Neural Correlates of Timbre Change in Harmonic Sounds

NeuroImage 17, 1742–1754 (2002) doi:10.1006/nimg.2002.1295

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), acoustic 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

spectral centroid (a measure of the relative presence of high- frequency versus low-frequency energy in the frequency spectrum), 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 discrimination (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 discrimination 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. 1). The acoustic correlates of the commonly ployed a subtraction in which selective attending to timbral shared dimensions were the logarithm of the attack time (the change was compared to selective attending to pitch and time it takes the energy envelope to go from perceptual rhythm changes. Johnsrude et al. (1997) examined process- threshold to its maximum), the spectral center of gravity, or ing of acoustic transients in nonspeech sounds using PET. 1744 MENON ET AL.

This study is of particular interest because psychophysical bits. Each sound had an amplitude envelope defined in terms and cognitive studies of timbre have shown transients to be of linear attack time (AT), sustain time (ST), and exponential an important component in timbral identification and recog- decay time (DT). These three values were, respectively, 15, nition (Berger, 1964). Participants in this study discrimi- 60, and 198 ms for Timbre A and 80, 0, and 117 ms for Timbre nated pure tone stimuli incorporating frequency glides of B (Fig. 2). The main interest was in attack time and the other either long (100 ms) or short (30 ms) duration. Comparison of two values were adjusted to achieve similar perceived dura- these two conditions revealed significant activation foci in tions across the two timbres. The sounds were composed of the left orbitofrontal cortex, left fusiform gyrus, and right harmonic spectra. The levels of the harmonies decreased as a p cerebellum. The left hemisphere activations are consistent power function of harmonic rank (An ϭ n ). The exponent p of with previously cited work implicating left hemisphere struc- this function was used to establish the base spectral centroid tures for temporal processing (Efron, 1963; Robin et al., (SCbase), which is defined as the amplitude-weighted mean 1990). harmonic rank. For a pure tone SCbase ϭ 1, whereas for a Based therefore on psychophysical models of timbre per- tone composed of the first three harmonics with amplitudes ception, which point to an important role for both spectral equal to the inverse of the harmonic rank, SCbase ϭ (1*1 ϩ and temporal parameters of sound, we hypothesized a critical 2*1/2 ϩ 3*1/3)/(1 ϩ 1/2 ϩ 1/3) ϭ 1.63. Expressed in this way, role for the the left and right temporal lobes in tasks involv- the relative amplitudes among harmonics remain constant ing timbral processing, as well as those left hemisphere re- with variations in fundamental frequency. Spectral flux gions previously implicated by Johnsrude et al.’s (1997) study (⌬SC, expressed as a change in amplitude-weighted mean of transient perception. In order to maximize the difference harmonic rank) was defined as a variation over time of SC along acoustic dimensions known to affect timbre perception, with a rise time SCRT and a fall time SCFT. Between time 0 we selected two types of sounds that differed maximally in and SCRT, SC rose from SCbase to SCbase ϩ⌬SC, following terms of attack time, spectral centroid, and spectral flux, as a raised cosine trajectory. From time SCRT to SCRT ϩ SCFT, found by McAdams et al. (1995). The two distinct timbre SC decreased back to SCbase, following a slower raised co- stimuli (A and B) created for the present experiment differed sine trajectory. After time SCRT ϩ SCFT, SC remained con- significantly along these three dimensions. Their approxi- stant at SCbase. Timbre A was characterized by a fast attack mate positions with respect to the original space are shown in (AT ϭ 15 ms), a low base spectral centroid (SCbase ϭ 1.05), Fig. 1. Our experimental design was as follows. We compared and no spectral flux (⌬SC ϭ 0). Timbre B was characterized brain activation in response to melodies composed of tones by a slower attack (AT ϭ 80 ms), a higher base spectral with a fast attack, low spectral centroid, and no spectral flux centroid (SCbase ϭ 1.59), and a higher degree of spectral flux (Timbre A) to that resulting from melodies formed of tones (⌬SC ϭ 4.32, SCRT ϭ 49 ms, SCFT ϭ 102). For Timbre B, the with a slow attack, higher spectral centroid, and greater instantaneous SC therefore varied from 1.59 to 5.91 between spectral flux (Timbre B). The theoretical interest in these 0 and 49 ms and from 5.91 back to 1.59 between 49 and 151 sounds is that they include spectral, temporal, and spectro- ms, remaining at 1.59 thereafter (Fig. 2). Prior to the exper- temporal parameters that have been shown to be correlated imental session, the two timbre stimuli were matched psy- with perceptual dimensions of timbre. A case in which tim- chophysically for loudness by four raters, and this necessi- bres changed across the entire perceptual space needed to be tated attenuating the sounds with Timbre B by 8.5 dB tested first in order to demonstrate that perceptually salient compared to those with Timbre A. stimuli reveal differences in activation as measured with Stimuli consisted of 60 six-note melodies played with these fMRI. The critical question is thus: what are the character- timbres. The range of fundamental frequencies was 288.2 Hz istics of brain responses associated with differences in me- (C No. 4) to 493.9 Hz (B4). One of these melodies, realized lodic stimuli created with precisely controlled synthetic with each of the timbres, is shown in a spectrographic rep- sounds having different timbres? resentation in Fig. 2. Ten melodies with a given timbre con- stituted a block. All melodies were tonal and ended on the MATERIALS AND METHODS tonic note. The pitch range was confined to an octave but varied from five to nine semitones across melodies: 21 melo- Subjects dies had a range with five semitones (ST), 21 with seven ST, Ten healthy adult subjects (4 males and 6 females; ages and 18 with nine ST. Each block had 3 or 4 five-ST melodies, 21–45, mean 33) participated in the study after giving writ- 3 or 4 seven-ST melodies, and 3 nine-ST melodies. Thirty ten informed consent, and all protocols were approved by the melodies had one contour change, and 30 had two changes human subjects committee at Stanford University School of (five of each per block). There were 36 major-mode and 24 Medicine. All participants were volunteers and were treated minor-mode melodies (6 major/4 minor per group). Key in accordance with the APA “Ethical Principles of Psycholo- changed from melody to melody in order to keep the mean gists and Code of Conduct.” pitch constant across melodies. An attempt was also made to keep the pitch distribution relatively constant across blocks. The time interval between onsets of successive tones within Stimuli a melody was 300 ms, making the total duration of each All sounds were created digitally using a 22,050-Hz sam- melody approximately 1.8 s for Timbre A melodies and 1.7 s pling rate and 16-bit resolution, although stimulus presen- for Timbre B melodies. A new melody occurred every 2.4 s tation in the MRI scanner used only the 8 most significant and a block of 10 melodies thus lasted 24 s. NEURAL CORRELATES OF TIMBRE 1745

