elektrische Erregbarkeit des Grosshirns Epilepsy Behav 2009;15:123–30. [5] Ferrier D. Experimental researches in cerebral physiology and pathology. J Anat Physiol 1873;8:152–5. [6] Bartholow R. Experimental investigations into the functions of the human brain. Am J Med Sci 1874;66:305–13. [7] Cushing III H. Partial hypophysectomy for acromegaly: with remarks on the function of the hypophysis. Ann Surg 1909;50:1002–17. [8] Krause F. Chirurgie des Gehirns und Ru¨ckenmarks nach eigenen Erfahrungen. Berlin: Urban und Schwarzenberg; 1911. [9] Foerster O, Penfield W. The structural basis of traumatic epilepsy and results of radical operation. Brain 1930;53:99–119. [10] Berger H. Uber das Elektrenkephalogramm des Menschen. Arch Psychiatr Nervenkr 1929;87:527–70. [11] Foerster O, Altenburger H. Elektrobiologische Vorga¨nge an der menschlichen Hirnrinde. Dtsch Z Nervenheilk 1934;135:277–88. [12] Adrian ED, Matthews BHC. The Berger Rhythm: potential changes from the occipital lobes in man. Brain 1934;57:355–85. [13] Gibbs FA, Gibbs EL, Lennox WG. The electro-encephalogram in diagnosis and in localization of epileptic seizures. AMA Arch Neurol Psychiatry 1936;36: 1225–35. [14] Schwartz HG, Kerr AS. Electrical activity of the exposed human brain. AMA Arch Neurol Psychiatry 1940;43:547–59. [15] Feindel W. Epilepsy surgery in Canada. In: Lueders HO, editor. Textbook of epilepsy surgery. London: Informa Healthcare; 2008. p. 103–15. [16] Almeida AN, Martinez V, Feindel W. The first case of invasive EEG monitoring for the surgical treatment of epilepsy: historical significance and context. Epilepsia 2005;46:1082–5. [17] Rasmussen T, Penfield W. The human sensorimotor cortex as studied by electrical stimulation. Fed Proc 1947;6:184. [18] Rasmussen T, Penfield W. Further studies of the sensory and motor cerebral cortex of man. Fed Proc 1947;6:452–60. [19] Schott GD. Penfield’s homunculus: a note on cerebral cartography. J Neurol Neurosurg Psychiatry 1993;56:329–33. [20] Penfield W, Boldrey E. Somatic motor and sensory representations in the cerebral cortex of man as studied by electrical stimulation. Brain 1937;60: 389–443. [21] Penfield W, Faulk Jr ME. The insula; further observations on its function. Brain 1955;78:445–70. [22] Jasper H. Electrical activity of the brain. Annu Rev Physiol 1941;3:377–98.
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