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Epilepsy surgery in professional musicians: Subjective and objective reports of three cases
Epilepsy & Behavior 7 (2005) 552–558 www.elsevier.com/locate/yebeh
Case Report
Epilepsy surgery in professional musicians: Subjective and objective reports of three cases Reinhard Schulz a,*, Simone Horstmann a, Hennric Jokeit b, Friedrich G. Woermann a, Alois Ebner a,* b
a Epilepsy Centre Bethel, Maraweg 21, D-33617 Bielefeld, Germany Swiss Epilepsy Centre, Bleulerstrasse 60, CH-8008 Zu¨rich, Switzerland
Received 3 May 2005; revised 12 July 2005; accepted 14 July 2005 Available online 6 September 2005
Abstract We describe a small series of three professional musicians who had right (two patients) and left (one patient) temporal lobe epilepsy surgery with the histological diagnoses of hippocampal sclerosis (two patients) and benign tumor (one patient, xanthoastrocytoma). The musicians were asked to complete a questionnaire about their musical abilities before and after surgery with respect to special musical skills like melody processing, musical memory, rhythm, meter, harmony/dissonance, timbre, concentration and endurance, emotionality, and absolute pitch. In addition, the musicians submitted reports of their experiences. Surgical outcome was excellent with respect to seizures and professional skills. The two patients with right temporal lobe epilepsy reported improvements of specific musical abilities. Vocational development was very positive in all three patients. We conclude that epilepsy surgery can be safe and rewarding in professional musicians and propose initiating a database on epilepsy surgery in this special group of patients. 2005 Elsevier Inc. All rights reserved. Keywords: Temporal lobe epilepsy; Epilepsy surgery; Music; Rehabilitation; Cerebral specialization
1. Introduction Musical abilities have been thoroughly studied in healthy subjects and in patients with epilepsy [1,2]. Epilepsy surgery offers interesting opportunities to investigate the effects of circumscribed lesions on musical performance and to draw hypotheses about the cerebral representation of various aspects of music [3]. The cortical representation of musical functions might be the reason for positive or negative changes after epilepsy surgery. A number of clinical studies attribute the majority of musical functions predominantly to the right hemisphere, but some functions to the left hemisphere: *
Corresponding authors. Fax: + 49 521 144 4562. E-mail addresses: [email protected] (R. Schulz), Alois. [email protected] (A. Ebner). 1525-5050/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2005.07.009
estimation of pitch (right temporal superior gyrus) [4], imagination of music (right temporal, right and left frontal) [5], timbre (right-sided asymmetry) [6], melody (right temporal, right frontotemporal, less left frontal) [7], meter (right hemisphere) [8], rhythm (left hemisphere) [8], dissonance (right temporal) and harmony (orbitofrontal) [9], hallucination of a known song with emotional links to the biography (right auditory cortex, spread to right mesiobasal temporal lobe structures) [10], contour (right temporal) and interval (right and left temporal) as parts of melody processing [11]. To our knowledge, the outcomes of epilepsy surgery in professional musicians has not been reported in the literature up to now. Self-awareness of professional deficits in this group of patients is expected to be highly elaborated and to exceed traditional neuropsychological evaluation as well as the recently developed test battery
Case Report / Epilepsy & Behavior 7 (2005) 552–558
of amusias (Montreal Battery of the Evaluation of Amusias: MBEA) [12]. Neuropsychological tests of musical abilities focus on deficits rather than talents and are not suitable for professional musicians. We present the cases of three musicians who had surgery for temporal lobe epilepsy and concentrate on the musiciansÕ self-assessment of their postoperative professional outcome.
2. Patients and methods Four professional musicians have been operated on because of medically refractory temporal lobe epilepsy during the course of the Bethel epilepsy surgery program since 1990 (in a total of about 1000 operations until April 2003). All four became seizure free (postoperative classification: Engel 1a). One of them, a musical teacher, despite being very satisfied with the results of his surgery, chose not to participate in this study.
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The remaining three musicians (two organists, one trumpeter) completed a questionnaire. First, they were asked to judge postoperative changes (better, worse, no change) in the following abilities while making music: memory, concentration, learning, endurance; apperception of absolute pitch (if present), harmony, dissonance, timbre, melody, rhythm, meter, emotion, interaction in making music with others or in an orchestra, e.g., with respect to their own adjustment or sensitivity to mistakes of other musicians; professional development before and after surgery; effects of medication. Second, the musicians were asked to write a free report about their professional training and expertise and pre- and postsurgical experiences with epilepsy and their profession. The neuropsychological evaluation included the Wechsler Adult Intelligence Scale—Revised (verbal and nonverbal subtests) assessing intellectual abilities, the Wechsler Memory Scale—Revised (subtest: Logical Memory) and the California Verbal Learning Test
Fig. 1. Functional MRI activation map of reading music and sound imagery in patient 1 (1.5-T scanner, blocked design, rest condition text reading and ideation, z > 4). Reading musical notation and translating this notation into musical sound imagery activate a bilateral network involving areas within the diseased right temporal lobe (right superior temporal gyrus, right temporal basal posterior; activation indicated by arrows, extent of the lesion indicated by a bar). Later, the patient was successfully treated for his refractory TLE with a right-sided anterior temporal lobe resection including the tumor. After surgery he did not notice a substantial change in reading music and sound imagery.
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assessing verbal memory functions, and the Rey Complex Figure Test and Rey Visual Design Learning Test assessing visual memory functions. We classified ability into the following categories (according to standard deviations): deficient (D) < 2; below average (BA) = 3– 15; low average (LA) = 16–33; average (A) = 34–68; high average (HA) = 69–84; above average = 85–98 (AA); superior (S) > 98. An intracarotid amobarbital (Wada) test was performed in two patients (patients 1 and 2). Functional MRI of reading music and sound imagery was performed in patient 1 (1.5 T scanner, blocked design, rest condition text reading and ideation) (Fig. 1). The follow-up on an inpatient schedule included neuropsychologic reevaluation, rehabilitation interviews, and neurologic examinations 6 months and 2 years after surgery. Outpatient, telephone, and e-mail contacts were added when necessary.
