- Email: [email protected]
Rhythm and Melody in Children and Adolescents after Left or Right Temporal Lobectomy
Brain and Cognition 47, 461–469 (2001) doi:10.1006/brcg.2001.1322, available online at http://www.idealibrary.com on
Rhythm and Melody in Children and Adolescents after Left or Right Temporal Lobectomy Maureen Dennis*,† and Talar Hopyan*,‡ Department of *Psychology, The Hospital for Sick Children; and Departments of †Surgery and ‡Psychology, University of Toronto Published online November 14, 2001
Rhythm (a pattern of onset times and duration of sounds) and melody (a pattern of sound pitches) were studied in 22 children and adolescents several years after temporal lobectomy for intractable epilepsy. Left and right lobectomy groups discriminated rhythms equally well, but the right lobectomy group was poorer at discriminating melodies. Children and adolescents with right lobectomy, but not those with left temporal lobectomy, had higher melody scores with increasing age. Rhythm but not melody was related to memory for the right lobectomy group. In neither group was melody related to age at onset of non-febrile seizures, time from surgery to music tests, or the linear amount of temporal lobe resection. Pitch and melodic contour show different patterns of lateralization after temporal lobectomy in childhood or adolescence. 2001 Elsevier Science Key Words: music; rhythm; melody; temporal lobectomy; childhood epilepsy.
INTRODUCTION
Rhythm and pitch are the two primary dimensions of music (Krumhansl, 2000). Rhythm is a pattern of onset times and duration of sounds; melody is a pattern of sound pitches (Griffiths, 2000). Rhythm and melody have somewhat different neural substrates in the mature brain. Perception and production of basic parameters of rhythm, such as perception of duration and temporal order, involve a distributed system involving cerebellum, basal ganglia, and superior temporal gyrus (Peretz et al., 1994). The cerebellum and basal ganglia are important for both perceptual and motor timing; for example, adult survivors of childhood cerebellar tumors have perceptual timing deficits (Hetherington, Dennis, & Spiegler, 2000). While the cerebellum and basal ganglia may be important for controlling timing across modalities, auditory temporal perception may involve sensory-specific regions in the temporal lobes (Penhune, Zatorre, & Evans, 1998). Perception of musical rhythm engages the auditory cortex of the temporal lobes, apparently without respect to laterality. For example, rhythm discrimination shows no lateralized impairment after temporal lobectomy (Milner, 1962; Boone & Rausch, 1989), and impairment in discriminating rhythms is unrelated to laterality of stroke This research was supported by a project grant from the Ontario Mental Health Foundation. The data are accepted for presentation at the Twenty-Ninth Annual Meeting of the International Neuropsychological Society, Chicago, IL. 14–17 February, 2001. Address correspondence and reprint requests to Maureen Dennis, Ph.D., Department of Psychology Research, The Hospital for Sick Children, 555 University Avenue, Toronto, ON, M5G 1X8, Canada. Fax: (416) 813-8839. E-mail: [email protected]. 461 0278-2626/01 $35.00 2001 Elsevier Science All rights reserved.
462
DENNIS AND HOPYAN
(Peretz, 1990). The superior temporal gyrus is involved in atonal sequences without conventional rhythm, suggesting that superior temporal networks might be specialized for the analysis of patterns in segmented sound, rather than for rhythm as such (Griffiths, Johnsrude, Dean, & Green, 1999). The region of primary auditory cortex is located on the posterior–medial twothirds of Heschl’s gyrus (Rademacher, Caviness, Steinmetz, & Galaburda, 1993). The perception of basic pitch involves the function of the primary auditory cortex, without respect to laterality (Milner, 1962; Zatorre, 1998; Griffiths et al., 1999). Higher-order perception of a sequence of pitch changes, or melody, involves cortical areas other than the primary auditory cortex, and melody appears lateralized to the right temporal lobe. Thus: (1) individuals with right but not left temporal lobectomy are impaired in discriminating tonal melodies (Zatorre, 1985); (2) intracarotid sodium amylobarbitone injections into the right carotid affect singing, although not rhythm or speech, whereas left injections affect speech more than singing (Gordon & Bogen, 1974); (3) pitch discrimination (whether two pitches are different) does not vary with laterality of temporal lobe resection, although judging the direction of pitch changes (whether a second pitch rises or falls in relation to a first pitch) is poorer in individuals with right lobectomy (Johnsrude, Penhune, & Zatorre, 2000); (4) in discriminating melodies, individuals with left temporal lobectomy cannot use interval information, whereas those with right temporal lobectomy cannot use information about either intervals or the succession of pitch directions, melodic contour (Peretz, 1990); (5) removal of the right rather than left temporal lobe impairs perception of (and memory for) melody (Milner, 1962; Zatorre, Evans, & Meyer, 1994; but see Kester et al., 1991); (6) individuals with right temporal lobectomy have difficulty recognizing melodies without words (Samson & Zatorre, 1991), and remember melodies less well than words 24 h after hearing them (Sampson & Zatorre, 1992); (7) melodic processing relies importantly on the superior temporal gyrus, especially in its posterior aspect (Lie´geois-Chauvel, Peretz, Babaı¨, Laguitton, & Chauvel, 1998); and (8) metabolic rate increases for musically naı¨ve adults in the right posterior temporal and middle temporal cortex during stimulation with melodies (Mazziotta, Phelps, Carson, & Kuhl, 1982). Two broad generalizations emerge from the literature on rhythm and melody. First, the primary auditory cortex is concerned with features like duration and pitch, rather than with higher-level components of music such as rhythm and melody; in agreement with this, complex musical hallucinations engage, not the primary auditory cortex, a distributed system involving the temporal lobes (Griffiths, 2000). Second, rhythm and melody have somewhat different neural representation. Lesions in either hemisphere impair the discrimination of durational values or rhythms, whereas only right-hemisphere lesions impair the presentation of melody in terms of its global contour (Peretz, 1990). To be sure, a more complex pattern of lateralization is observed when rhythm and melody are functionally decomposed. The temporal organization of rhythm involves at least two types of temporal organization: rhythm, the pattern of relative durations of tones and silences without regard to periodicity, and meter, the perceived beat marking off equal durational units and the arrangement of these beats into measures that allow one to distinguish, for instance, a waltz from a march (Peretz, 1990). There may be left-hemisphere involvement in both rhythm (e.g., rhythm activates the left inferior Broca’s area and insula; Platel et al., 1997) and access to semantic representations of meter (Lie´geois-Chauvel et al., 1998; Zatorre, 1998). For some melodic functions, there is an interaction between side of temporal lobectomy and primary auditory cortex involvement. Individuals with right temporal lobe lobectomy that includes primary auditory cortex are unable to retain an accurate representation of the temporal dimension of the auditory stimuli (Penhune, Zatorre, & Feindel, 1999).