FIG. 2. Acoustic features of Timbre A (top) and Timbre B (bottom). (Left panel) Spectrographic representation of one of the stimulus melodies. The level is indicated by the darkness of the gray scale. The range represented by the gray scale is approximately 90 dB. (Top right panel) The amplitude envelope of a single tone, representing the rms amplitude as a function of time. (Bottom right panel) The spectral flux function for a single tone, representing the variation of the spectral centroid (SC) over time. fMRI Tasks the scan and practiced the experiment prior to entering the scanner. Each subject performed two runs of the same experiment in the scanner. Each experiment consisted of 12 alternating Behavioral Data Analysis 24-s epochs (epochs of 10 melodies with a given timbre), for a total of 120 melodies per scan. There were 6 Timbre A epochs The aim of the behavioral data collection was to verify that interleaved with 6 Timbre B epochs. Each of the six blocks of listeners were paying attention to the stimuli to the same ten melodies was presented for each timbre, but the order of extent for A and B epochs. Reaction time (RT) and number of blocks and the order of melodies within blocks were random- correct and incorrect responses for A and B epochs were ized for each subject. Subjects were asked to engage their collapsed across the two runs. A response was considered attention on the melodies. For each six-note melody they correct if the subject pressed the appropriate response key were asked to press a response key as soon as the melody was after the end of the musical segment, but before the onset of over. In one run, the first epoch was played with Timbre A, the next stimulus. The percentages of correct responses and and in the second run, the first epoch was played with RTs to correct trials were compared using two-tailed paired t Timbre B. tests. The significance threshold was set at 0.05.