The musiciansÕ self-assessments of their musical abilities with respect to memory, concentration, learning, endurance, apperception of absolute pitch, harmony, dissonance, timbre, melody, rhythm, meter, emotion, and interaction with others in making music revealed the following: In patient 1, concentration, learning (slight changes), timbre, meter, emotionality, and adaptation in making music with others improved. In patient 2, concentration, learning (slight changes), endurance (slight changes), dissonance, and rhythm improved. Patient 3 did not report any changes. None of the three patients reported a deterioration of musical abilities. Developments in their careers before and after surgery and effects of antiepileptic medications are listed in Table 2. The musiciansÕ own reports follow.
4. Case reports 3. Results
4.1. Patient 1
The general history of the epilepsy and the results of diagnostic testing are summarized in Table 1. Neuropsychologic tests demonstrated improvement of at least one standard deviation in patient 2 (nonverbal intellectual ability from LA to A, verbal learning/memory from LA to AA, nonverbal learning/memory from BA to LA) and patient 3 (nonverbal intellectual ability from HA to AA). No deterioration was noted.
4.1.1. Vocational career I studied church music and piano with organ and choir music and completed the German ‘‘A-degree’’ including artistic final examination (organ) and musical pedagogic examination (piano). Since 1981 I have permanently been employed as a church musician in the same parish. The choir developed particularly well to one of the largest in the diocese with more than 100 active singers. Concerts
Table 1 General history of epilepsy and summary of diagnosis
Age at surgery Syndrome Histology Age of onset Duration of seizures
Frequency Interictal IED Ictal EEG MRI Size of resectionb
Outcome Follow-up a b c
Patient 1
Patient 2
Patient 3
45 years (10/2001) Right TLE Xanthoastrocytoma (grade 2, WHO) Auras: childhood Seizures: age 35 10 years Gustatory + abdominal aura fi psychomotor seizurea fiRarely generalized tonic–clonic seizure Several per day 98% right mesial temporal 2% right anterior temporal Right temporal
45 years (9/2001) Right mesial TLE Hippocampal sclerosis 13 years
34 years (3/1992) Left mesial TLE Hippocampal sclerosis 13 years
32 years Abdominal aura
Right anterior and lateral temporal lobe tumor 5.5 cm plus hippocampus (complete resection of tumor)
Right mesial temporal lobe sclerosis
22 years Abdominal aura (until 5 years before surgery) fi Psychomotor seizure 5 or 6/month 90% left mesial temporal 10% right mesial temporal 21/23 left mesial temporal 2/23 right mesial temporal Normal (8/1991)
Seizure free 3 years
Seizure freec 3 years
fi psychomotor seizurea One cluster/4–6 weeks 100% right mesial temporal Right temporal
3 cm plus hippocampus
Anterior temporal with anterior hippocampus and inferior part of amygdala Seizure free 12 years
In part, automatisms with preservation of responsiveness. Lateral distance from the tip of the temporal lobe, measured in the middle temporal gyrus. Two questionable events with movements and short impairment of reactivity out of sleep, without aura some months after reduction of AEDs.
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Table 2 Vocational career and antiepileptic medication Medication (a) before and (b) after surgery and (c) at present (10/2004)
Effects of medication
1
(a) CBZa 1000 mg (b) CBZ 1200 mg for 2 years (c) No medication since 2 months
Feeling of increased vigilance at every step of medication withdrawal, also after complete cessation of medication
2
(a) LEV 2000 mg, LTG 400 mg, VPA 600 mg (b) LEV 2000 mg, LTG 600 mg (c) Mono LTG since 2/04, plus LEV since 7/04
Cessation of tremor after withdrawal of VPA before surgery; LEV without effect on musical abilities (add-on of LEV because of two mild seizures in sleep or parasomnia)
3
(a) DPH 387.5 mg, PB 100 mg (b) From 8 months after surgery complete withdrawal during 22 months (c) No medication since 6 years
Marked side effects of withdrawal after each step
Patient
a
Vocational career before surgery
Vocational career after surgery
CBZ, carbamazepine; LEV, levetiracetam; LTG, lamotrigine; DPH, phenytoin; PB, phenobarbital.