MUSIC AFTER TEMPORAL LOBECTOMY
463
Much information about the neural basis of music has come from individuals with temporal lobe resection, or temporal lobectomy. For the most part, music outcomes after temporal lobectomy have been studied in adults on a group-wise basis, with groups of individuals with temporal lobectomy contrasted with each other (e.g., leftvs. right-sided surgery) or with controls. Within-group variability in relation to demographic and medical variables related to the surgery and seizure history has been less fully explored, and for children and adolescents has not been reported. Inspection of the standard deviations for music tasks in several articles suggests that the variability within groups is not negligible. Demographic and medical variables relevant to within-group variability would include age at music tests, age at onset of nonfebrile seizures, time from surgery to music tests, and linear amount of temporal lobe resection. Individuals considered for temporal lobectomy typically have a long history of intractable seizures, often dating from childhood; for example, 85% of adults in the Lie´geois-Chauvel et al. (1998) study had childhood-onset epilepsy. Most studies do not report age at onset of nonfebrile seizures, and age at seizure onset has not been explored with respect to music, even though age at onset of seizures is a variable relevant to some types of oral language comprehension outcomes after temporal lobe surgery (e.g., Kohn, 1980) and to some types of memory outcome (Saykin, Gur, Sussman, O’Connor, & Gur, 1989). Time from surgery to tests is a measure of recovery from surgery, adjustment of medication regimes, and the length of time the individual has had no seizures, or reduced seizure frequency. Studies have considered acute postsurgical effects, for instance, measuring the change in musical abilities before and immediately after surgery (Kester et al., 1991), or chronic effects, but the relation between time since surgery and music outcome has not been directly measured. Linear amount of temporal lobe resection is a marker (if not a direct measure) of the extent of temporal lobe involvement in the production of seizures. It has been proposed that larger temporal lobe resections may be associated with more disrupted music abilities than smaller resections (Koike, Shimizu, Suzuki, Ishijima, & Sugishita, 1996; but see Milner, 1962). The relation between music and memory is not clear. It has been argued that shortterm memory is one of two processes involved in discriminating melodies (Zatorre, 1985), although it is not known how memory for melody, which involves pitch sequences, is related to auditory or visual sequence memory in younger individuals with temporal lobectomy. In this article, we compared rhythm and melody in children and adolescents with temporal lobectomy for longstanding seizure disorder in relation to a number of variables: side of temporal lobectomy, age at onset of non-febrile seizures, age at music tests, time from surgery to music tests, and linear amount of temporal lobe resection. We also explored the relation between music and auditory and visual memory tasks. Between-group comparisons were made by means of MANOVAS, and within-group variability in music outcome was analyzed with regression models. Hypotheses concern between-group comparisons of laterality, and the within- and between-group effects of age variables, extent of temporal lobe removal, and memory function. 1.
Laterality
Just as with adults, children and adolescents with left and right temporal lobectomy will perform equally well a task of rhythm discrimination, but those with right temporal lobectomy will perform more poorly on a task of melody. Memory tasks involving auditory or visual sequences will show no laterality effects; that is, any lateralized results will concern music, not memory.
464 2.
DENNIS AND HOPYAN
Age Variables
Because the groups are matched for chronological age, neither rhythm nor melody will be related to age at music tests. Because early music experience affects the neural representation of music (Schlaug, Ja¨ncke, Huang, Staiger, & Steinmetz, 1995a, 1995b), an earlier age at nonfebrile seizures may be related to both rhythm and melody. 3.
Extent of Temporal Lobe Resection
Extent of temporal lobe resection will be unrelated to rhythm but negatively related to tonal memory scores for the right temporal lobectomy group. This is in keeping with data from Koike et al. (1996). 4.
Memory
There will be no relation within either left or right group between music and memory tasks involving auditory or visual sequences. The literature suggests that rhythm and melody are not processed in the same manner as are other auditory tasks. METHODS
Participants Participants were 22 adolescents who had had unilateral temporal lobectomy for intractable epilepsy. Inclusion in the study required that the participant had a postsurgical Verbal and/or Performance IQ score of 70 or above on the Wechsler scales. Medical information on participants was obtained by reviewing hospital charts or by direct inquiry. Sample characteristics are shown in Table 1. The left and right temporal lobectomy groups did not differ statistically in age at test, age at onset of nonfebrile seizures, time from surgery to test, amount of temporal lobe resection, Verbal IQ, or Performance IQ.
Tasks Rhythm (Rhythm Test, Seashore Measures of Musical Talents: Seashore, Lewis, & Saetveit, 1960). The Rhythm test required the participants to indicate whether each of 30 pairs of rhythmic patterns were the same or different. Stimuli were generated from a beat-frequency oscillator set at 500 cycles. Tempo was constant at the rate of 92 quarter notes per minute. After practice items, the test proper was administered with three item groupings, each of 10 patterns: 5 note patterns in 2/4 time; 6 note patterns in 3/4 time; and 7 note patterns in 4/4 time. Melody (Tonal Memory Test, Seashore Measures of Musical Talents: Seashore, Lewis, & Saetveit, 1960). The Tonal Memory test required the participants to indicate which note was different in each of 30 pairs of tonal sequences consisting of 10 items each of 3, 4, and 5 tone spans. Stimuli were
TABLE 1
Age at test a Age at seizure onset a Time surgery to test a Amount of resection b Verbal IQ Performance IQ
Left lobectomy
Right lobectomy
17.2 (3.4, 13.5–22.5) 5.5 (2.4, 2.0–10.1) 3.7 (2.7, 0.6–8.8) 5.4 (1.0, 4.0–7.5) 90.3 (17.4, 62–119) 103.0 (17.5, 71–129)
18.2 (3.9, 12.0–23.4) 5.7 (2.9, 2.0–11.1) 4.7 (2.9, 1.1–8.7) 6.3 (1.3, 4.5–8.0) 100.1 (15.4, 68–120) 98.2 (16.0, 77–124)
Note. Values are means (standard deviation, range). a Years and decimal months. b Centimeters.
465
MUSIC AFTER TEMPORAL LOBECTOMY
produced from a Hammond organ, using 18 chromatic steps up from middle C. Tempo was controlled and intensity was essentially constant. After practice items, the participants were instructed that they would hear a short series of notes played twice, and that one note would always be changed in the second playing. They were instructed to indicate which note (first, second, third, and so on) had been changed. Auditory memory (Memory for Sequence Task, Auditory Memory Tests: Goldman, Fristoe, & Woodcock, 1974). The Memory for Sequence task requires participants to judge the serial order of a set of words. Participants listen to a prerecorded list of words while facing a blank easel page. After the last word is heard, cards picturing the words are presented, and the participants arranged the cards into the order of the words heard. Scores are given for placing the first card, the last card, and for any sequence of two cards corresponding to the order of contiguous pair of words in the list. Lists progress in difficulty from two to eight words presented at the rate of one every 2 s. Visual memory (Visual–Sequential Memory Test, Illinois Tests of Psycholinguistic Abilities: Kirk, McCarthy, & Kirk, 1968). The Visual–Sequential Memory task requires the participants to observe the examiner placing a series of chips in sequence in a tray, and then to reproduce the sequence. Each chip is marked with a black and white abstract design.