Procedure fMRI Acquisition The order of the two runs was randomized across subjects. Images were acquired on a 3T GE Signa scanner using a They were briefed on the task they were to perform during standard GE whole head coil (software Lx 8.3). A custom- 1746 MENON ET AL. built head holder was used to prevent head movement; 25 using least squares minimization without higher order cor- axial slices (5 mm thick, 0 mm skip) parallel to the AC/PC rections for spin history (Friston et al., 1996) and were nor- line and covering the whole brain were imaged with a tem- malized to stereotaxic Talairach coordinates using nonlinear poral resolution of 1.6 s using a T2*-weighted gradient echo transformations (Ashburner and Friston, 1999; Friston et al., spiral pulse sequence (TR, 1600 ms; TE, 30 ms; flip angle, 1996). Images were then resampled every 2 mm using sinc 70°; 180 time frames; and one interleave) (Glover and Lai, interpolation and smoothed with a 4-mm Gaussian kernel to 2 1998). The field of view was 220 ϫ 220 mm , and the matrix reduce spatial noise. size was 64 ϫ 64, providing an in-plane spatial resolution of 3.44 mm. To reduce blurring and signal loss arising from field inhomogeneities, an automated high-order shimming Statistical Analysis method based on spiral acquisitions was used before acquir- ing functional MRI scans (Kim et al., 2000). Images were Statistical analysis was performed on individual and group reconstructed, by gridding interpolation and inverse Fourier data using the general linear model and the theory of Gauss- transform, for each of the 180 time points into 64 ϫ 64 ϫ 25 ian random fields as implemented in SPM99. This method image matrices (voxel size, 3.44 ϫ 3.44 ϫ 5 mm). A linear takes advantage of multivariate regression analysis and cor- shim correction was applied separately for each slice during rects for temporal and spatial autocorrelations in the fMRI reconstruction using a magnetic field map acquired automat- data (Friston et al., 1995). Activation foci were superimposed ically by the pulse sequence at the beginning of the scan on high-resolution T1-weighted images and their locations (Glover and Lai, 1998). were interpreted using known neuroanatomical landmarks To aid in localization of functional data, a high-resolution (Duvernoy et al., 1999). MNI coordinates were transformed to T1-weighted spoiled grass gradient recalled (SPGR) inver- Talairach coordinates using a nonlinear transformation sion recovery 3D MRI sequence was used with the following (Brett, 2000). parameters: TI, 300 ms; TR, 8 ms; TE, 3.6 ms; flip angle, 15°; A within-subjects procedure was used to model all the 22-cm field of view; 124 slices in the sagittal plane; 256 ϫ 192 effects of interest for each subject. Individual subject models matrix; two averages; acquired resolution, 1.5 ϫ 0.9 ϫ 1.1 were identical across subjects (i.e., a balanced design was mm. The images were reconstructed as a 124 ϫ 256 ϫ 256 used). Confounding effects of fluctuations in the global mean matrix with a 1.5 ϫ 0.9 ϫ 0.9 mm spatial resolution. Struc- were removed by proportional scaling where, for each time tural and functional images were acquired in the same scan point, each voxel was scaled by the global mean at that time session. point. Low-frequency noise was removed with a high-pass filter (0.5 cycles/min) applied to the fMRI time series at each Stimulus Presentation voxel. A temporal smoothing function (Gaussian kernel cor- responding to a half-width of 4 s) was applied to the fMRI The task was programmed using Psyscope (Cohen et al., time series to enhance the temporal signal to noise ratio. 1993) on a Macintosh (Cupertino, CA) computer. Initiation of Regressors were modeled with a boxcar function correspond- scan and task was synchronized using a TTL pulse delivered ing to the epochs during which each timbre was presented to the scanner timing microprocessor board from a “CMU and convolved with a hemodynamic response function. We Button Box” microprocessor (http://poppy.psy.cmu.edu/ then defined the effects of interest for each subject with the psyscope) connected to the Macintosh. Auditory stimuli were relevant contrasts of the parameter estimates. Group analy- presented binaurally using a custom-built magnet compati- sis was performed using a random-effects model that incor- ble system. This pneumatic delivery system was constructed porated a two-stage hierarchical procedure. This model esti- using a piezoelectric loudspeaker attached to a cone-shaped mates the error variance for each condition of interest across funnel, which in turn was connected to flexible plastic tubing subjects, rather than across scans, and therefore provides a leading to the participant’s ears. This delivery system filters stronger generalization to the population from which data the sound with an overall low-pass characteristic and a spec- are acquired (Holmes and Friston, 1998). In the first stage, tral dip in the region of 1.5 kHz (Fig. 3). The tubing passed through foam earplug inserts that attenuated external sound contrast images for each subject and each effect of interest by approximately 28 dB. The sound pressure level at the were generated as described above. In the second stage, these head of the participant due to the fMRI equipment during contrast images were analyzed using a general linear model scanning was approximately 98 dB (A), and so after the to determine voxelwise t statistics. One contrast image was attenuation provided by the ear inserts, background noise generated per subject, for each effect of interest. A one-way, was approximately 70 dB (A) at the ears of the listener. The two-tailed t test was then used to determine group activation experimenters set the stimuli at a comfortable listening level for each effect. Finally, the t statistics were normalized to Z determined individually by each participant during a test scores, and significant clusters of activation were determined scan. using the joint expected probability distribution of height and extent of Z scores (Poline et al., 1997), with height (Z Ͼ 1.67; P Ͻ 0.05) and extent (P Ͻ 0.05) thresholds. Image Preprocessing Contrast images were calculated using a within-subjects fMRI data were preprocesssed using SPM99 (http://www. design for the following comparisons: (1) Timbre B–Timbre fil.ion.ucl.ac.uk/spm). Images were corrected for movement A; (2) Timbre A–Timbre B. NEURAL CORRELATES OF TIMBRE 1747

