"When the feeling’s gone": a selective loss of musical emotion
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《神经病学神经外科学杂志》
1 Auditory Group, University of Newcastle Medical School, Newcastle-upon-Tyne, UK
2 Wellcome Department of Imaging Neuroscience, Institute of Neurology, Queen Square, London, UK
3 Department of Speech, University of Newcastle, Newcastle-upon-Tyne, UK
Correspondence to:
T D Griffiths
Auditory Group, University of Newcastle Medical School, Framlington Place, Newcastle-upon-Tyne NE2 4HH, UK; t.d.griffiths@ncl.ac.uk
Keywords: music; emotion; amusia
Loss of "feeling" is a common lament in popular music:
Tragedy: when the feeling’s gone and you can’t go on (Tragedy as performed by the Bee Gees. Spirits have flown, 1979.)
Here we describe loss of the feeling or emotion produced by music itself. Musical emotion can be considered at a number of levels. At the most fundamental level, dissonance produces a perception that is unpleasant to most listeners.1 More variable is the intense pleasure that certain music may evoke in particular listeners, often described as a "shiver down the spine" or "chills",2 which is likely to represent a more complex aesthetic response. We describe a patient with selective loss of this emotional response to music, due to a focal brain lesion.
A 52 year old right handed radio announcer collapsed in February 2000. He was found afterwards to have a total loss of speech comprehension and output, and a right hemiplegia. His speech recovered well, such that 12 months after the event he had only subtle output phonological problems. Motor functions recovered completely and he had no residual lateralising motor signs. However, he reported a persistent alteration in his auditory experience. He was in the habit of listening to classical music, to relax after working his night shift at the radio station, and had derived particular pleasure from listening to Rachmaninov preludes. He experienced an intense, altered emotional state or "transformation" when he did this. In common with other subjects who have this experience, the transformation was only produced by particular pieces, and he did not describe such an experience in response to music other than Rachmaninov’s, nor to other sensory experiences. This emotional response to the music was lost following the acute event, and remained absent during the period of testing between 12 and 18 months after the stroke. During this period he was able to enjoy other aspects of life, and reported no biological features of depression. He had noticed no change in his hearing, and was still able to identify speech, music, and environmental sounds normally.
When assessed in April 2001, pure tone audiometry, auditory filter widths,3 speech audiometry, prosody perception,4 and music perception were all normal. Musical perception was examined using a battery of tests during which subjects are required to make same/different judgments on melody pairs that can show differences in melodic structure, rhythm, and metre.5 Our patient showed normal scores on tests of scale (28/30), contour (27/30), interval (28/30), rhythm (28/30), metre (29/30), and incidental memory (27/30); see http://www.fas.umontreal.ca/psy/GRPLABS/lnmcg/website/index.html for normative data. Structural MRI revealed infarction involving the left insula and extending anteriorly into the left frontal lobe and inferiorly into the left amygdala. After normalisation to the standard stereotactic space of Talairach, the infarcted areas showed a close correspondence with left hemisphere areas activated during emotional response to music in normal subjects2 (fig 1).
Figure 1 (A) Structural T1 weighted MRI sections of the patient’s brain in the coronal (left) and axial (right) planes, showing infarction involving the left insula (black arrows) and amygdala (white arrows). (B) Coronal (left) and sagittal (right) T1 structural sections have been used to demonstrate the correspondence between the left insula lesion in our patient and the left insula activation associated with "chills" in response to music in normal subjects.2 Grey crosses showing the location of peak activation in the left insula of normal subjects have been superimposed on the patient’s structural brain volume. The images from the patient were normalised to the common stereotactic space of Talairach used in the previous functional imaging experiment2 to allow this comparison. The correspondence indicates that the left insula is necessary for a strong emotional response to music.
In a case such as this it is impossible to prove that the stroke produced a new deficit in the emotional reaction to music without direct evidence of the emotional reaction and its autonomic effect both before and after the stroke. The interest of this investigation accrues from the subjective report of the patient alone. Nevertheless, this is the first documented case of such a deficit of which we are aware, completing an important double dissociation between musical cognition and emotional processing. Such a dissociation would require the presence of distinct substrates for musical cognition and emotion.