RESULTS
Data are presented in Table 2. A MANCOVA was conducted with side of surgery as the between-subjects factor, Test Age as the covariate, and Rhythm, Melody, Auditory Memory, and Visual Memory as the outcome measures. The overall MANCOVA was significant for side of surgery [F(4, 15) ⫽ 4.6, p ⫽ .0131]. For Rhythm, Auditory Memory, and Visual Memory, there were no significant effects for side of surgery or test age, and no significant interaction between the two. For Melody, there was a significant effect of side of surgery [F(1, 18) ⫽ 6.0, p ⫽ .0251] that was qualified by a significant interaction between side of surgery and test age [F(1, 18) ⫽ 5.1, p ⫽ .0368]. Children and adolescents with right temporal lobectomy, but not those with left temporal lobectomy, had higher melody scores with increasing age (Fig. 1). Seizure status postsurgery had been classified for each participant as (1) unchanged or (2) improved or seizure-free. Two individuals in each lobectomy group had unchanged seizure frequency, with the rest being either seizure-free or having reduced seizure frequency. The MANCOVA was run excluding the four individuals (two left, two right lobectomy) with seizure disorders continuing after surgery, and a similar pattern of results was obtained. The overall MANCOVA was significant for side of surgery [F(4, 11) ⫽ 3.5, p ⫽ .0453]. For Rhythm and Visual Memory, there were no significant effects for side of surgery or test age, and no significant interaction between the two. For Auditory Memory, there was no significant side of surgery effect, but a marginal interaction between side of surgery and test age [F(1, 14) ⫽ 4.4, p ⫽ .0555]. For Melody, again, there was a significant effect of side of surgery [F(1, 14) ⫽ 5.7, p ⫽ .0314] that was qualified by a significant interaction between side of surgery and test age [F(1, 14) ⫽ 5.0, p ⫽ .0419]. TABLE 2 Left lobectomy Rhythm a Melody Auditory memory Visual memory
22.9 20.0 52.9 31.1
(3.2, 17–27) (5.9, 7–27) (13.5, 17–72) (7.5, 19–42)
Right lobectomy 22.9 17.7 58.2 29.0
(3.6, 17–29) (6.4, 8–27) (14.8, 32–76) (10.0, 18–44)
Controls a 25.3 (3.3) 22.7 (5.3)
Note. Values are mean numbers correct (standard deviation, range). a Published control data, means and standard deviations for Grades 6–16 (Seashore et al., 1960).
466
DENNIS AND HOPYAN
FIG. 1. Regression analyses of test age on rhythm and melody for left and right temporal lobectomy groups.
Regression analyses were used to explore within-group variability in melody scores. There was no relation between melody in either left or right temporal lobectomy group and age at onset of nonfebrile seizures, time from surgery to music tests, or the linear amount of temporal lobe resection. Regression analyses were used to explore the relation between music and memory. There was no relation between melody and auditory or visual memory for either left or right temporal lobectomy group. Rhythm was unrelated to memory for the left lobectomy group. For the right lobectomy group, rhythm was related to both auditory [F(1, 7) ⫽ 6.5, p ⫽ .0383] and visual [F(1, 7) ⫽ 13.9, p ⫽ .0074] memory. For children and adolescents with right lobectomy, auditory memory accounted for 48%, and visual memory for 66%, of the variance in rhythm. DISCUSSION
Children and adolescents several years after temporal lobectomy show a similar pattern of results to those previously reported for adults after the same surgery, i.e., similar proficiency at discriminating rhythm, but a right lateralized deficit in melodic discrimination. This is in agreement with the first hypothesis of the study. Even before adulthood, damage to the right temporal lobe has a relatively selective effect on the domain of music involving melody. Rhythm tasks activate left anterior brain regions (Platel et al., 1997), and meter tasks requiring semantic categorization (Zatorre, 1998) are impaired by anterior damage to either temporal lobe, whereas rhythm discrimination is affected by damage
MUSIC AFTER TEMPORAL LOBECTOMY
467
to the posterior temporal gyrus (Lie´geois-Chauvel et al., 1998). It is unclear how components of rhythm may be represented within the immature, damaged temporal lobe. For example, a comparison of rhythm and meter tasks may reveal a pattern of skill that varies by both laterality and distribution of temporal lobe damage. Although we found no lateralization effects for the rhythm task, rhythm (but not melody) varied with memory. Why rhythm rather than melody should be related to auditory memory function is not clear, although the results for children and adolescents are in agreement with the fact that some right temporal lobectomy subgroups have difficulty remembering rhythms (Penhune et al., 1999). The data do suggest that the manner in which the rhythm task was performed may vary by side of lobectomy, even when the outcome is not lateralized. Age at onset of epilepsy is a moderating influence on memory outcome after temporal lobectomy, at least for semantic and figural memory (Saykin et al., 1989). The present results do not confirm the second hypothesis, and show, instead, that age at onset was unrelated to either rhythm or melody. Age at test was important for melody in the right, but not left, lobectomy group, which emphasizes the developmental nature of musical skill. Given sufficient time, the right lobectomy individuals become more proficient at the melody task, although performance in the left lobectomy group is constant over age. Music experience, particularly before age 7, not only affects musical skills and musical imagery (Aleman, Nieuwenstein, Bocker, & de Haan, 2000), but influences the brain organization for music (e.g., Schlaug et al., 1995a, 1995b). Perhaps early seizures in the right temporal lobe prevent the facilitating effect of listening to and/or making music on the later brain organization for melody. In any event, studies of music in individuals with longstanding developmental brain compromise, such as those with childhood seizure disorders and subsequent temporal lobectomy, might consider outcome in relation to age at test. Extent of temporal lobe resection was unrelated to music in children and adolescents, in agreement with earlier studies of adults (e.g., Milner, 1962; Zatorre, 1985), and the data did not vary after excluding four individuals with continuing postsurgical seizures (presumably the group with most functional temporal lobe damage). In the absence of postsurgical functional imaging, it is difficult to identify the limits of the effective temporal lobe lesions in these children and adolescents. Nor do our data address the issue of how music might be represented within the immature temporal lobe on either side. Earlier studies suggested that music outcome after temporal lobectomy did not vary according to the involvement of Heschl’s gyrus (e.g., Milner, 1962), although later studies have suggested that some music outcomes