(organ works and oratorios) were performed regularly and I participated in several organ festivals. 4.1.2. Status before surgery I was successful in my profession also before surgery. However, I became more and more ‘‘unreliable’’ because of a growing number of absences which also occurred during my work. At last, after a spectacular absence during a 70th wedding anniversary, I lost the ability I used to have of musical ideas turning up during walks. I did not explicitly miss this ability, but now—after surgery—speculation and playing with musical ideas while walking rhythmically returned, and in retrospect, I noticed the difference. 4.1.3. Status after surgery One year ago, I was appointed as cantor of the deanship and I am now responsible for the professional training of all my colleagues. The number of organ concerts increased, and my organ was enlarged to 50 registers. I can say that in the parish my reputation is good and the working atmosphere is excellent. When I played on the organ during the farewell service of my previous principal several weeks after my surgery, I instantly felt that my fine motor movements in running notes and trills had become more rapid, my music was more intense and emotionally more dedicated. After an interval of several weeks I was more adept at playing my instrument than before surgery. I had a different perception as an accompanist of songs. Before surgery I predominantly heard in a harmonic way, somehow ‘‘vertically’’: To each tone of the melody I mentally filled in the suitable chord. After surgery I also heard the voices of the accompanists in their melodic development, especially in the bass voice, almost as in a choir composition. This more pronounced ‘‘horizontal’’ perception of single voices made the
playing of polyphonic music (e.g., fugues) unfamiliar and in part more difficult to me. I now perceive this change as enrichment. After surgery I now hear more sensitively and sharply, especially in the higher frequencies; I hear loud sound more pronouncedly. Musical pieces which I could play by heart before surgery are still completely at my disposal. I again rely on my rhythmicity in playing the organ. I produce fewer unwanted variations in tempo. I believe that I now hold a tempo well also in situations of stress. Before surgery I occasionally played too fast under stress. Since the operation I have more musical means and ideas at my disposal. It especially struck me that I now play in the romantic style and in the harmonics of the 19th century. I also observed a better adaptation to a colleague in four-handed play. Before surgery I solely relied on playing literature in the church service; now I dare to try larger improvisations during the beginning of the service, at the, or during the administration of the, Communion. The members of the choir perceive me as markedly more spirited. One person told me that I have downright exploded after surgery. I noticed I could speak easier and more spontaneously since having surgery. 4.2. Patient 2 4.2.1. Vocational career I started to learn the trumpet at the age of 11 years. I started my training as a military musician when I was 15 and, after two and a half years, took up a position as a trumpet player in a regimental band. On completion of my military service I started to study brass instrumental pedagogy at the Dortmund Department of the Academy of Music in Detmold. My compulsory second instrument was the piano. I completed my studies with top grades in the main subjects. Since 1980, after my
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military service, I have been working as a music teacher and freelance musician. 4.2.2. Status before surgery The trembling of my fingers stopped after the reduction of valproic acid during the preoperative examinations. This had become a great hindrance to my trumpet playing. Apart from this I had no great difficulties in my musical career. 4.2.3. Status after surgery My musical capability has remained mostly unchanged, but I can work more intensively because of the higher level of concentration and endurance. I consider, e.g., dissonances in the music of George Gershwin as ‘‘harmless;’’ this is different to the works of Schostakovitsch, Orff, Stravinsky and company. I find dissonances slightly ‘‘unpleasant’’; with harmony there is no change. The differences between dissonance and consonance were always very clear to me, and I do not think that this has changed. Chords and intervals that are out of tune sometimes make me start a little; the same thing happens with sudden loud noise! This was not so intensive earlier. Since my operation, I have been able to work much more. I play lead trumpet in the music school symphony orchestra and I am the co-conductor of the school brass band. I receive a lot of recognition from the music school director and my colleagues, but, unfortunately, this has no influence on my income! 4.3. Patient 3 4.3.1. Vocational career Artistic final examination (organ) and musical pedagogic examination (piano, organ). Instruments: piano, organ, cembalo, harp (after surgery a little trombone). During my studies (part-time) and afterwards (full-time) I was employed as a teacher in a music school (piano, organ, harp, theory; later also in the education of handicapped children). Avocations: church music since the age of 12; numerous national and international concerts (abroad only rarely before the surgery). 4.3.2. Status before surgery My antiepileptic medication had been extremely high over the previous twenty years, particularly during the preoperative period when pharmocoresistance was tested to the limits of toxicity with the hope of avoiding surgery. On Good Friday 1991 I played an entire concert nearly blind or one-eyed because I was not able to see a single note, the staffs or a line of the text sharply. 4.3.3. Status after surgery My general memory showed huge problems in the first one and a half years after surgery. The capacity
to memorize new information was very limited; most appointments were noted in written form to avoid lapses. Memory considerably improved in the years to come. However, I still write down all necessary notes in a weekly calendar. My musical abilities did not change after the surgery. The growing number of concerts also on the stage demanded learning numerous new piano pieces. I also had to learn many new organ pieces before surgery, e.g., to perform new literature in my own series of concerts (presently amounting to a total of 262 concerts). Postoperative reduction of medication (phenytoin, phenobarbital) resulted in frequent sleeplessness (even today I sleep only four to five hours a night). In addition it was a very difficult time for me emotionally because I reduced the medication without the knowledge of my physician, and because of marriage problems (which had been predicted before surgery). Third, there were the long desired positive consequences of unrestricted professional performance, of an autonomous and self-determined life (I often felt as if I were kept under surveillance over the last seven years before surgery) and of the feeling of again being completely accepted by my colleagues and friends (even though some colleagues had not noticed my disease at all). The feeling of a cured disease increased my self-esteem in spite of the still present fear of seizure relapses over years to come and resulted in increased courage to start and carry through unusual projects like the recording of CDs, writing of books, composing, giving lectures, and new activities in the special education of handicapped children. Consequently, my vocational orientation has become different. I frequently stage concerts in locations throughout Germany because I am now allowed to drive a car. I am well accepted as a soloist now and I have received a lot of respect for the publication of my books on special education in piano and of piano courses for handicapped children.
