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Neural Correlates of Timbre Change in Harmonic Sounds

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Neural Correlates of Timbre Change in Harmonic Sounds NeuroImage 17, 1742–1754 (2002) doi:10.1006/nimg.2002.1295 Neural Correlates of Timbre Change in Harmonic Sounds V. Menon,*,†,‡ D. J. Levitin,§ B. K. Smith,࿣ A. Lembke,* B. D. Krasnow,* D. Glazer,¶ G. H. Glover,‡,¶ and S. McAdams࿣ *Department of Psychiatry and Behavioral Sciences, †Program in Neuroscience, ‡Stanford Brain Research Center, Stanford University School of Medicine, Stanford, California 94305; §Department of Psychology, McGill University, Montre´al, Que´bec, Canada; ࿣Institut de Recherche et Coordination Acoustique/Musique (IRCAM-CNRS), Paris, France; and ¶Department of Radiology, Stanford University School of Medicine, Stanford, California 94305 Received October 22, 2001 known about the psychological representation of timbre (Mc- Timbre is a major structuring force in music and one Adams and Cunibile, 1992; McAdams and Winsberg, 2000; of the most important and ecologically relevant fea- McAdams et al., 1995; Pitt, 1995) but relatively little is tures of auditory events. We used sound stimuli se- known about its neural underpinnings (Shamma, 1999). This lected on the basis of previous psychophysiological report is the first in a series of experiments designed to studies to investigate the neural correlates of timbre uncover the functional neuroanatomy of timbre perception in perception. Our results indicate that both the left and humans and its relation to human psychophysics. right hemispheres are involved in timbre processing, “Timbre” refers to those aspects of sound quality other challenging the conventional notion that the elemen- than pitch, loudness, perceived duration, spatial location, tary attributes of musical perception are predomi- and reverberant environment (McAdams, 1993; Plomp, 1970; nantly lateralized to the right hemisphere. Significant Risset and Wessel, 1999). More generally, timbre can be timbre-related brain activation was found in well-de- defined as that feature of an auditory stimulus that allows us fined regions of posterior Heschl’s gyrus and superior to distinguish one source from another when all of the other temporal sulcus, extending into the circular insular five perceptual features are held constant. That is, timbre is sulcus. Although the extent of activation was not sig- the “tonal color and texture” that allows us to distinguish a nificantly different between left and right hemi- trumpet from a clarinet playing the same note or to distin- spheres, temporal lobe activations were significantly guish one speaker from another when they are reciting the posterior in the left, compared to the right, hemi- same words. In spite of its prime importance in identification sphere, suggesting a functional asymmetry in their and memory, timbre is one of the least understood compo- respective contributions to timbre processing. The im- nents of auditory perception. Helmholtz was the first to rec- plications of our findings for music processing in par- ognize that it is to some extent related to a tone’s spectral ticular and auditory processing in general are dis- composition (Helmholtz, 1863/1954). More recent investiga- cussed. © 2002 Elsevier Science (USA) tors have found that it is crucially related not just to spectral Key Words: timbre; temporal lobe; superior temporal parameters but also to the temporal aspects of tone, such as gyrus; superior temporal sulcus; middle temporal gy- the rate of increase in level or the presence of inharmonic rus; fMRI. components in the initial part of the tone (Grey, 1977), acous- tic features that affect the “attack quality” (Hajda et al. INTRODUCTION 1997). For example, a piano is easily recognized as such in a taped recording, but if that same recording is played back- An auditory event comprises six general classes of percep- wards, the distinct timbre that identifies “piano” is lost, even tual attributes: pitch, loudness, timbre, perceived duration, though the long-term frequency spectrum remains un- spatial location, and reverberant environment (Levitin, changed for any given tone (Berger, 1964). 1999). Of these six, timbre is arguably the most important Accurate memory for the timbral qualities of everyday and ecologically relevant feature of auditory events. The tim- music was shown recently in a compelling study by Schellen- bre of a sound is the principal feature that distinguishes the berg and his colleagues (1999). Participants in this study growl of a lion from the purr of a cat, the crack of thunder were able to identify popular songs from brief excerpts of only from the crash of ocean waves, the voice of a friend from that 100 and 200 ms. The authors argued that this was too brief of a bill collector one is trying to dodge. Timbral discrimina- an excerpt for cues such as rhythm, pitch, or tonality to tion is so acute in humans that most of us can recognize trigger memory and that it must have been timbral memory hundreds of different voices and, within a single well-known that was being accessed. Timbral memory may also be the voice, distinguish whether its possessor is in