depend on an interaction between side of lobectomy and involvement of Heschl’s gyrus. For example, Penhune et al. (1999) found that individuals with right temporal resections that included primary auditory cortex can retain a visual, but not an auditory, rhythm. In our children and adolescents, we cannot infer the extent of primary auditory cortex involvement from the extent of resection from the temporal pole. Excision of Heschl’s gyrus need not entail a larger total volume of resected cortical tissue, because the extent of resection along the first temporal gyrus is generally independent of removal along the third temporal convolution of the mesial aspect of the temporal lobe. Nor can we assess the specific anatomical claim that the right superior temporal gyrus is critical for the processing of melody (Lie´geois-Chauvel et al., 1998). Neuroimaging studies with children are required to clarify these issues. Finally, the data from children and adolescents with temporal lobectomy are in broad agreement with the idea that rhythm and pitch, two core elements of music (Krumhansl, 2000), might be processed by rather distinct brain mechanisms (Peretz, 1990). Future studies with children and adolescents after temporal lobectomy should
468
DENNIS AND HOPYAN
fractionate music within the domains of rhythm and pitch to better understand the developmental course of these mechanisms. REFERENCES Aleman, A., Nieuwenstein, M. R., Bocker, K. B. E., & de Haan, E. H. F. (2000). Music training and mental imagery ability. Neuropsychologia, 38, 1664–1668. Boone, K. B., & Rausch, R. (1989). Seashore Rhythm test performance in patients with unilateral temporal lobe damage. Journal of Clinical Psychology, 45, 614–618. Goldman, R., Fristoe, M., & Woodcock, R. W. (1974). Goldman–Fristoe–Woodcock Auditory Memory Tests. American Guidance Service, Circle Pines, Minnesota. Gordon, H. W., & Bogen, J. E. (1974). Hemispheric lateralization of singing after intracarotid sodium amylobarbitone. Journal of Neurology, Neurosurgery, and Psychiatry, 37, 727–738. Griffiths, T. D. (2000). Musical hallucinosis in acquired deafness—Phenomenology and brain substrate. Brain, 123, 2056–2076. Griffiths, T. D., Johnsrude, I., Dean, J. L., & Green, G. G. R. (1999). A common substrate for the analysis of pitch and duration pattern in segmented sound? Neuroreport, 10, 3825–3830. Hetherington, R., Dennis, M., & Spiegler, B. (2000). Perception and estimation of time in long-term survivors of childhood posterior fossa tumors. Journal of the International Neuropsychological Society, 6, 682–692. Johnsrude, I. S., Penhune, V. B., & Zatorre, R. J. (2000). Functional specificity in the right human auditory cortex for perceiving pitch direction. Brain, 123, 155–163. Kester, D. B., Saykin, A. J., Sperling, M. R., O’Connor, M. J., Robinson, L. J., & Gur, R. C. (1991). Acute effect of anterior temporal lobectomy on musical processing. Neuropsychologia, 29, 703– 709. Kirk, S. A., McCarthy, J. J., & Kirk, W. D. (1968). Illinois Test of Psycholinguistic Abilities. Examiner’s manual. (Rev. ed). Urbana, IL: University of Illinois Press. Kohn, B. (1980). Right-hemisphere speech representation and comprehension of syntax after left cerebral injury. Brain and Language, 9, 350–361. Koike, A., Shimizu, H., Suzuki, I., Ishijima, B., & Sugishita, M. (1996). Preserved musical abilities following right temporal lobectomy. Journal of Neurosurgery, 85, 1000–1004. Krumhansl, C. L. (2000). Rhythm and pitch in music cognition. Psychological Bulletin, 126, 159–179. Lie´geois-Chauvel, C., Peretz, I., Babaı¨, M., Laguitton, V., & Chauvel, P. (1998). Contribution of different cortical areas in the temporal lobes to music processing. Brain, 121, 1853–1867. Mazziotta, J. C., Phelps, M. E., Carson, R. E., & Kuhl, D. E. (1982). Tomographic mapping of human cerebral metabolism: Auditory stimulation. Neurology, 32, 921–937. Milner, B. (1962). Laterality effects in audition. In V. B. Mountcastle (Ed.), Interhemispheric relations and cerebral dominance (pp. 177–195). Baltimore, MD: Johns Hopkins Univ. Press. Penhune, V. B., Zatorre, R. J., & Evans, A. C. (1998). Cerebellar contributions to motor timing: A PET study of auditory and visual rhythm reproduction. Journal of Cognitive Neuroscience, 10, 752– 765. Penhune, V. B., Zatorre, R. J., & Feindel, W. H. (1999). The role of auditory cortex in retention of rhythmic patterns as studied in patients with temporal lobe removals including Heschl’s gyrus. Neuropsychologia, 37, 315–331. Peretz, I. (1990). Processing of local and global musical information by unilateral brain-damaged patients. Brain, 113, 1185–1205. Peretz, I., Kolinsky, R., Tramo, M., Labrecque, R., Hublet, C., Demeurisse, G., & Belleville, S. (1994). Functional dissociations following bilateral lesions of auditory cortex. Brain, 117, 1283–1301. Platel, H., Price, C., Baron, J-C., Wise, R., Lambert, J., Frackowiak, R. S. J., Lechevalier, B., & Eustache, F. (1997). The structural components of music perception. A functional anatomical study. Brain, 120, 229–243. Rademacher, J., Caviness, V. S., Steinmetz, H., & Galaburda, A. M. (1993). Topographical variation of the human primary auditory cortices: Implications for neuroimaging, brain mapping and neurobiology. Cerebral Cortex, 3, 313–329. Samson, S., & Zatorre, R. J. (1988). Melodic and harmonic discrimination following unilateral cerebral excision. Brain and Cognition, 7, 348–360.
MUSIC AFTER TEMPORAL LOBECTOMY
469
Samson, S., & Zatorre, R. J. (1991). Recognition memory for text and melody of songs after unilateral temporal lobe lesion: Evidence for dual encoding. Journal of Experimental Psychology: Learning, Memory, and Cognition, 17, 793–804. Samson, S., & Zatorre, R. J. (1992). Learning and retention of melodic and verbal information after unilateral temporal lobectomy. Neuropsychologia, 30, 815–826. Saykin, A. J., Gur, R. C., Sussman, N. M., O’Connor, M. J., & Gur, R. E. (1989). Memory deficits before and after temporal lobectomy: Effect of laterality and age at onset. Brain and Cognition, 9, 191–200. Schlaug, G., Ja¨ncke, L., Huang, Y., Staiger, J. F., & Steinmetz, H. (1995a). Increased corpus callosum size in musicians. Neuropsychologia, 33, 1047–1055. Schlaug, G., Ja¨ncke, L., Huang, Y., & Steinmetz, H. (1995b). In vivo evidence of structural brain asymmetry in musicians. Science, 267, 699. Seashore, C. E., Lewis, D., & Saetveit, J. G. (1960). Seashore Measure of Musical Talents, Manual revised. New York: Psychological Corp. Zatorre, R. J. (1985). Discrimination and recognition of tonal melodies after unilateral cerebral excisions. Neuropsychologia, 23, 31–41. Zatorre, R. J. (1998). Functional specialization of human auditory cortex for musical processing. Brain, 121, 1817–1818. Zatorre, R. J., Evans, A. C., & Meyer, E. (1994). Neural mechanisms underlying melodic perception and memory for pitch. Journal of Neuroscience, 14, 1908–1919.