5. Discussion The complexity of cognitive and motor abilities in making music and the fear of small, but in these cases essential, postoperative deficits make the decision for epilepsy surgery on professional musicians more difficult. Our three case reports, however, show excellent results with respect to seizure outcome and postoperative professional outcome. In the following, we discuss possible explanations for functional improvements and for the absence of deficits, including possible implications for the cerebral lateralization of musical functions. Psychosocial factors and changes in antiepileptic medication may result in postoperative functional improvements. The feeling that the disease is now cured,
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increased self-esteem, renewed acceptance among colleagues, and the loss of limitations can boost professional performance. On the other hand, the self-awareness of deficits may be deceiving, as shown in a study of selfawareness of memory in patients with right or left hemisphere epilepsy. Patients with right hemisphere epilepsy tended to overestimate their memory abilities [13]. However, our three patients reported long-lasting effects on their career, with increased activities and responsibilities. Mere emotional effects would not have been so sustained, nor acknowledged by superiors and audience, and followed by professional promotion. All three patients reported marked side effects of the antiepileptic drugs. However, postoperative improvements are probably not due to changes in the medication. Patient 2, a trumpeter, is still on lamotrigine and levetiracetam. He lost a marked tremor when valproate was stopped prior to surgery. Beginning the drug reduction 2 years after surgery, patient 1 felt an increased vigilance after every step of carbamazepine withdrawal and after complete cessation of drugs. Patient 3 was handicapped by toxic side effects of a combination of phenytoin and phenobarbital before surgery. From 8 months to 3 years after surgery, he experienced marked effects of drug withdrawal when, step-by-step, he reduced and finally discontinued his medication. In summary, all three musicians reported positive effects of the surgery on their professional lives while under constant medication, and patient 3 also later, despite difficult social adaptation and the effects of drug withdrawal. Long-lasting improvements are sometimes ascribed to the functional recovery of adjoining cortical regions, which are often depressed in temporal lobe epilepsy, with the consequence of worse cognitive functions [14]. Cerebral functions may lie or shift outside the zone of the lesion and the surrounding zones of the epileptogenic or irritative cortex [15]. Cortical functions that enable musical abilities might even be located widespread over the brain and represented in both hemispheres. In imaging [16] or MEG [17] studies, several ipsilateral regions and the contralateral hemisphere are usually involved, with varying predominance. Some studies especially emphasize the involvement of both hemispheres (interval [11], rhythm, and meter). In a direct current EEG study, Kuck and co-workers suggested that, in rhythm and meter, findings of right frontotemporal predominance reflect the auditory working memory and a pattern recognition module [18]. Zatorre observed worse discrimination of single-note changes in unfamiliar tonal melodies after excision of either the left or right primary auditory cortex (worse after rightsided excision) [19]. In split-brain studies, the right hemisphere is superior in correct identification of completely identical stimuli, suggesting a more elementary processing, whereas the left hemisphere is capable of mental manipulation,
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imagination, and storage of inferences [20,21]. One could speculate that the laypersonÕs listening to music is represented predominately by activities in the right hemisphere, whereas the professional making of music is also solidly based in the left hemisphere. Changes in brain anatomy in professional musicians are well known [22]. Because professional musicians rely on both hemispheres, their abilities might be more robust in response to epilepsy surgery than often feared. In addition to the general professional improvements in all three cases, only patients 1 and 2, who had right temporal lobe resections, reported better function in specific musical abilities like perception of rhythm, meter, dissonance, timbre, as well as emotionality, adaptation to other musicians, concentration, learning, and endurance. Except for rhythm, these functions are attributed mostly to the right hemisphere or the frontal lobes. When one considers a right temporal resection, the improvement or preservation of right hemisphere musical abilities must be attributed to the location of these functions in other parts of the right hemisphere or in the left hemisphere. The concept of location of musical functions in large regions of the right hemisphere is supported by the case of a trained musician with receptive amelodia who had a hemodynamically significant stenosis of the right intracarotid artery [23]. Two other case reports showed conflicting results. One composer suffered a left hemisphere stroke with speech difficulties but was able to compose a brilliant symphony [24]. The other composer experienced speech difficulties and was unable to compose because of a benign brain tumor [25]. The stability, but lack of improvement, of specific musical functions in patient 3, who had a left temporal resection, could be attributed to a partial representation of specific musical functions within the left temporal lobe or to involvement of left temporal neural circuits. On the other hand, patient 3 showed robust and astonishing professional development, which suggests a widespread cerebral representation of making music. Interestingly, his verbal memory subjectively declined after surgery in contrast to the estimation of his musical memory (with neuropsychological testing, no significant changes were observed; re-test effects, however, might overestimate postoperative memory functions). Our three cases suggest that epilepsy surgery in professional musicians is safe and rewarding. However, the decision to perform epilepsy surgery in musicians should not be based only on case reports. We propose initiating a database of cases of epilepsy surgery in this special group of patients that integrates the spectrum of musical skills as well as different etiologies and localizations of focal epilepsies. The musiciansÕ own experiences and insights might be especially helpful in identifying special risks and in collecting information about the cortical representation of making music.
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Acknowledgments Johannes Vetter, organist and church music director in Bethel, was very helpful during the first steps of this project. The authors also thank Terri Shore Ebner, who, as a native English speaker, revised the article.
References [1] Avanzini G, Faienza C, Minciacchi D, Lopez L, Majno M, editors. Neurosciences and music. Ann NY Acad Sci 2003;999. [2] Peretz I. Music perception and recognition. In: Rapp B, editor. The handbook of cognitive neuropsychology: what deficits reveal about the human mind. Philadelphia: Psychology Press; 2001. p. 519–40. [3] Halpern AR. Cerebral substrates of musical imagery. Ann NY Acad Sci 2001;930:179–92. [4] Zatorre RJ, Halpern AR. Effect of unilateral temporal-lobe excision on perception and imagery of songs. Neuropsychologia 1993;31:221–32. [5] Halpern AR, Zatorre RJ. When that tune runs through your head: a PET investigation of auditory imagery for familiar melodies. Cereb Cortex 1999;9:697–704. [6] Halpern AR, Zatorre RJ, Bouffard M, Johnson JA. Behavioral and neural correlates of perceived and imagined musical timbre. Neuropsychologia 2004;42:1281–92. [7] Samson S, Zatorre RJ. Melodic and harmonic discrimination following unilateral cerebral excision. Brain Cogn 1988;7:348–60. [8] Ibbotson NR, Morton J. Rhythm and dominance. Cognition 1981;9:125–38. [9] Blood AJ, Zatorre RJ, Bermudez P, Evans AC. Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat Neurosci 1999;2:382–7. [10] Wieser HG. Temporal lobe or psychomotor status epilepticus: a case report. Electroencephalogr Clin Neurophysiol 1980;48:558–72. [11] Lie´gois-Chauvel C, Peretz I, Babai M, Laguitton V, Chauvel P. Contribution of different cortical areas in the temporal lobes to music processing. Brain 1998;121:1853–67.
