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Clinical article
Franck-Emmanuel Roux, M.D., Ph.D.,1,2 Stefano Borsa, M.D., 2
and Jean-François Démonet, M.D., Ph.D.1,3
1
Institut National de la Santé Et de la Recherche Médicale, Unité 825; and Fédérations de
2
Neurochirurgie et 3Neurologie, Centres Hospitalo-Universitaires, Toulouse, France
Object. In an attempt to identify cortical areas involved in singing in addition to language areas, the authors used
a singing task during direct cortical mapping in 5 patients who were amateur singers and had undergone surgery for
brain tumors. The organization of the cortical areas involved in language and singing was analyzed in relation with
these surgical data.
Methods. One left-handed and 4 right-handed patients with brain tumors in left (2 cases) and right (3 cases)
hemispheres and no significant language or singing deficits underwent surgery with the “awake surgery” technique.
All patients had a special interest in singing and were involved in amateur singing activities. They were tested using
naming, reading, and singing tasks.
Results. Outside primary sensorimotor areas, singing interferences were rare and were exclusively localized in
small cortical areas (< 1 cm2). A clear distinction was found between speech and singing in the Broca region. In the
Broca region, no singing interference was found in areas in which interference in naming and reading tasks were
detected. Conversely, a specific singing interference was found in nondominant middle frontal gyri in one patient.
This interference consisted of abrupt singing arrest without apparent face, mouth, and tongue contraction. Finally,
nonspecific singing interferences were found in the right and left precentral gyri in all patients (probably by interfer-
ence in final articulatory mechanisms of singing).
Conclusions. Dissociations between speech and singing found outside primary sensorimotor areas showed that
these 2 functions use, in some cortical stages, different cerebral pathways. (DOI: 10.3171/2007.9.17565)
I
n 1745, Olof Dalin, a Swedish literacy figure of his other regions, the right frontal lobe plays a major role in
time, reported the case of a farmer, Jan Person, who singing.23
suddenly suffered from a right hemiparesis. What at- We routinely use direct brain mapping in patients
tracted Dalin’s attention was that Person, who completely with brain tumors to identify language cortical areas.
lost his ability to speak was still able to sing (certain re- Some of the patients treated in our institution were ama-
ligious hymns for instance), leading to the probably first teur musicians. Although infrequent, some of them were
known striking observation of, as Dalin quoted, “a mute involved in singing activities such as choral or folk sing-
who can sing.”26 Similar cases of aphasia and relatively ing. To identify cortical areas involved in singing in addi-
preserved singing were subsequently described by other tion to language areas, we studied these patients by using
authors,2,8,11,14,16,19,29,34 leading to consideration that speech standard language tasks and a singing task during direct
and song could have distinct cerebral representations.12,13 cortical mapping. Because amateur musicians involved in
Given that many of these reports concerned patients with singing and who must undergo a neurosurgical procedure
no special music training, this hypothesis would reflect and brain mapping are very rare, data from these succes-
a general feature of brain organization. The introduc- sive brain mappings were prospectively collected by the
tion of noninvasive brain mapping tools has permitted same team using the same protocol during a period of 10
the study of the cerebral areas activated in response to years. To the best of our knowledge, singing has never
singing.3,23,24,27,30,33 It has been hypothesized that, among been systematically studied in a group of patients by di-
rect cortical stimulation. The organization of the cortical
areas, involved in language and singing respectively, was
Abbreviation used in this paper: fMR = functional MR. analyzed in relation to the surgical data.
Fig. 1. Schematic representation of the localization of the singing interference and language (naming and reading tasks) found
in the left and right hemispheres in our 5 patients. The dotted line denotes the area of craniotomy. The numbers in the upper left
of each panel denote the case number. F1 = superior frontal gyrus; F2 = middle frontal gyrus; F3 = inferior frontal gyrus; T1 =
superior temporal gyrus.
were common with other language (naming or reading) terference found in this gyrus in our patients were abrupt
interferences. Within precentral gyrus, singing interfer- “speech arrest” (patient stopped naming or reading). In
ences were located preferentially close to the rolandic these 2 right-handed patients, no singing interference was
sulcus. Almost all singing interferences detected in pre- found when stimulating either naming or reading interfer
central gyri were abrupt singing arrests (probably due to ence areas or other parts of the cortex. Singing was not
“articulatory” interference), sometimes with visible face affected by stimulation of the Broca region (Fig. 2). Even
or mouth contraction. Although less visible, contraction during stimulation of the opercular ramus where “speech
or impairment of the tongue or the vocal folds due to arrest” phenomena were frequent, patients kept singing
stimulation could be suspected to explain these singing without any perturbation.