Rhythm and Melody in Children and Adolescents after Left or Right Temporal Lobectomy Maureen Dennis*,† and Talar Hopyan*,‡ Department of *Psychology, The Hospital for Sick Children; and Departments of †Surgery and ‡Psychology, University of Toronto Published online November 14, 2001
Rhythm (a pattern of onset times and duration of sounds) and melody (a pattern of sound pitches) were studied in 22 children and adolescents several years after temporal lobectomy for intractable epilepsy. Left and right lobectomy groups discriminated rhythms equally well, but the right lobectomy group was poorer at discriminating melodies. Children and adolescents with right lobectomy, but not those with left temporal lobectomy, had higher melody scores with increasing age. Rhythm but not melody was related to memory for the right lobectomy group. In neither group was melody related to age at onset of non-febrile seizures, time from surgery to music tests, or the linear amount of temporal lobe resection. Pitch and melodic contour show different patterns of lateralization after temporal lobectomy in childhood or adolescence. 2001 Elsevier Science Key Words: music; rhythm; melody; temporal lobectomy; childhood epilepsy.
INTRODUCTION
Rhythm and pitch are the two primary dimensions of music (Krumhansl, 2000). Rhythm is a pattern of onset times and duration of sounds; melody is a pattern of sound pitches (Griffiths, 2000). Rhythm and melody have somewhat different neural substrates in the mature brain. Perception and production of basic parameters of rhythm, such as perception of duration and temporal order, involve a distributed system involving cerebellum, basal ganglia, and superior temporal gyrus (Peretz et al., 1994). The cerebellum and basal ganglia are important for both perceptual and motor timing; for example, adult survivors of childhood cerebellar tumors have perceptual timing deficits (Hetherington, Dennis, & Spiegler, 2000). While the cerebellum and basal ganglia may be important for controlling timing across modalities, auditory temporal perception may involve sensory-specific regions in the temporal lobes (Penhune, Zatorre, & Evans, 1998). Perception of musical rhythm engages the auditory cortex of the temporal lobes, apparently without respect to laterality. For example, rhythm discrimination shows no lateralized impairment after temporal lobectomy (Milner, 1962; Boone & Rausch, 1989), and impairment in discriminating rhythms is unrelated to laterality of stroke This research was supported by a project grant from the Ontario Mental Health Foundation. The data are accepted for presentation at the Twenty-Ninth Annual Meeting of the International Neuropsychological Society, Chicago, IL. 14–17 February, 2001. Address correspondence and reprint requests to Maureen Dennis, Ph.D., Department of Psychology Research, The Hospital for Sick Children, 555 University Avenue, Toronto, ON, M5G 1X8, Canada. Fax: (416) 813-8839. E-mail: [email protected]. 461 0278-2626/01 $35.00 2001 Elsevier Science All rights reserved.
462
DENNIS AND HOPYAN
(Peretz, 1990). The superior temporal gyrus is involved in atonal sequences without conventional rhythm, suggesting that superior temporal networks might be specialized for the analysis of patterns in segmented sound, rather than for rhythm as such (Griffiths, Johnsrude, Dean, & Green, 1999). The region of primary auditory cortex is located on the posterior–medial twothirds of Heschl’s gyrus (Rademacher, Caviness, Steinmetz, & Galaburda, 1993). The perception of basic pitch involves the function of the primary auditory cortex, without respect to laterality (Milner, 1962; Zatorre, 1998; Griffiths et al., 1999). Higher-order perception of a sequence of pitch changes, or melody, involves cortical areas other than the primary auditory cortex, and melody appears lateralized to the right temporal lobe. Thus: (1) individuals with right but not left temporal lobectomy are impaired in discriminating tonal melodies (Zatorre, 1985); (2) intracarotid sodium amylobarbitone injections into the right carotid affect singing, although not rhythm or speech, whereas left injections affect speech more than singing (Gordon & Bogen, 1974); (3) pitch discrimination (whether two pitches are different) does not vary with laterality of temporal lobe resection, although judging the direction of pitch changes (whether a second pitch rises or falls in relation to a first pitch) is poorer in individuals with right lobectomy (Johnsrude, Penhune, & Zatorre, 2000); (4) in discriminating melodies, individuals with left temporal lobectomy cannot use interval information, whereas those with right temporal lobectomy cannot use information about either intervals or the succession of pitch directions, melodic contour (Peretz, 1990); (5) removal of the right rather than left temporal lobe impairs perception of (and memory for) melody (Milner, 1962; Zatorre, Evans, & Meyer, 1994; but see Kester et al., 1991); (6) individuals with right temporal lobectomy have difficulty recognizing melodies without words (Samson & Zatorre, 1991), and remember melodies less well than words 24 h after hearing them (Sampson & Zatorre, 1992); (7) melodic processing relies importantly on the superior temporal gyrus, especially in its posterior aspect (Lie´geois-Chauvel, Peretz, Babaı¨, Laguitton, & Chauvel, 1998); and (8) metabolic rate increases for musically naı¨ve adults in the right posterior temporal and middle temporal cortex during stimulation with melodies (Mazziotta, Phelps, Carson, & Kuhl, 1982). Two broad generalizations emerge from the literature on rhythm and melody. First, the primary auditory cortex is concerned with features like duration and pitch, rather than with higher-level components of music such as rhythm and melody; in agreement with this, complex musical hallucinations engage, not the primary auditory cortex, a distributed system involving the temporal lobes (Griffiths, 2000). Second, rhythm and melody have somewhat different neural representation. Lesions in either hemisphere impair the discrimination of durational values or rhythms, whereas only right-hemisphere lesions impair the presentation of melody in terms of its global contour (Peretz, 1990). To be sure, a more complex pattern of lateralization is observed when rhythm and melody are functionally decomposed. The temporal organization of rhythm involves at least two types of temporal organization: rhythm, the pattern of relative durations of tones and silences without regard to periodicity, and meter, the perceived beat marking off equal durational units and the arrangement of these beats into measures that allow one to distinguish, for instance, a waltz from a march (Peretz, 1990). There may be left-hemisphere involvement in both rhythm (e.g., rhythm activates the left inferior Broca’s area and insula; Platel et al., 1997) and access to semantic representations of meter (Lie´geois-Chauvel et al., 1998; Zatorre, 1998). For some melodic functions, there is an interaction between side of temporal lobectomy and primary auditory cortex involvement. Individuals with right temporal lobe lobectomy that includes primary auditory cortex are unable to retain an accurate representation of the temporal dimension of the auditory stimuli (Penhune, Zatorre, & Feindel, 1999).