[12] Peretz I, Champod AS, Hyde K. Varieties of musical disorders: the Montreal Battery of Evaluation of Amusia. Ann NY Acad Sci 2001;930:58–75. [13] Andelman F, Zuckerman-Feldhay E, Hoffien D, Fried I, Neufeld MY. Lateralization of deficit in self-awareness of memory in patients with intractable epilepsy. Epilepsia 2004;45:826–33. [14] Jokeit H, Seitz RJ, Markowitsch HJ, Neumann N, Witte OW, Ebner A. Prefrontal asymmetric interictal glucose hypometabolism and cognitive impairment in patients with temporal lobe epilepsy. Brain 1997;120:2283–94. [15] Rosenow F, Lu¨ders HO. Overview. In: Rosenow F, Lu¨ders HO, editors. Presurgical assessment of the epilepsies with clinical neurophysiology and functional imaging. In: Daube JF, Mauguie`re F, editors. Handbook of clinical neurophysiology. Amsterdam: Elsevier; 2004. Vol. 3, p 3–7. [16] Zatorre RJ, Belin P. Spectral and temporal processing in human auditory cortex. Cereb Cortex 2001;11:946–53. [17] Schurmann M, Raij T, Fujiki N, Hari R. MindÕs ear in a musician: where and when in the brain. Neuroimage 2002;16:434–40. [18] Kuck H, Grossbach M, Bangert M, Altenmuller E. Brain processing of meter and rhythm in music. Electrophysiological evidence of a common network. Ann NY Acad Sci 2003;999:244–53. [19] Zatorre RJ. Discrimination and recognition of tonal melodies after unilateral cerebral excisions. Neuropsychologia 1985;23:31–41. [20] Metcalfe J, Funnell M, Gazzaniga MS. Right-hemisphere memory superiority: studies of a split-brain patient. Psychol Sci 1995;6:157–64. [21] Gazzaniga MS. Cerebral specialization and interhemispheric communication: Does the corpus callosum enable the human condition? Brain 2000;123:1293–326. [22] Altenmu¨ller E, Mu¨nte TF, Ja¨ncke L. The musicianÕs brain as a model of neuroplasticity. Nat Rev Neurosci 2002;3:473–8. [23] Sparr SA. Receptive amelodia in a trained musician. Neurology 2002;59:1659–60. [24] Luria AR, Tsvetkova LS, Futer DS. Aphasia in a composer (V.G. Shebalin). J Neurol Sci 1965;2:288–92. [25] Critchley M. Aphasiology and other aspects of language. London: Edward Arnold; 1970. p. 256–276.
Case Report
Epilepsy surgery in professional musicians: Subjective and objective reports of three cases Reinhard Schulz a,*, Simone Horstmann a, Hennric Jokeit b, Friedrich G. Woermann a, Alois Ebner a,* b
a Epilepsy Centre Bethel, Maraweg 21, D-33617 Bielefeld, Germany Swiss Epilepsy Centre, Bleulerstrasse 60, CH-8008 Zu¨rich, Switzerland
Received 3 May 2005; revised 12 July 2005; accepted 14 July 2005 Available online 6 September 2005
Abstract We describe a small series of three professional musicians who had right (two patients) and left (one patient) temporal lobe epilepsy surgery with the histological diagnoses of hippocampal sclerosis (two patients) and benign tumor (one patient, xanthoastrocytoma). The musicians were asked to complete a questionnaire about their musical abilities before and after surgery with respect to special musical skills like melody processing, musical memory, rhythm, meter, harmony/dissonance, timbre, concentration and endurance, emotionality, and absolute pitch. In addition, the musicians submitted reports of their experiences. Surgical outcome was excellent with respect to seizures and professional skills. The two patients with right temporal lobe epilepsy reported improvements of specific musical abilities. Vocational development was very positive in all three patients. We conclude that epilepsy surgery can be safe and rewarding in professional musicians and propose initiating a database on epilepsy surgery in this special group of patients. 2005 Elsevier Inc. All rights reserved. Keywords: Temporal lobe epilepsy; Epilepsy surgery; Music; Rehabilitation; Cerebral specialization
1. Introduction Musical abilities have been thoroughly studied in healthy subjects and in patients with epilepsy [1,2]. Epilepsy surgery offers interesting opportunities to investigate the effects of circumscribed lesions on musical performance and to draw hypotheses about the cerebral representation of various aspects of music [3]. The cortical representation of musical functions might be the reason for positive or negative changes after epilepsy surgery. A number of clinical studies attribute the majority of musical functions predominantly to the right hemisphere, but some functions to the left hemisphere: *
Corresponding authors. Fax: + 49 521 144 4562. E-mail addresses: [email protected] (R. Schulz), Alois. [email protected] (A. Ebner). 1525-5050/$ - see front matter 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2005.07.009
estimation of pitch (right temporal superior gyrus) [4], imagination of music (right temporal, right and left frontal) [5], timbre (right-sided asymmetry) [6], melody (right temporal, right frontotemporal, less left frontal) [7], meter (right hemisphere) [8], rhythm (left hemisphere) [8], dissonance (right temporal) and harmony (orbitofrontal) [9], hallucination of a known song with emotional links to the biography (right auditory cortex, spread to right mesiobasal temporal lobe structures) [10], contour (right temporal) and interval (right and left temporal) as parts of melody processing [11]. To our knowledge, the outcomes of epilepsy surgery in professional musicians has not been reported in the literature up to now. Self-awareness of professional deficits in this group of patients is expected to be highly elaborated and to exceed traditional neuropsychological evaluation as well as the recently developed test battery
Case Report / Epilepsy & Behavior 7 (2005) 552–558
of amusias (Montreal Battery of the Evaluation of Amusias: MBEA) [12]. Neuropsychological tests of musical abilities focus on deficits rather than talents and are not suitable for professional musicians. We present the cases of three musicians who had surgery for temporal lobe epilepsy and concentrate on the musiciansÕ self-assessment of their postoperative professional outcome.
2. Patients and methods Four professional musicians have been operated on because of medically refractory temporal lobe epilepsy during the course of the Bethel epilepsy surgery program since 1990 (in a total of about 1000 operations until April 2003). All four became seizure free (postoperative classification: Engel 1a). One of them, a musical teacher, despite being very satisfied with the results of his surgery, chose not to participate in this study.