The cerebral basis for musical emotion has only recently been the subject of systematic study. In the clinical literature, an impaired emotional response to music is generally accompanied by disordered musical perception (amusia). However, one previously reported patient6 had impaired recognition of music despite a preserved affective response. In contrast, our patient strikingly illustrates the reverse dissociation, with normal recognition of music but loss of the emotional response to music. Together, these two cases complete a double dissociation between the perceptual and emotional components of music processing. This double dissociation suggests that the emotional effect of a piece of music is not predetermined by simple acoustic properties (which were processed normally in our patient).
Accumulating evidence from functional brain imaging studies in normal individuals suggests that functionally and anatomically separable neural networks mediate music perception and emotion. The perception of music involves the superior temporal lobes and inferior frontal lobes.7,8 In contrast, emotional processing of music engages a distributed brain network that is also recruited by other powerful emotional stimuli that produce autonomic arousal. This network includes bilateral medial limbic structures, insula, ventral striatum, thalamus, midbrain, and widespread neocortical regions.1,2 The present study enables us to conclude that the left insula is involved in normal musical emotional processing of music.
ACKNOWLEDGEMENTS
We thank R Zatorre and I Peretz for helpful discussion, and C Mandell for structural MR brain imaging.
References
Blood AJ, Zatorre RJ, Bermudez P, et al. Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat Neurosci 1999;2:382–7.
Blood AJ, Zatorre R. Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc Natl Acad Sci U S A 2001;98:11818–23.
Patterson RD, Moore BCJ. Auditory filters and excitation patterns as representations of frequency resolution. In: Moore BCJ, ed. Frequency selectivity in hearing. London: Academic Press, 1986.
Patel AD, Peretz I, Tramo M, et al. Processing prosodic and musical patterns: a neuropsychological investigation. Brain Lang 1998;61:123–44.
Peretz I, Champod A- S, Hyde KL. Varieties of musical disorders. The Montreal Battery of Evaluation of Amusia. Ann NY Acad Sci (in press).
Peretz I, Cagnon L, Bouchard B. Music and emotion: perceptual determinants, immediacy, and isolation after brain damage. Cognition 1998;68:111–41.
Liegeois-Chauvel C, Peretz I, Babai M, et al. Contribution of different cortical areas in the temporal lobes to music processing. Brain 1998;121:1853–67.
Zatorre RJ, Evans AC, Meyer E. Neural mechanisms underlying melodic perception and memory for pitch. J Neurosci 1994;14:1908–19.(T D Griffiths1,2, J D War)
2 Wellcome Department of Imaging Neuroscience, Institute of Neurology, Queen Square, London, UK
3 Department of Speech, University of Newcastle, Newcastle-upon-Tyne, UK
Correspondence to:
T D Griffiths
Auditory Group, University of Newcastle Medical School, Framlington Place, Newcastle-upon-Tyne NE2 4HH, UK; t.d.griffiths@ncl.ac.uk
Keywords: music; emotion; amusia
Loss of "feeling" is a common lament in popular music:
Tragedy: when the feeling’s gone and you can’t go on (Tragedy as performed by the Bee Gees. Spirits have flown, 1979.)
Here we describe loss of the feeling or emotion produced by music itself. Musical emotion can be considered at a number of levels. At the most fundamental level, dissonance produces a perception that is unpleasant to most listeners.1 More variable is the intense pleasure that certain music may evoke in particular listeners, often described as a "shiver down the spine" or "chills",2 which is likely to represent a more complex aesthetic response. We describe a patient with selective loss of this emotional response to music, due to a focal brain lesion.
A 52 year old right handed radio announcer collapsed in February 2000. He was found afterwards to have a total loss of speech comprehension and output, and a right hemiplegia. His speech recovered well, such that 12 months after the event he had only subtle output phonological problems. Motor functions recovered completely and he had no residual lateralising motor signs. However, he reported a persistent alteration in his auditory experience. He was in the habit of listening to classical music, to relax after working his night shift at the radio station, and had derived particular pleasure from listening to Rachmaninov preludes. He experienced an intense, altered emotional state or "transformation" when he did this. In common with other subjects who have this experience, the transformation was only produced by particular pieces, and he did not describe such an experience in response to music other than Rachmaninov’s, nor to other sensory experiences. This emotional response to the music was lost following the acute event, and remained absent during the period of testing between 12 and 18 months after the stroke. During this period he was able to enjoy other aspects of life, and reported no biological features of depression. He had noticed no change in his hearing, and was still able to identify speech, music, and environmental sounds normally.