FIG. 3. Fourier spectra (red) for Timbres A and B (left and right panels, respectively). The spectra were computed on 2048-sample (46 ms) segments with a Hanning window in the middle of the second tone from melody 1 (Fig. 2). The top panels show the spectra at the output of the computer’s converters. The bottom panels show the sound after filtering by the pneumatic delivery system. Note an overall low-pass characteristic plus a dip in the spectrum in the region of 1500 Hz. The filtering affects Timbre B sounds more than Timbre A sounds, but the two are still quite distinct spectrally. Also superimposed on the bottom panels is the estimated spectrum of the scanner noise (black). This noise could not be recorded under the same conditions due to the magnetic field of the scanner. This relative level is roughly estimated to correspond to that present in the headphone system. It does not take into account filtering by the headphones, which would be quite variable in the low-frequency region depending on the fit of the headphones to the head of each listener, nor the fact that the stimulus level was adjusted individually for each listener. FIG. 4. Surface rendering of brain activation in response to Timbre B stimuli compared to Timbre A stimuli. Significant clusters of activation were observed in the central sections of the STG and STS. Note that left hemisphere activations are posterior to right hemisphere activations. No brain regions showed greater activation in response to Timbre B stimuli, compared to those with Timbre A.

RESULTS for Timbre A and 99.8 Ϯ 1.0% for Timbre B. RTs were 1914 Ϯ 59.5 and 1931 Ϯ 76.0 ms for Timbres A and B, respectively. Behavioral We conclude that there were no behavioral differences (and End-of-melody detections did not differ in accuracy be- thus no confounding attentional or arousal differences) between A and B blocks (t(8) ϭϪ0.900; P ϭ 0.40), nor did RT tween the two sets of stimulus blocks containing the two (t(8) ϭϪ1.876; P ϭ 0.10). Accuracy rates were 99.5 Ϯ 2.8% timbres. 1748 MENON ET AL.