good health or mechanism by which some absolute pitch possessors identify suffering from a cold—even over the telephone. Much is now tones (Takeuchi and Hulse, 1993). The distinctive sound of a 1053-8119/02 $35.00 1742 © 2002 Elsevier Science (USA) All rights reserved. NEURAL CORRELATES OF TIMBRE 1743 spectral centroid (a measure of the relative presence of high- frequency versus low-frequency energy in the frequency spec- trum), and spectral flux (a measure of how much the spectral envelope changes over the duration of a tone). Although the psychoacoustics of timbre continues to be extensively investigated (McAdams et al., 1995), information about its neural substrates remains sparse. In general, lesion studies have shown that the right temporal lobe is involved in spectral processing, i.e., pitch matching, frequency dis- crimination (Milner, 1962; Robin et al. 1990; Sidtis and Volpe, 1988; Zatorre, 1988), and the left temporal lobe is involved in temporal processing (Efron, 1963; Robin et al., 1990). Samson and Zatorre (1994) examined timbre discrim- ination in patients with unilateral temporal lobe excisions, right and left, while manipulating both the spectral and temporal components of timbre. To their surprise, only those subjects with right temporal lobe excisions were impaired in timbre discrimination, independently of the temporal and spectral cues. These findings support a functional role for the right temporal lobe in timbre discrimination, but leave am- biguous the role of the left temporal lobe, if any. A few neuroimaging studies have examined the neural basis of music perception in general, with attempts to frac- tionate musical processing into component operations. The emerging picture is that music perception per se does not FIG. 1. The timbre space for 18 synthetic musical instrument have a specific neural locus, but that the components of music sounds found by McAdams et al. (1995). A three-dimensional space perception—specifically pitch and rhythm—may. One early with acoustic correlates of attack time, spectral centroid, and spec- PET study showed a specialized role for the right temporal tral flux was found. For comparison, Timbres A and B from the lobe in pitch perception (Zatorre et al., 1993); a more recent present study are shown approximately as they would appear in the PET study by Griffiths et al. (1999) showed remarkably sim- space on the basis of these same acoustic parameters. Note that the ilar bilateral activation for both pitch and duration, in the change from Timbre A to Timbre B occurs as a diagonal across the space since all three dimensions change. cerebellum, posterior superior temporal cortices, and inferior frontal cortices. A PET study by Blood et al. (1999) examined affective processing of musical pieces and found activation of piano or saxophone—presumably based on its timbre—is be- neocortical and paralimbic structures in response to pleas- lieved to serve as a cue for pitch identification among abso- ant/unpleasant musical stimuli. Belin et al. (2000) found lute pitch possessors who are unable to identify the pitch of regions in the superior temporal sulcus (bilaterally) that sine tones or of instruments with which they are less famil- were involved in the processing of human voices. Although iar. the study did not explicitly address timbre perception, tim- The psychological space for timbre representation has been bre-related attributes would have been among the primary investigated in an extensive series of studies by McAdams cues for subjects in this experiment to distinguish human and his colleagues, among others. Since the work of Plomp from environmental sounds and to distinguish human voices (1970), the principal paradigm for uncovering the perceptual from one another. structure of timbre has employed multidimensional scaling The functional neuroanatomy of timbre perception in hu- of dissimilarity judgments among sets of musical sounds mans remains almost entirely unknown, and yet this impor- equated for pitch, loudness, and duration and generally pre- tant topic may hold the key to understanding fundamental sented over headphones or loudspeakers (see McAdams, questions about voice identification, musical processing, and 1993; Hajda et al., 1997, for reviews). Over many different memory for the numerous sound sources encountered in ev- studies, two or three perceptual dimensions are generally eryday life. The only known study to date identified right extracted. The acoustic correlates of these “timbre spaces” superior and middle frontal gyrus as candidates for selective depend on the set of sounds tested and to some extent the attending to timbre in the presence of simultaneous variation listener population. For example, using a set of synthesized in pitch and rhythm (Platel et al., 1997), yet this finding is sounds designed to imitate orchestral instruments or hybrids difficult to interpret for several reasons: first, the timbral of these instruments, McAdams et al. (1995) found a three- change was subtle and primarily spectral in nature (a dimensional space with specific features on several of the “bright” vs “dull” oboe) and second, the data analysis em- timbres (Fig.
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