When assessed in April 2001, pure tone audiometry, auditory filter widths,3 speech audiometry, prosody perception,4 and music perception were all normal. Musical perception was examined using a battery of tests during which subjects are required to make same/different judgments on melody pairs that can show differences in melodic structure, rhythm, and metre.5 Our patient showed normal scores on tests of scale (28/30), contour (27/30), interval (28/30), rhythm (28/30), metre (29/30), and incidental memory (27/30); see http://www.fas.umontreal.ca/psy/GRPLABS/lnmcg/website/index.html for normative data. Structural MRI revealed infarction involving the left insula and extending anteriorly into the left frontal lobe and inferiorly into the left amygdala. After normalisation to the standard stereotactic space of Talairach, the infarcted areas showed a close correspondence with left hemisphere areas activated during emotional response to music in normal subjects2 (fig 1).
Figure 1 (A) Structural T1 weighted MRI sections of the patient’s brain in the coronal (left) and axial (right) planes, showing infarction involving the left insula (black arrows) and amygdala (white arrows). (B) Coronal (left) and sagittal (right) T1 structural sections have been used to demonstrate the correspondence between the left insula lesion in our patient and the left insula activation associated with "chills" in response to music in normal subjects.2 Grey crosses showing the location of peak activation in the left insula of normal subjects have been superimposed on the patient’s structural brain volume. The images from the patient were normalised to the common stereotactic space of Talairach used in the previous functional imaging experiment2 to allow this comparison. The correspondence indicates that the left insula is necessary for a strong emotional response to music.
In a case such as this it is impossible to prove that the stroke produced a new deficit in the emotional reaction to music without direct evidence of the emotional reaction and its autonomic effect both before and after the stroke. The interest of this investigation accrues from the subjective report of the patient alone. Nevertheless, this is the first documented case of such a deficit of which we are aware, completing an important double dissociation between musical cognition and emotional processing. Such a dissociation would require the presence of distinct substrates for musical cognition and emotion.
The cerebral basis for musical emotion has only recently been the subject of systematic study. In the clinical literature, an impaired emotional response to music is generally accompanied by disordered musical perception (amusia). However, one previously reported patient6 had impaired recognition of music despite a preserved affective response. In contrast, our patient strikingly illustrates the reverse dissociation, with normal recognition of music but loss of the emotional response to music. Together, these two cases complete a double dissociation between the perceptual and emotional components of music processing. This double dissociation suggests that the emotional effect of a piece of music is not predetermined by simple acoustic properties (which were processed normally in our patient).
Accumulating evidence from functional brain imaging studies in normal individuals suggests that functionally and anatomically separable neural networks mediate music perception and emotion. The perception of music involves the superior temporal lobes and inferior frontal lobes.7,8 In contrast, emotional processing of music engages a distributed brain network that is also recruited by other powerful emotional stimuli that produce autonomic arousal. This network includes bilateral medial limbic structures, insula, ventral striatum, thalamus, midbrain, and widespread neocortical regions.1,2 The present study enables us to conclude that the left insula is involved in normal musical emotional processing of music.
ACKNOWLEDGEMENTS
We thank R Zatorre and I Peretz for helpful discussion, and C Mandell for structural MR brain imaging.
References
Blood AJ, Zatorre RJ, Bermudez P, et al. Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat Neurosci 1999;2:382–7.
Blood AJ, Zatorre R. Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion. Proc Natl Acad Sci U S A 2001;98:11818–23.
Patterson RD, Moore BCJ. Auditory filters and excitation patterns as representations of frequency resolution. In: Moore BCJ, ed. Frequency selectivity in hearing. London: Academic Press, 1986.
Patel AD, Peretz I, Tramo M, et al. Processing prosodic and musical patterns: a neuropsychological investigation. Brain Lang 1998;61:123–44.
Peretz I, Champod A- S, Hyde KL. Varieties of musical disorders. The Montreal Battery of Evaluation of Amusia. Ann NY Acad Sci (in press).
Peretz I, Cagnon L, Bouchard B. Music and emotion: perceptual determinants, immediacy, and isolation after brain damage. Cognition 1998;68:111–41.
Liegeois-Chauvel C, Peretz I, Babai M, et al. Contribution of different cortical areas in the temporal lobes to music processing. Brain 1998;121:1853–67.
Zatorre RJ, Evans AC, Meyer E. Neural mechanisms underlying melodic perception and memory for pitch. J Neurosci 1994;14:1908–19.(T D Griffiths1,2, J D War)