TABLE 1 Brain Regions That Showed Signiﬁcant Activation Differences between the Two Timbre Stimuli

P value No. of Peak (corrected) voxels Z score Talairach coordinates

Timbre B–Timbre A Right STG/STS (BA 41/22/21) Ͻ0.001 297 3.31 50, Ϫ8, Ϫ4 Left STG/STS (BA 41/22/21) Ͻ0.002 285 2.55 Ϫ36, Ϫ24, 8 Timbre A–Timbre B No signiﬁcant clusters —— —

Note. For each significant cluster, region of activation, significance level, number of activated voxels, maximum Z score, and location of peak in Talairach coordinates are shown. Each cluster was significant after height and extent correction (P Ͻ 0.05). STG, superior temporal gyrus; MTG, middle temporal gyrus; BA, Brodmann Area.

Brain Activation 0.21; P ϭ 0.66), nor were mean Anterior/Posterior differences (F(1,8) ϭ 0.72; P Ͻ 0.42). Timbre B–Timbre A. Two significant, tightly focused, Timbre A–Timbre B. No brain regions showed greater clusters of activation were observed in both the left and right activation during Timbre A compared to Timbre B. temporal lobes (Table 1, Fig. 4). In both hemispheres, the main activation foci were localized to the dorsomedial surface of the superior temporal gyrus (STG) (BA 41/42/22), adjoin- DISCUSSION ing the insular cortex and extending to the upper and lower banks of the STS (BA 21). Additionally, in the left hemi- Our findings strongly support the notion that timbre-re- sphere, a more posterior and medial activation focus overly- lated information is processed in both the left and right ing the circular insular sulcus was also observed. hemispheres. Furthermore, timbre-related differences in ac- Seven of the nine subjects showed significant activation in tivation were detected only in mid sections of the STG, STS, the left temporal lobe cluster and eight also showed activa- and adjoining insular cortex. Although the overall extent of tion in the right temporal lobe cluster. There was no differ- activation was not significantly different in the left and right ence overall between the percentages of voxels activated in temporal lobes, left temporal lobe activations were signifi- left and right temporal lobes (Wilcoxon matched pairs test, cantly posterior to right temporal lobe activations, suggest- Z ϭ 0.296; P ϭ 0.76). Similarly, no difference was seen in the ing a functional asymmetry in the left and right temporal average intensity of activation between the two hemispheres lobe regions involved in timbre processing. The present study (Z ϭ 1.006; P ϭ 0.31). Interestingly, activation in the left provides information about the precise temporal lobe regions temporal lobe was posterior to the right temporal lobe acti- involved in timbre processing. The implications of these find- vation (Fig. 5). In the left hemisphere, the most anterior ings for timbre processing are discussed below. activation point was at Ϫ34, Ϫ20, 8 and the most posterior Specifically, we found that timbre stimuli with greater point was at Ϫ41, Ϫ40, 10. In the right hemisphere, the most spectral flux, higher spectral centroid, and slower attack anterior point was at 54, Ϫ4, Ϫ8, and the most posterior (Timbre B) resulted in greater activation than timbre stimuli point was at 40, Ϫ28, Ϫ6. with low spectral centroid, no spectral flux, and faster attack To quantify this asymmetry in activation, we examined the (Timbre A). No brain regions showed significantly greater number of voxels activated anterior and posterior to y ϭϪ22 activation during Timbre A compared to Timbre B. Another (midway between the anteriormost and posteriormost acti- functional imaging study of timbre processing identified the vations). Only 14 voxels were activated in the left anterior right superior and middle frontal gyri as brain regions in- region compared to 271 in the left posterior region, whereas volved in timbral processing (Platel et al., 1997), a finding 286 voxels were activated in the right anterior region com- that was based on a comparison of selective attending to pared to only 11 in the right posterior region. Three of the timbral change with selective attending to pitch or rhythm nine subjects had no activated voxels in the left anterior change rather than a direct comparison of two distinct timbre region and six had no activation in the right posterior region. stimuli. The present study did not find significant activation To further analyze the asymmetry in activation, we exam- in these regions. The lack of prefrontal cortical activation in ined the Hemisphere by Anterior/Posterior interaction using the present study may be related to the fact that subjects did Analysis of Variance (ANOVA). For this analysis, we con- not have to make any complex comparisons or decisions structed identical and (left/right) mirror symmetric regions of about the timbre stimuli, nor did the task require the in- interest (ROI) in the left and right hemispheres based on the volvement of selective attentional processes. Unlike the Pla- observed group activation. Within these ROIs, the number of tel et al. study, which used a subtle, primarily spectral tim- voxels activated in each Hemisphere in the Anterior and bral change (“bright” vs “dull” oboe), the present study used Posterior subdivisions was computed for each subject. As timbre stimuli that have been shown to be perceptually very shown in Fig. 6, ANOVA revealed a significant Hemisphere x dissimilar (McAdams et al., 1995). The subtle timbral Anterior/Posterior interaction (F(1,8) ϭ 20.11; P Ͻ 0.002). changes may also have been the reason for the lack of tem- Mean hemispheric differences were not significant (F(1,8) ϭ poral lobe activation in the Platel et al. study. Our data are in NEURAL CORRELATES OF TIMBRE 1749 agreement with those of lesion studies which have suggested Our results also bear upon the cortical representation of involvement of the temporal lobe in timbre processing (Mil- loudness and its examination using fMRI since the fMRI ner, 1962; Samson and Zatorre, 1994). Lesion studies from activation patterns of two loudness-matched stimuli are so the Montreal Neurological Institute have reported that right unbalanced. Studies of the effect of sound level on the extent temporal lobe lesions result in greater impairment in timbre and level of temporal lobe activation have shown complex discrimination than left temporal lobe lesions (Milner, 