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The remaining three musicians (two organists, one trumpeter) completed a questionnaire. First, they were asked to judge postoperative changes (better, worse, no change) in the following abilities while making music: memory, concentration, learning, endurance; apperception of absolute pitch (if present), harmony, dissonance, timbre, melody, rhythm, meter, emotion, interaction in making music with others or in an orchestra, e.g., with respect to their own adjustment or sensitivity to mistakes of other musicians; professional development before and after surgery; effects of medication. Second, the musicians were asked to write a free report about their professional training and expertise and pre- and postsurgical experiences with epilepsy and their profession. The neuropsychological evaluation included the Wechsler Adult Intelligence Scale—Revised (verbal and nonverbal subtests) assessing intellectual abilities, the Wechsler Memory Scale—Revised (subtest: Logical Memory) and the California Verbal Learning Test
Fig. 1. Functional MRI activation map of reading music and sound imagery in patient 1 (1.5-T scanner, blocked design, rest condition text reading and ideation, z > 4). Reading musical notation and translating this notation into musical sound imagery activate a bilateral network involving areas within the diseased right temporal lobe (right superior temporal gyrus, right temporal basal posterior; activation indicated by arrows, extent of the lesion indicated by a bar). Later, the patient was successfully treated for his refractory TLE with a right-sided anterior temporal lobe resection including the tumor. After surgery he did not notice a substantial change in reading music and sound imagery.
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assessing verbal memory functions, and the Rey Complex Figure Test and Rey Visual Design Learning Test assessing visual memory functions. We classified ability into the following categories (according to standard deviations): deficient (D) < 2; below average (BA) = 3– 15; low average (LA) = 16–33; average (A) = 34–68; high average (HA) = 69–84; above average = 85–98 (AA); superior (S) > 98. An intracarotid amobarbital (Wada) test was performed in two patients (patients 1 and 2). Functional MRI of reading music and sound imagery was performed in patient 1 (1.5 T scanner, blocked design, rest condition text reading and ideation) (Fig. 1). The follow-up on an inpatient schedule included neuropsychologic reevaluation, rehabilitation interviews, and neurologic examinations 6 months and 2 years after surgery. Outpatient, telephone, and e-mail contacts were added when necessary.
The musiciansÕ self-assessments of their musical abilities with respect to memory, concentration, learning, endurance, apperception of absolute pitch, harmony, dissonance, timbre, melody, rhythm, meter, emotion, and interaction with others in making music revealed the following: In patient 1, concentration, learning (slight changes), timbre, meter, emotionality, and adaptation in making music with others improved. In patient 2, concentration, learning (slight changes), endurance (slight changes), dissonance, and rhythm improved. Patient 3 did not report any changes. None of the three patients reported a deterioration of musical abilities. Developments in their careers before and after surgery and effects of antiepileptic medications are listed in Table 2. The musiciansÕ own reports follow.
4. Case reports 3. Results
4.1. Patient 1
The general history of the epilepsy and the results of diagnostic testing are summarized in Table 1. Neuropsychologic tests demonstrated improvement of at least one standard deviation in patient 2 (nonverbal intellectual ability from LA to A, verbal learning/memory from LA to AA, nonverbal learning/memory from BA to LA) and patient 3 (nonverbal intellectual ability from HA to AA). No deterioration was noted.
4.1.1. Vocational career I studied church music and piano with organ and choir music and completed the German ‘‘A-degree’’ including artistic final examination (organ) and musical pedagogic examination (piano). Since 1981 I have permanently been employed as a church musician in the same parish. The choir developed particularly well to one of the largest in the diocese with more than 100 active singers. Concerts
Table 1 General history of epilepsy and summary of diagnosis
Age at surgery Syndrome Histology Age of onset Duration of seizures
Frequency Interictal IED Ictal EEG MRI Size of resectionb
Outcome Follow-up a b c
Patient 1
Patient 2
Patient 3
45 years (10/2001) Right TLE Xanthoastrocytoma (grade 2, WHO) Auras: childhood Seizures: age 35 10 years Gustatory + abdominal aura fi psychomotor seizurea fiRarely generalized tonic–clonic seizure Several per day 98% right mesial temporal 2% right anterior temporal Right temporal
45 years (9/2001) Right mesial TLE Hippocampal sclerosis 13 years
34 years (3/1992) Left mesial TLE Hippocampal sclerosis 13 years
32 years Abdominal aura
Right anterior and lateral temporal lobe tumor 5.5 cm plus hippocampus (complete resection of tumor)
Right mesial temporal lobe sclerosis
22 years Abdominal aura (until 5 years before surgery) fi Psychomotor seizure 5 or 6/month 90% left mesial temporal 10% right mesial temporal 21/23 left mesial temporal 2/23 right mesial temporal Normal (8/1991)
Seizure free 3 years
Seizure freec 3 years
fi psychomotor seizurea One cluster/4–6 weeks 100% right mesial temporal Right temporal
3 cm plus hippocampus
Anterior temporal with anterior hippocampus and inferior part of amygdala Seizure free 12 years
In part, automatisms with preservation of responsiveness. Lateral distance from the tip of the temporal lobe, measured in the middle temporal gyrus. Two questionable events with movements and short impairment of reactivity out of sleep, without aura some months after reduction of AEDs.
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Table 2 Vocational career and antiepileptic medication Medication (a) before and (b) after surgery and (c) at present (10/2004)
Effects of medication
1
(a) CBZa 1000 mg (b) CBZ 1200 mg for 2 years (c) No medication since 2 months
Feeling of increased vigilance at every step of medication withdrawal, also after complete cessation of medication
2
(a) LEV 2000 mg, LTG 400 mg, VPA 600 mg (b) LEV 2000 mg, LTG 600 mg (c) Mono LTG since 2/04, plus LEV since 7/04
Cessation of tremor after withdrawal of VPA before surgery; LEV without effect on musical abilities (add-on of LEV because of two mild seizures in sleep or parasomnia)
3
(a) DPH 387.5 mg, PB 100 mg (b) From 8 months after surgery complete withdrawal during 22 months (c) No medication since 6 years
Marked side effects of withdrawal after each step
Patient
a
Vocational career before surgery
Vocational career after surgery
CBZ, carbamazepine; LEV, levetiracetam; LTG, lamotrigine; DPH, phenytoin; PB, phenobarbital.