MUSIC AFTER TEMPORAL LOBECTOMY
463
Much information about the neural basis of music has come from individuals with temporal lobe resection, or temporal lobectomy. For the most part, music outcomes after temporal lobectomy have been studied in adults on a group-wise basis, with groups of individuals with temporal lobectomy contrasted with each other (e.g., leftvs. right-sided surgery) or with controls. Within-group variability in relation to demographic and medical variables related to the surgery and seizure history has been less fully explored, and for children and adolescents has not been reported. Inspection of the standard deviations for music tasks in several articles suggests that the variability within groups is not negligible. Demographic and medical variables relevant to within-group variability would include age at music tests, age at onset of nonfebrile seizures, time from surgery to music tests, and linear amount of temporal lobe resection. Individuals considered for temporal lobectomy typically have a long history of intractable seizures, often dating from childhood; for example, 85% of adults in the Lie´geois-Chauvel et al. (1998) study had childhood-onset epilepsy. Most studies do not report age at onset of nonfebrile seizures, and age at seizure onset has not been explored with respect to music, even though age at onset of seizures is a variable relevant to some types of oral language comprehension outcomes after temporal lobe surgery (e.g., Kohn, 1980) and to some types of memory outcome (Saykin, Gur, Sussman, O’Connor, & Gur, 1989). Time from surgery to tests is a measure of recovery from surgery, adjustment of medication regimes, and the length of time the individual has had no seizures, or reduced seizure frequency. Studies have considered acute postsurgical effects, for instance, measuring the change in musical abilities before and immediately after surgery (Kester et al., 1991), or chronic effects, but the relation between time since surgery and music outcome has not been directly measured. Linear amount of temporal lobe resection is a marker (if not a direct measure) of the extent of temporal lobe involvement in the production of seizures. It has been proposed that larger temporal lobe resections may be associated with more disrupted music abilities than smaller resections (Koike, Shimizu, Suzuki, Ishijima, & Sugishita, 1996; but see Milner, 1962). The relation between music and memory is not clear. It has been argued that shortterm memory is one of two processes involved in discriminating melodies (Zatorre, 1985), although it is not known how memory for melody, which involves pitch sequences, is related to auditory or visual sequence memory in younger individuals with temporal lobectomy. In this article, we compared rhythm and melody in children and adolescents with temporal lobectomy for longstanding seizure disorder in relation to a number of variables: side of temporal lobectomy, age at onset of non-febrile seizures, age at music tests, time from surgery to music tests, and linear amount of temporal lobe resection. We also explored the relation between music and auditory and visual memory tasks. Between-group comparisons were made by means of MANOVAS, and within-group variability in music outcome was analyzed with regression models. Hypotheses concern between-group comparisons of laterality, and the within- and between-group effects of age variables, extent of temporal lobe removal, and memory function. 1.
Laterality
Just as with adults, children and adolescents with left and right temporal lobectomy will perform equally well a task of rhythm discrimination, but those with right temporal lobectomy will perform more poorly on a task of melody. Memory tasks involving auditory or visual sequences will show no laterality effects; that is, any lateralized results will concern music, not memory.
464 2.
DENNIS AND HOPYAN
Age Variables
Because the groups are matched for chronological age, neither rhythm nor melody will be related to age at music tests. Because early music experience affects the neural representation of music (Schlaug, Ja¨ncke, Huang, Staiger, & Steinmetz, 1995a, 1995b), an earlier age at nonfebrile seizures may be related to both rhythm and melody. 3.
Extent of Temporal Lobe Resection
Extent of temporal lobe resection will be unrelated to rhythm but negatively related to tonal memory scores for the right temporal lobectomy group. This is in keeping with data from Koike et al. (1996). 4.
Memory
There will be no relation within either left or right group between music and memory tasks involving auditory or visual sequences. The literature suggests that rhythm and melody are not processed in the same manner as are other auditory tasks. METHODS
Participants Participants were 22 adolescents who had had unilateral temporal lobectomy for intractable epilepsy. Inclusion in the study required that the participant had a postsurgical Verbal and/or Performance IQ score of 70 or above on the Wechsler scales. Medical information on participants was obtained by reviewing hospital charts or by direct inquiry. Sample characteristics are shown in Table 1. The left and right temporal lobectomy groups did not differ statistically in age at test, age at onset of nonfebrile seizures, time from surgery to test, amount of temporal lobe resection, Verbal IQ, or Performance IQ.
Tasks Rhythm (Rhythm Test, Seashore Measures of Musical Talents: Seashore, Lewis, & Saetveit, 1960). The Rhythm test required the participants to indicate whether each of 30 pairs of rhythmic patterns were the same or different. Stimuli were generated from a beat-frequency oscillator set at 500 cycles. Tempo was constant at the rate of 92 quarter notes per minute. After practice items, the test proper was administered with three item groupings, each of 10 patterns: 5 note patterns in 2/4 time; 6 note patterns in 3/4 time; and 7 note patterns in 4/4 time. Melody (Tonal Memory Test, Seashore Measures of Musical Talents: Seashore, Lewis, & Saetveit, 1960). The Tonal Memory test required the participants to indicate which note was different in each of 30 pairs of tonal sequences consisting of 10 items each of 3, 4, and 5 tone spans. Stimuli were
TABLE 1
Age at test a Age at seizure onset a Time surgery to test a Amount of resection b Verbal IQ Performance IQ
Left lobectomy
Right lobectomy
17.2 (3.4, 13.5–22.5) 5.5 (2.4, 2.0–10.1) 3.7 (2.7, 0.6–8.8) 5.4 (1.0, 4.0–7.5) 90.3 (17.4, 62–119) 103.0 (17.5, 71–129)
18.2 (3.9, 12.0–23.4) 5.7 (2.9, 2.0–11.1) 4.7 (2.9, 1.1–8.7) 6.3 (1.3, 4.5–8.0) 100.1 (15.4, 68–120) 98.2 (16.0, 77–124)
Note. Values are means (standard deviation, range). a Years and decimal months. b Centimeters.
465
MUSIC AFTER TEMPORAL LOBECTOMY
produced from a Hammond organ, using 18 chromatic steps up from middle C. Tempo was controlled and intensity was essentially constant. After practice items, the participants were instructed that they would hear a short series of notes played twice, and that one note would always be changed in the second playing. They were instructed to indicate which note (first, second, third, and so on) had been changed. Auditory memory (Memory for Sequence Task, Auditory Memory Tests: Goldman, Fristoe, & Woodcock, 1974). The Memory for Sequence task requires participants to judge the serial order of a set of words. Participants listen to a prerecorded list of words while facing a blank easel page. After the last word is heard, cards picturing the words are presented, and the participants arranged the cards into the order of the words heard. Scores are given for placing the first card, the last card, and for any sequence of two cards corresponding to the order of contiguous pair of words in the list. Lists progress in difficulty from two to eight words presented at the rate of one every 2 s. Visual memory (Visual–Sequential Memory Test, Illinois Tests of Psycholinguistic Abilities: Kirk, McCarthy, & Kirk, 1968). The Visual–Sequential Memory task requires the participants to observe the examiner placing a series of chips in sequence in a tray, and then to reproduce the sequence. Each chip is marked with a black and white abstract design.