interferences. We did not find specific effects stimulating
the left versus right precentral gyri except in the patient in Stimulation of the Right Hemisphere (Outside Pre- and
Case 5 in whom stimulation of one area within the right Postcentral Gyri)
precentral gyrus induced a singing impairment consisting Three patients (Cases 3, 4, and 5) had their right
of a lack of melodic contours leading to monotonous sing- hemisphere studied. Two were right-handed and the other
ing. Stimulation of this area also affected speech prosody was left-handed (Case 5). Naming and reading interfer-
during naming and reading tasks. ence were found once in the supramarginal gyrus in a
common area in left-handed patient. No other naming or
Stimulation of the Left Hemipshere (Outside Pre- and reading interferences were detected in frontal gyri in the
Postcentral Gyri)
patients in Cases 3 and 4. Repetitive singing interference
Interference sites related to naming and reading tasks was detected in the patient in Case 3 during stimulation
were found in 2 patients whose left hemisphere was stud- of 2 small areas in the middle frontal gyrus (Fig. 3). The
ied (Cases 1 and 2). In the Broca region, we found 2 nam- patient stopped singing abruptly after the electrode stim-
ing or reading interference sites in one patient and 3 in the ulated the cortex. Within the middle frontal gyrus, this
other. Four more language sites were found in the patient interference was extremely localized. The patient became
in Case 1 in the supramarginal and superior temporal gy silent, and no word or melody was heard. We are cautious
ri. These sites were extremely localized (1 cm2), either in analyzing the intrinsic mechanisms producing such
affecting both reading as well as naming interference singing interference. We did not notice any face, mouth,
or task-specific (reading or naming interference). Often, or tongue contraction. No seizure was detected and there
when testing the opercular ramus, naming and reading in- were no electrocorticographic spikes. In the other 2 pa-
Fig. 2. Case 1. Illustration of preserved singing during direct brain mapping in the Broca area and the supramarginal gyrus
where speech was impaired. The bilingual right-handed French/Rwandan 37-year-old patient had a low-grade astrocytoma in
the postcentral gyrus for which he had previously undergone surgery at another institution. Although the patient spoke rather
slowly, no preoperative language impairment was noted. A and B: Intraoperative images showing naming mappings in French
and Rwandan. Naming interferences (L) in both languages were found in common (Broca region) or distinct areas (supramarginal
gyrus). To improve the understanding of the intraoperative pictures, cortical sites that did not produce a naming impairment were
not systematically labeled by a sterile ticket. The blue thread indicates the rolandic sulcus. Naming “motor” interferences were
found in primary sensorimotor areas. C: Intraoperative photograph showing singing mapping in French and Rwandan. No
singing interference was found (N) in the regions (supramarginal and opercular ramus) where the patient had a typical “speech
arrest” during naming and reading tasks. Singing interference was only found in the primary sensorimotor area. D: Diagram
showing the French and Rwandan naming and singing interference found in this patient. Outside the sensorimotor areas, no
singing interference was detected.
tients, no singing interference was detected in supramar- the capacity to sing precedes the capacity to speak. The
ginal, nondominant middle or inferior frontal gyrus. ability to sing can be a basic music function but also a
very elaborate one, using all the musical capabilities as
professional opera singers who are able to read scores and
Discussion translate them into melodies.
Among the human music abilities, singing is one
of the oldest, individualized in the most ancient Meso- The Striking Independence Between Speech and Singing in
potamian texts of antiquity.17 However, singing is not Patients With Brain Lesions
specifically a human function because the same type of Several reports have underlined the striking possi-
pitch and rhythm modulations in vocal production, im- bility of a functional independence between speech and
plying that interindividual communication exists in other singing in patients with brain lesions in their left hemi-
species and especially in birds.28 The brain substrates of sphere.4,10,29,34 The classic interpretation of these dissocia-
singing in birds is bilaterally organized, each hemisphere tions between speech and song in aphasic patients is that
contributing in a specific way to produce coordinated out- singing, a particular form of automatized speech (like
put.28 According to researchers such as Darwin6 and Jes- prayers, lists of the days of the week or months), would
persen,15 singing has been linked to the origins of speech; depend on the right hemisphere. Contrary to “proposi-
Fig. 3. Case 3. Example of impaired singing in the right hemisphere in a right-handed 70-year-old patient with a metastasis
close the right precentral gyrus. Two specific singing interferences (S) were found in the nondominant middle frontal gyrus. No
naming or reading interference were found in this region. A: Three-dimensional intraoperative reconstructions of the patient’s
brain with brain mapping findings. B: Corresponding intraoperative picture. The black line indicates the rolandic sulcus. C
and D: Photographs of the patient’s face during singing interference. Once stimulation was applied in nondominant middle frontal
gyrus, the patient stopped singing suddenly. Note that there is no contraction of the face, lips, or tongue. F = face motor areas
within the precentral gyrus; H = hand areas (contraction of the fingers during stimulation of these 2 areas); P = face or hand
paresthesia areas found in the postcentral gyrus.