1962; relationships based on the nature of pure/harmonic-complex Samson and Zatorre, 1994). Nevertheless, a closer look at the tones used (Hall et al., 2001) as well as the precise subregion published data also suggests that left temporal lesions do and laterality of the auditory cortical activation examined impair timbre discrimination. These studies have not, how- (Brechmann et al., 2002). For example, sound level had a ever, provided any details of the precise temporal lobe re- small, but significant, effect on the extent of auditory cortical gions involved in timbre perception and have instead focused activation for the pure tone, but not for the harmonic-com- on examining the relative contributions of the entire left and plex tone, while it had a significant effect on the response right temporal lobes to timbre processing. The present study magnitude for both types of stimuli (Hall et al., 2001). Fur- clearly indicates that focal regions of the left and right tem- thermore, the relationships among sound level, loudness per- poral lobes are involved in timbre processing. ception, and intensity coding in the auditory system are Equal levels of activation were detected in the left and complex (Moore, 1995). In any case, our results discount right temporal lobes. To our knowledge, lateralization of simple models for loudness that are based, implicitly or ex- timbre-related activation has never been directly tested be- plicitly, on the degree of activation of neural populations. fore. Within the temporal lobes, activation was localized to Although there were no overall hemispheric differences in the primary auditory cortex (PAC) as well as the auditory extent of activation, our results clearly point to differences in association areas in the belt areas of the STG and in the STS. the specific temporal lobe regions activated in the left and Anteriorly, the activation foci did not extend beyond Heschl’s right hemispheres. ANOVA revealed that distinct subregions gyrus (HG) (Howard et al., 2000; Kaas and Hackett, 2000; of the STG/STS were activated in each hemisphere: activa- Tian et al., 2001). The most anterior activation point was at tion in the left hemisphere was significantly posterior to right hemisphere activation, with very few voxels showing activa- y ϭϪ4 mm (Talairach coordinates) in the right temporal tion in the anterior regions (y ϾϪ22) in the left hemisphere. lobe. The bilateral activation observed in the present study is Conversely, very few voxels showed activation in the poste- in agreement with human electrophysiological studies that rior regions (y ϽϪ22) in the right hemisphere. These results have found bilateral N100 sources during timbre-specific pro- point to a hemispheric asymmetry in neural response to cessing (Crummer et al., 1994; Jones et al., 1998; Pantev et timbre; indeed, the location of peak activation in left auditory al., 2001). cortex was 16 mm posterior to that of peak activation in right Interestingly, activation for Timbre B was greater than auditory cortex. This shift is 8–11 mm more posterior than that for Timbre A, despite the matching of the two stimuli for can be accounted for by morphological differences in the loudness. One plausible explanation is that Timbre B has a locations of the left and right auditory areas (Rademacher et greater spectral spread (or perceivable spectral bandwidth) al., 2001). Based on a detailed cytoarchitectonic study of than Timbre A and would thus have a more extensive tono- postmortem brains, Rademacher et al. have reported a sta- topic representation, at least in the primary and secondary tistically significant asymmetry in the location of the PAC in auditory cortices (Howard et al., 2000; Wessinger et al., the left and right hemispheres. The right PAC is shifted 2001). While the two timbres have the same number of har- anteriorly by 7 or 8 mm and laterally by 4 or 5 mm, with monics and thus ideally would have the same bandwidths, it respect to the left PAC. An almost identical pattern of func- is likely that the higher harmonics of Timbre A are below the tional asymmetry was observed in the present study—the auditory threshold and/or masked by the scanner noise, thus right hemisphere activation peak was shifted more anteriorly creating a perceptible bandwidth difference. Bandwidth dif- and laterally than the activation peak in the left hemisphere. ferences were also present in the Wessinger et al. (2000) and While the centroid of the right PAC is roughly shifted by Hall et al. (2001) studies. However, in all three cases, other ⌬X ϭ 4, ⌬Y ϭ 8, and ⌬Z ϭ 1 mm, the peak fMRI activations factors were also varied (the relative periodicity of the signals in the present study are shifted by ⌬X ϭ 14, ⌬Y ϭ 16, and in Wessenger et al., the pitch in Hall et al., and attack time ⌬Z ϭϪ12 mm in the X, Y, and Z directions, respectively. and spectral flux in the present study), so the true contribu- Thus, even after accounting for the anatomical asymmetry in tion of bandwidth per se cannot be unambiguously deter- location of the PAC, left hemisphere activation is still con- mined. Another possibility is that the greater spectral flux in siderably posterior to right hemisphere activation, thus sug- Timbre B may result in greater cortical activation, particu- gesting a functional asymmetry in the left and right temporal larly in the STS, as this region appears to be sensitive to lobe contributions to timbre processing. Furthermore, these temporal changes in spectral distribution. Finally, the rela- hemispheric differences do not appear to arise from volumet- tive salience of the stimuli may also be important since ric differences since careful measurements of the highly con- Timbre B is clearly more salient perceptually than A, but it is voluted auditory cortex surface have revealed no size differ- not easy to measure “salience” per se. At any rate, it may not ence between the left and right PAC or HG (Rademacher et be possible to independently control salience and timbre, al., 2001). Moreover, the functional asymmetry observed dur- since some timbral attributes, such as brightness and sharp ing timbre processing extends beyond the dorsal STG to the attack, generally seem to make sounds “stand out.” STS and the adjoining circular insular sulcus as well. 1750 MENON ET AL.