(organ works and oratorios) were performed regularly and I participated in several organ festivals. 4.1.2. Status before surgery I was successful in my profession also before surgery. However, I became more and more ‘‘unreliable’’ because of a growing number of absences which also occurred during my work. At last, after a spectacular absence during a 70th wedding anniversary, I lost the ability I used to have of musical ideas turning up during walks. I did not explicitly miss this ability, but now—after surgery—speculation and playing with musical ideas while walking rhythmically returned, and in retrospect, I noticed the difference. 4.1.3. Status after surgery One year ago, I was appointed as cantor of the deanship and I am now responsible for the professional training of all my colleagues. The number of organ concerts increased, and my organ was enlarged to 50 registers. I can say that in the parish my reputation is good and the working atmosphere is excellent. When I played on the organ during the farewell service of my previous principal several weeks after my surgery, I instantly felt that my fine motor movements in running notes and trills had become more rapid, my music was more intense and emotionally more dedicated. After an interval of several weeks I was more adept at playing my instrument than before surgery. I had a different perception as an accompanist of songs. Before surgery I predominantly heard in a harmonic way, somehow ‘‘vertically’’: To each tone of the melody I mentally filled in the suitable chord. After surgery I also heard the voices of the accompanists in their melodic development, especially in the bass voice, almost as in a choir composition. This more pronounced ‘‘horizontal’’ perception of single voices made the
playing of polyphonic music (e.g., fugues) unfamiliar and in part more difficult to me. I now perceive this change as enrichment. After surgery I now hear more sensitively and sharply, especially in the higher frequencies; I hear loud sound more pronouncedly. Musical pieces which I could play by heart before surgery are still completely at my disposal. I again rely on my rhythmicity in playing the organ. I produce fewer unwanted variations in tempo. I believe that I now hold a tempo well also in situations of stress. Before surgery I occasionally played too fast under stress. Since the operation I have more musical means and ideas at my disposal. It especially struck me that I now play in the romantic style and in the harmonics of the 19th century. I also observed a better adaptation to a colleague in four-handed play. Before surgery I solely relied on playing literature in the church service; now I dare to try larger improvisations during the beginning of the service, at the, or during the administration of the, Communion. The members of the choir perceive me as markedly more spirited. One person told me that I have downright exploded after surgery. I noticed I could speak easier and more spontaneously since having surgery. 4.2. Patient 2 4.2.1. Vocational career I started to learn the trumpet at the age of 11 years. I started my training as a military musician when I was 15 and, after two and a half years, took up a position as a trumpet player in a regimental band. On completion of my military service I started to study brass instrumental pedagogy at the Dortmund Department of the Academy of Music in Detmold. My compulsory second instrument was the piano. I completed my studies with top grades in the main subjects. Since 1980, after my
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military service, I have been working as a music teacher and freelance musician. 4.2.2. Status before surgery The trembling of my fingers stopped after the reduction of valproic acid during the preoperative examinations. This had become a great hindrance to my trumpet playing. Apart from this I had no great difficulties in my musical career. 4.2.3. Status after surgery My musical capability has remained mostly unchanged, but I can work more intensively because of the higher level of concentration and endurance. I consider, e.g., dissonances in the music of George Gershwin as ‘‘harmless;’’ this is different to the works of Schostakovitsch, Orff, Stravinsky and company. I find dissonances slightly ‘‘unpleasant’’; with harmony there is no change. The differences between dissonance and consonance were always very clear to me, and I do not think that this has changed. Chords and intervals that are out of tune sometimes make me start a little; the same thing happens with sudden loud noise! This was not so intensive earlier. Since my operation, I have been able to work much more. I play lead trumpet in the music school symphony orchestra and I am the co-conductor of the school brass band. I receive a lot of recognition from the music school director and my colleagues, but, unfortunately, this has no influence on my income! 4.3. Patient 3 4.3.1. Vocational career Artistic final examination (organ) and musical pedagogic examination (piano, organ). Instruments: piano, organ, cembalo, harp (after surgery a little trombone). During my studies (part-time) and afterwards (full-time) I was employed as a teacher in a music school (piano, organ, harp, theory; later also in the education of handicapped children). Avocations: church music since the age of 12; numerous national and international concerts (abroad only rarely before the surgery). 4.3.2. Status before surgery My antiepileptic medication had been extremely high over the previous twenty years, particularly during the preoperative period when pharmocoresistance was tested to the limits of toxicity with the hope of avoiding surgery. On Good Friday 1991 I played an entire concert nearly blind or one-eyed because I was not able to see a single note, the staffs or a line of the text sharply. 4.3.3. Status after surgery My general memory showed huge problems in the first one and a half years after surgery. The capacity
to memorize new information was very limited; most appointments were noted in written form to avoid lapses. Memory considerably improved in the years to come. However, I still write down all necessary notes in a weekly calendar. My musical abilities did not change after the surgery. The growing number of concerts also on the stage demanded learning numerous new piano pieces. I also had to learn many new organ pieces before surgery, e.g., to perform new literature in my own series of concerts (presently amounting to a total of 262 concerts). Postoperative reduction of medication (phenytoin, phenobarbital) resulted in frequent sleeplessness (even today I sleep only four to five hours a night). In addition it was a very difficult time for me emotionally because I reduced the medication without the knowledge of my physician, and because of marriage problems (which had been predicted before surgery). Third, there were the long desired positive consequences of unrestricted professional performance, of an autonomous and self-determined life (I often felt as if I were kept under surveillance over the last seven years before surgery) and of the feeling of again being completely accepted by my colleagues and friends (even though some colleagues had not noticed my disease at all). The feeling of a cured disease increased my self-esteem in spite of the still present fear of seizure relapses over years to come and resulted in increased courage to start and carry through unusual projects like the recording of CDs, writing of books, composing, giving lectures, and new activities in the special education of handicapped children. Consequently, my vocational orientation has become different. I frequently stage concerts in locations throughout Germany because I am now allowed to drive a car. I am well accepted as a soloist now and I have received a lot of respect for the publication of my books on special education in piano and of piano courses for handicapped children.