tional” speech, over-learned songs (and other kinds of au- was a center for singing in the pars triangularis of the Broca
tomatic speech) could also rely on subcortical networks area, arguing that the cases that seemed to point to a local-
in the left hemisphere. ization of singing in the right hemisphere did not provide
The occasional differential impairment between conclusive evidence. He conceded that in the cases in which
speech and singing is a puzzling phenomenon. In 1898, the so-called left-sided center for singing had been destroyed,
Mann20 reported the case of a nonaphasic patient who was the right hemisphere could take over its function. More re-
a good singer and lost his capacity to sing as well as to cently, Calvin and Ojemann5 reported the case of a man,
whistle after excision of a right middle frontal gyrus cyst. whose hobby was singing folk songs, who had a hemorrhage
Jossman16 described a trained musician who could not in the anterior part of left superior temporal gyrus. This man
sing (or read a score) after right carotid artery ligation, whose speech was pretty good, could not sing at all (“neither
although he was not aphasic. Kleist18 reported the case tune nor words came even for his old favorite”).
of a right-handed man with a wound in the lower end of
the right middle frontal gyrus whose singing ability was Studies on Singing Function
partially impaired. Interestingly, when this right frontal
scar was frozen by ethyl chloride he was not able to sing Although studies on singing functions are rather
at all. Alexander et al.1 observed impaired singing follow- scarce,3,23,30,33 recent research seems to indicate the pref-
ing damage to the internal capsule of the nondominant erential involvement of the right hemisphere in singing.7
hemisphere. Finally, among 24 patients with Broca apha- Using transmagnetic cranial stimulations in 5 right-hand-
sia and severely impaired speech output, Yamadori et al.34 ed individuals, Stewart et al.30 showed that although stim-
reported that 21 could sing with words (6 excellently). All ulations over some sites of the left frontal lobe disturbed
these clinical observations seem to indicate that singing speech, patients could sing with words without problem.
critically depends on right-hemisphere structures. Studying singing with PET in 13 right-handed individu-
Nonetheless, this right hemisphere predominance in als, Perry et al.23 found 2 distinct peaks of activation in
singing has been contested. Henschen13 believed that there the right insula and precentral gyrus during singing. They
ans AC: Localization of cerebral activity during simple sing- ping as the routine surgical approach to treating patients with
ing. Neuroreport 10:3979–3984, 1999 supratentorial intraaxial tumors: a prospective trial of 200
24. Popp AJ: Music, musicians, and the brain: an exploration of cases. J Neurosurg 90:35–41, 1999
musical genius. J Neurosurg 101:895–903, 2004 32. Wildgruber D, Ackerman H, Klose U, Kardatzki B, Grodd W:
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Toga AW: Variability of intraoperative electrocortical stimu- tor cortex: a fMRI study. Neuroreport 7:2791–2795, 1996
lation mapping parameters across and within individuals. J 33. Wildgruber D, Riecker A, Hertrich I, Erb M, Grodd W, Ethofer
Neurosurg 101:458–466, 2004 T, et al: Identification of emotional intonation evaluated by
26. Prins R, Bastiaanse R: The early history of aphasiology: from fMRI. Neuroimage 24:1233–1241, 2005
the Egyptian surgeons (c. 1700 bc) to Broca (1861). Aphasiol- 34. Yamadori A, Osumi Y, Masuhara S, Okubo M: Preservation
ogy 20:762–791, 2006 of singing in Broca’s aphasia. J Neurol Neurosurg Psychia-
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28. Schmidt MF, Ashmore RC, Vu ET: Bilateral control and in-
terhemispheric coordination in the avian song motor system. Manuscript submitted May 14, 2007.
Ann N Y Acad Sci 1016:171–186, 2004 Accepted September 4, 2007.
29. Smith A: Speech and other functions after left hemispherec- Please include this information when citing this paper: published
tomy. J Neurol Neurosurg Psychiatry 29:467–471, 1966 online September 26, 2008; DOI: 10.3171/2007.9.17565.
30. Stewart L, Walsh V, Frith U, Rothwell J: Transcranial magnetic Address correspondence to: Franck-Emmanuel Roux, M.D.,
stimulation produces speech arrest but not song arrest. Ann N Ph.D., Institut National de la Santé Et de la Recherche Médicale 825
Y Acad Sci 930:433–435, 2001 et Service de Neurochirurgie, Hôpital Purpan, F-31059 Toulouse,
31. Taylor MD, Bernstein M: Awake craniotomy with brain map- France. email: franck.roux@club-internet.fr.