RESULTS
Data are presented in Table 2. A MANCOVA was conducted with side of surgery as the between-subjects factor, Test Age as the covariate, and Rhythm, Melody, Auditory Memory, and Visual Memory as the outcome measures. The overall MANCOVA was significant for side of surgery [F(4, 15) ⫽ 4.6, p ⫽ .0131]. For Rhythm, Auditory Memory, and Visual Memory, there were no significant effects for side of surgery or test age, and no significant interaction between the two. For Melody, there was a significant effect of side of surgery [F(1, 18) ⫽ 6.0, p ⫽ .0251] that was qualified by a significant interaction between side of surgery and test age [F(1, 18) ⫽ 5.1, p ⫽ .0368]. Children and adolescents with right temporal lobectomy, but not those with left temporal lobectomy, had higher melody scores with increasing age (Fig. 1). Seizure status postsurgery had been classified for each participant as (1) unchanged or (2) improved or seizure-free. Two individuals in each lobectomy group had unchanged seizure frequency, with the rest being either seizure-free or having reduced seizure frequency. The MANCOVA was run excluding the four individuals (two left, two right lobectomy) with seizure disorders continuing after surgery, and a similar pattern of results was obtained. The overall MANCOVA was significant for side of surgery [F(4, 11) ⫽ 3.5, p ⫽ .0453]. For Rhythm and Visual Memory, there were no significant effects for side of surgery or test age, and no significant interaction between the two. For Auditory Memory, there was no significant side of surgery effect, but a marginal interaction between side of surgery and test age [F(1, 14) ⫽ 4.4, p ⫽ .0555]. For Melody, again, there was a significant effect of side of surgery [F(1, 14) ⫽ 5.7, p ⫽ .0314] that was qualified by a significant interaction between side of surgery and test age [F(1, 14) ⫽ 5.0, p ⫽ .0419]. TABLE 2 Left lobectomy Rhythm a Melody Auditory memory Visual memory
22.9 20.0 52.9 31.1
(3.2, 17–27) (5.9, 7–27) (13.5, 17–72) (7.5, 19–42)
Right lobectomy 22.9 17.7 58.2 29.0
(3.6, 17–29) (6.4, 8–27) (14.8, 32–76) (10.0, 18–44)
Controls a 25.3 (3.3) 22.7 (5.3)
Note. Values are mean numbers correct (standard deviation, range). a Published control data, means and standard deviations for Grades 6–16 (Seashore et al., 1960).
466
DENNIS AND HOPYAN
FIG. 1. Regression analyses of test age on rhythm and melody for left and right temporal lobectomy groups.
Regression analyses were used to explore within-group variability in melody scores. There was no relation between melody in either left or right temporal lobectomy group and age at onset of nonfebrile seizures, time from surgery to music tests, or the linear amount of temporal lobe resection. Regression analyses were used to explore the relation between music and memory. There was no relation between melody and auditory or visual memory for either left or right temporal lobectomy group. Rhythm was unrelated to memory for the left lobectomy group. For the right lobectomy group, rhythm was related to both auditory [F(1, 7) ⫽ 6.5, p ⫽ .0383] and visual [F(1, 7) ⫽ 13.9, p ⫽ .0074] memory. For children and adolescents with right lobectomy, auditory memory accounted for 48%, and visual memory for 66%, of the variance in rhythm. DISCUSSION
Children and adolescents several years after temporal lobectomy show a similar pattern of results to those previously reported for adults after the same surgery, i.e., similar proficiency at discriminating rhythm, but a right lateralized deficit in melodic discrimination. This is in agreement with the first hypothesis of the study. Even before adulthood, damage to the right temporal lobe has a relatively selective effect on the domain of music involving melody. Rhythm tasks activate left anterior brain regions (Platel et al., 1997), and meter tasks requiring semantic categorization (Zatorre, 1998) are impaired by anterior damage to either temporal lobe, whereas rhythm discrimination is affected by damage
MUSIC AFTER TEMPORAL LOBECTOMY
467
to the posterior temporal gyrus (Lie´geois-Chauvel et al., 1998). It is unclear how components of rhythm may be represented within the immature, damaged temporal lobe. For example, a comparison of rhythm and meter tasks may reveal a pattern of skill that varies by both laterality and distribution of temporal lobe damage. Although we found no lateralization effects for the rhythm task, rhythm (but not melody) varied with memory. Why rhythm rather than melody should be related to auditory memory function is not clear, although the results for children and adolescents are in agreement with the fact that some right temporal lobectomy subgroups have difficulty remembering rhythms (Penhune et al., 1999). The data do suggest that the manner in which the rhythm task was performed may vary by side of lobectomy, even when the outcome is not lateralized. Age at onset of epilepsy is a moderating influence on memory outcome after temporal lobectomy, at least for semantic and figural memory (Saykin et al., 1989). The present results do not confirm the second hypothesis, and show, instead, that age at onset was unrelated to either rhythm or melody. Age at test was important for melody in the right, but not left, lobectomy group, which emphasizes the developmental nature of musical skill. Given sufficient time, the right lobectomy individuals become more proficient at the melody task, although performance in the left lobectomy group is constant over age. Music experience, particularly before age 7, not only affects musical skills and musical imagery (Aleman, Nieuwenstein, Bocker, & de Haan, 2000), but influences the brain organization for music (e.g., Schlaug et al., 1995a, 1995b). Perhaps early seizures in the right temporal lobe prevent the facilitating effect of listening to and/or making music on the later brain organization for melody. In any event, studies of music in individuals with longstanding developmental brain compromise, such as those with childhood seizure disorders and subsequent temporal lobectomy, might consider outcome in relation to age at test. Extent of temporal lobe resection was unrelated to music in children and adolescents, in agreement with earlier studies of adults (e.g., Milner, 1962; Zatorre, 1985), and the data did not vary after excluding four individuals with continuing postsurgical seizures (presumably the group with most functional temporal lobe damage). In the absence of postsurgical functional imaging, it is difficult to identify the limits of the effective temporal lobe lesions in these children and adolescents. Nor do our data address the issue of how music might be represented within the immature temporal lobe on either side. Earlier studies suggested that music outcome after temporal lobectomy did not vary according to the involvement of Heschl’s gyrus (e.g., Milner, 1962), although later studies have suggested that some music outcomes