FIG. 5. (a) Coronal and (b) axial sections showing brain activation in response to Timbre B stimuli, compared to those with Timbre A. Activation is shown superimposed on group-averaged, spatially normalized, T1-weighted images. In each hemisphere, two distinct subclusters of activation could be clearly identiﬁed, one in the dorsomedial STG and the other localized to the STS. The activations also extend into the circular insular sulcus and insula. See text for details.

In each hemisphere, two distinct subclusters of activation borders the circular sulcus medially, the first transverse could be clearly identified, one in the STG and the other sulcus anteriorly, and the roof of HG caudolaterally. The localized to the STS. The anteriormost aspects of the dorso- caudally adjacent T2 was centered on Heschl’s sulcus, thus medial STG activations in both hemispheres were localized including the posterior rim of HG and a similar area behind to a stripe-like pattern of activation in area T1b which fol- the sulcus on the anterior planum temporale/second Heschl’s lows the rostromedial slope of HG (Brechmann et al., 2002). gyrus. There is very little activation in area T1a, the division In the left hemisphere, the activation extends posteriorly to of the HG rostral to the first transverse sulcus. Areas T1a area T2, which is centered on Heschl’s sulcus. In both hemi- and T1b overlap to a great extent the PAC probability maps spheres, the activations appear to be anterior to area T3, and Talairach coordinate ranges reported by Rademacher et which principally overlaps the main body of the planum al. (2001). Based on the landmarks identified by Rademacher temporale. As defined by Brechmann et al. (2002), area T1b et al. and Brechmann et al., it therefore appears that in the NEURAL CORRELATES OF TIMBRE 1751