5. Discussion The complexity of cognitive and motor abilities in making music and the fear of small, but in these cases essential, postoperative deficits make the decision for epilepsy surgery on professional musicians more difficult. Our three case reports, however, show excellent results with respect to seizure outcome and postoperative professional outcome. In the following, we discuss possible explanations for functional improvements and for the absence of deficits, including possible implications for the cerebral lateralization of musical functions. Psychosocial factors and changes in antiepileptic medication may result in postoperative functional improvements. The feeling that the disease is now cured,
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increased self-esteem, renewed acceptance among colleagues, and the loss of limitations can boost professional performance. On the other hand, the self-awareness of deficits may be deceiving, as shown in a study of selfawareness of memory in patients with right or left hemisphere epilepsy. Patients with right hemisphere epilepsy tended to overestimate their memory abilities [13]. However, our three patients reported long-lasting effects on their career, with increased activities and responsibilities. Mere emotional effects would not have been so sustained, nor acknowledged by superiors and audience, and followed by professional promotion. All three patients reported marked side effects of the antiepileptic drugs. However, postoperative improvements are probably not due to changes in the medication. Patient 2, a trumpeter, is still on lamotrigine and levetiracetam. He lost a marked tremor when valproate was stopped prior to surgery. Beginning the drug reduction 2 years after surgery, patient 1 felt an increased vigilance after every step of carbamazepine withdrawal and after complete cessation of drugs. Patient 3 was handicapped by toxic side effects of a combination of phenytoin and phenobarbital before surgery. From 8 months to 3 years after surgery, he experienced marked effects of drug withdrawal when, step-by-step, he reduced and finally discontinued his medication. In summary, all three musicians reported positive effects of the surgery on their professional lives while under constant medication, and patient 3 also later, despite difficult social adaptation and the effects of drug withdrawal. Long-lasting improvements are sometimes ascribed to the functional recovery of adjoining cortical regions, which are often depressed in temporal lobe epilepsy, with the consequence of worse cognitive functions [14]. Cerebral functions may lie or shift outside the zone of the lesion and the surrounding zones of the epileptogenic or irritative cortex [15]. Cortical functions that enable musical abilities might even be located widespread over the brain and represented in both hemispheres. In imaging [16] or MEG [17] studies, several ipsilateral regions and the contralateral hemisphere are usually involved, with varying predominance. Some studies especially emphasize the involvement of both hemispheres (interval [11], rhythm, and meter). In a direct current EEG study, Kuck and co-workers suggested that, in rhythm and meter, findings of right frontotemporal predominance reflect the auditory working memory and a pattern recognition module [18]. Zatorre observed worse discrimination of single-note changes in unfamiliar tonal melodies after excision of either the left or right primary auditory cortex (worse after rightsided excision) [19]. In split-brain studies, the right hemisphere is superior in correct identification of completely identical stimuli, suggesting a more elementary processing, whereas the left hemisphere is capable of mental manipulation,
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imagination, and storage of inferences [20,21]. One could speculate that the laypersonÕs listening to music is represented predominately by activities in the right hemisphere, whereas the professional making of music is also solidly based in the left hemisphere. Changes in brain anatomy in professional musicians are well known [22]. Because professional musicians rely on both hemispheres, their abilities might be more robust in response to epilepsy surgery than often feared. In addition to the general professional improvements in all three cases, only patients 1 and 2, who had right temporal lobe resections, reported better function in specific musical abilities like perception of rhythm, meter, dissonance, timbre, as well as emotionality, adaptation to other musicians, concentration, learning, and endurance. Except for rhythm, these functions are attributed mostly to the right hemisphere or the frontal lobes. When one considers a right temporal resection, the improvement or preservation of right hemisphere musical abilities must be attributed to the location of these functions in other parts of the right hemisphere or in the left hemisphere. The concept of location of musical functions in large regions of the right hemisphere is supported by the case of a trained musician with receptive amelodia who had a hemodynamically significant stenosis of the right intracarotid artery [23]. Two other case reports showed conflicting results. One composer suffered a left hemisphere stroke with speech difficulties but was able to compose a brilliant symphony [24]. The other composer experienced speech difficulties and was unable to compose because of a benign brain tumor [25]. The stability, but lack of improvement, of specific musical functions in patient 3, who had a left temporal resection, could be attributed to a partial representation of specific musical functions within the left temporal lobe or to involvement of left temporal neural circuits. On the other hand, patient 3 showed robust and astonishing professional development, which suggests a widespread cerebral representation of making music. Interestingly, his verbal memory subjectively declined after surgery in contrast to the estimation of his musical memory (with neuropsychological testing, no significant changes were observed; re-test effects, however, might overestimate postoperative memory functions). Our three cases suggest that epilepsy surgery in professional musicians is safe and rewarding. However, the decision to perform epilepsy surgery in musicians should not be based only on case reports. We propose initiating a database of cases of epilepsy surgery in this special group of patients that integrates the spectrum of musical skills as well as different etiologies and localizations of focal epilepsies. The musiciansÕ own experiences and insights might be especially helpful in identifying special risks and in collecting information about the cortical representation of making music.
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Acknowledgments Johannes Vetter, organist and church music director in Bethel, was very helpful during the first steps of this project. The authors also thank Terri Shore Ebner, who, as a native English speaker, revised the article.
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