depend on an interaction between side of lobectomy and involvement of Heschl’s gyrus. For example, Penhune et al. (1999) found that individuals with right temporal resections that included primary auditory cortex can retain a visual, but not an auditory, rhythm. In our children and adolescents, we cannot infer the extent of primary auditory cortex involvement from the extent of resection from the temporal pole. Excision of Heschl’s gyrus need not entail a larger total volume of resected cortical tissue, because the extent of resection along the first temporal gyrus is generally independent of removal along the third temporal convolution of the mesial aspect of the temporal lobe. Nor can we assess the specific anatomical claim that the right superior temporal gyrus is critical for the processing of melody (Lie´geois-Chauvel et al., 1998). Neuroimaging studies with children are required to clarify these issues. Finally, the data from children and adolescents with temporal lobectomy are in broad agreement with the idea that rhythm and pitch, two core elements of music (Krumhansl, 2000), might be processed by rather distinct brain mechanisms (Peretz, 1990). Future studies with children and adolescents after temporal lobectomy should
468
DENNIS AND HOPYAN
fractionate music within the domains of rhythm and pitch to better understand the developmental course of these mechanisms. REFERENCES Aleman, A., Nieuwenstein, M. R., Bocker, K. B. E., & de Haan, E. H. F. (2000). Music training and mental imagery ability. Neuropsychologia, 38, 1664–1668. Boone, K. B., & Rausch, R. (1989). Seashore Rhythm test performance in patients with unilateral temporal lobe damage. Journal of Clinical Psychology, 45, 614–618. Goldman, R., Fristoe, M., & Woodcock, R. W. (1974). Goldman–Fristoe–Woodcock Auditory Memory Tests. American Guidance Service, Circle Pines, Minnesota. Gordon, H. W., & Bogen, J. E. (1974). Hemispheric lateralization of singing after intracarotid sodium amylobarbitone. Journal of Neurology, Neurosurgery, and Psychiatry, 37, 727–738. Griffiths, T. D. (2000). Musical hallucinosis in acquired deafness—Phenomenology and brain substrate. Brain, 123, 2056–2076. Griffiths, T. D., Johnsrude, I., Dean, J. L., & Green, G. G. R. (1999). A common substrate for the analysis of pitch and duration pattern in segmented sound? Neuroreport, 10, 3825–3830. Hetherington, R., Dennis, M., & Spiegler, B. (2000). Perception and estimation of time in long-term survivors of childhood posterior fossa tumors. Journal of the International Neuropsychological Society, 6, 682–692. Johnsrude, I. S., Penhune, V. B., & Zatorre, R. J. (2000). Functional specificity in the right human auditory cortex for perceiving pitch direction. Brain, 123, 155–163. Kester, D. B., Saykin, A. J., Sperling, M. R., O’Connor, M. J., Robinson, L. J., & Gur, R. C. (1991). Acute effect of anterior temporal lobectomy on musical processing. Neuropsychologia, 29, 703– 709. Kirk, S. A., McCarthy, J. J., & Kirk, W. D. (1968). Illinois Test of Psycholinguistic Abilities. Examiner’s manual. (Rev. ed). Urbana, IL: University of Illinois Press. Kohn, B. (1980). Right-hemisphere speech representation and comprehension of syntax after left cerebral injury. Brain and Language, 9, 350–361. Koike, A., Shimizu, H., Suzuki, I., Ishijima, B., & Sugishita, M. (1996). Preserved musical abilities following right temporal lobectomy. Journal of Neurosurgery, 85, 1000–1004. Krumhansl, C. L. (2000). Rhythm and pitch in music cognition. Psychological Bulletin, 126, 159–179. Lie´geois-Chauvel, C., Peretz, I., Babaı¨, M., Laguitton, V., & Chauvel, P. (1998). Contribution of different cortical areas in the temporal lobes to music processing. Brain, 121, 1853–1867. Mazziotta, J. C., Phelps, M. E., Carson, R. E., & Kuhl, D. E. (1982). Tomographic mapping of human cerebral metabolism: Auditory stimulation. Neurology, 32, 921–937. Milner, B. (1962). Laterality effects in audition. In V. B. Mountcastle (Ed.), Interhemispheric relations and cerebral dominance (pp. 177–195). Baltimore, MD: Johns Hopkins Univ. Press. Penhune, V. B., Zatorre, R. J., & Evans, A. C. (1998). Cerebellar contributions to motor timing: A PET study of auditory and visual rhythm reproduction. Journal of Cognitive Neuroscience, 10, 752– 765. Penhune, V. B., Zatorre, R. J., & Feindel, W. H. (1999). The role of auditory cortex in retention of rhythmic patterns as studied in patients with temporal lobe removals including Heschl’s gyrus. Neuropsychologia, 37, 315–331. Peretz, I. (1990). Processing of local and global musical information by unilateral brain-damaged patients. Brain, 113, 1185–1205. Peretz, I., Kolinsky, R., Tramo, M., Labrecque, R., Hublet, C., Demeurisse, G., & Belleville, S. (1994). Functional dissociations following bilateral lesions of auditory cortex. Brain, 117, 1283–1301. Platel, H., Price, C., Baron, J-C., Wise, R., Lambert, J., Frackowiak, R. S. J., Lechevalier, B., & Eustache, F. (1997). The structural components of music perception. A functional anatomical study. Brain, 120, 229–243. Rademacher, J., Caviness, V. S., Steinmetz, H., & Galaburda, A. M. (1993). Topographical variation of the human primary auditory cortices: Implications for neuroimaging, brain mapping and neurobiology. Cerebral Cortex, 3, 313–329. Samson, S., & Zatorre, R. J. (1988). Melodic and harmonic discrimination following unilateral cerebral excision. Brain and Cognition, 7, 348–360.
MUSIC AFTER TEMPORAL LOBECTOMY
469
Samson, S., & Zatorre, R. J. (1991). Recognition memory for text and melody of songs after unilateral temporal lobe lesion: Evidence for dual encoding. Journal of Experimental Psychology: Learning, Memory, and Cognition, 17, 793–804. Samson, S., & Zatorre, R. J. (1992). Learning and retention of melodic and verbal information after unilateral temporal lobectomy. Neuropsychologia, 30, 815–826. Saykin, A. J., Gur, R. C., Sussman, N. M., O’Connor, M. J., & Gur, R. E. (1989). Memory deficits before and after temporal lobectomy: Effect of laterality and age at onset. Brain and Cognition, 9, 191–200. Schlaug, G., Ja¨ncke, L., Huang, Y., Staiger, J. F., & Steinmetz, H. (1995a). Increased corpus callosum size in musicians. Neuropsychologia, 33, 1047–1055. Schlaug, G., Ja¨ncke, L., Huang, Y., & Steinmetz, H. (1995b). In vivo evidence of structural brain asymmetry in musicians. Science, 267, 699. Seashore, C. E., Lewis, D., & Saetveit, J. G. (1960). Seashore Measure of Musical Talents, Manual revised. New York: Psychological Corp. Zatorre, R. J. (1985). Discrimination and recognition of tonal melodies after unilateral cerebral excisions. Neuropsychologia, 23, 31–41. Zatorre, R. J. (1998). Functional specialization of human auditory cortex for musical processing. Brain, 121, 1817–1818. Zatorre, R. J., Evans, A. C., & Meyer, E. (1994). Neural mechanisms underlying melodic perception and memory for pitch. Journal of Neuroscience, 14, 1908–1919.