FIG. 5—Continued

left hemisphere, the dorsal STG activation extends posteri- primarily from primary and secondary auditory cortices in orly beyond the PAC to the posterior HG/anterior tip of the the STG, and the upper bank receives input exclusively from planum temporale (BA 42/22) in the belt areas of the auditory the STG (Seltzer and Pandya, 1978). Note that these STS association cortex. In the right STG, activation was primarily regions are anterior to, and functionally distinct from, the observed in anterior and posterior HG, including the PAC visual association areas of the STS that are involved in visual (BA 41). No activation was observed in the auditory associa- motion and gaze perception. This central STS region is not tion cortex A2 covering the planum polare (BA 52) anterior to generally known to be activated by pure tones or even by the primary auditory cortex in either the left or right STG. frequency modulation (FM) of tones, in contrast to the T1b Although processing of nonlinguistic, nonvocal, auditory and T2 regions of the auditory cortex (Brechmann et al., stimuli is generally thought to take place in the STG, we also 2002). Relatively little is known about the auditory functions found signiﬁcant activation in the STS and adjoining circular of the STS, but Romanski et al. (1999) have proposed the insular sulcus and insula in both hemispheres. The STS existence of a ventral temporal lobe stream that plays a role regions activated in the present study have direct projections in identifying coherent auditory objects, analogous to the to the STG (Pandya, 1995) and are considered part of the ventral visual pathway involved in object recognition. Inter- hierarchical organization of the auditory association cortex estingly, Belin et al. (2000) have shown that similar central (Kaas and Hackett, 2000). These STS zones receive input STS auditory areas are activated when subjects listen pas- 1752 MENON ET AL.

FIG. 6. To characterize the observed hemispheric asymmetry in temporal lobe activation, we used analysis of variance (ANOVA) on the dependent variable “percentage of voxels activated,” with factors Hemisphere (Left/Right) and Anterior/Posterior divisions. ANOVA revealed a significant Hemisphere ϫ Anterior/Posterior interaction (F(1,8) ϭ 20.11; P Ͻ 0.002), with the left hemisphere activations significantly posterior to the right hemisphere activations. The coronal slice at y ϭϪ22 mm (Talairach coordinates), midway between the anterior- and posteriormost activation in the temporal lobes, was used to demarcate the anterior and posterior subdivisions. Note that this analysis was based on activation maps obtained in individual subjects. sively to vocal sounds, whether speech or nonspeech. The temporal lobe to timbre processing is of considerable interest present study suggests that these STS regions can be acti- is the fact that the same acoustical cues involved in the vated even when stimuli do not have any vocal characteris- perception of musical timbre may also be involved in process- tics. A common feature that the vocal sounds used in the ing linguistic cues. For example, spectral shape features may Belin et al. study and the Timbre B stimuli used in the provide a more complete set of acoustic correlates for vowel present study have is that both involve rapid temporal identity than do formants (Zahorian and Jagharghi, 1993), changes in spectral energy distribution (spectral flux). We analogous to the manner in which timbre is most closely suggest that timbre, which plays an important role in both associated with the distribution of acoustic energy across music and language, may invoke common neural processing frequency (i.e., the shape of the power spectrum). Evidence mechanisms in the STS. Unlike the STG, the precise func- for this comes from Quesnel’s study in which subjects were tional divisions of the left and right STS are poorly under- easily taught to identify subtle changes in musical timbre stood. One clue that may, in the future, aid in better under- based on similarities between these timbres and certain En- standing the functional architecture of STS is that we glish vowels (Quesnel, 2001). Although it has been commonly observed a functional hemispheric asymmetry in the STS assumed that the right and left hemispheres play dominant similar to that in the STG, in that left STS activations were roles in musical and language processing, respectively (Kolb also posterior to those observed in the right STS. The poste- and Willshaw, 2000), our findings suggest that music and rior insular regions activated in this study are known to be language processing may in fact share common neural sub- directly connected to the STG (Galaburda and Pandya, 1983), strates. In this regard, our data are consistent with human suggesting a role in auditory function, but the role of this electrophysiological recordings which have also found equiv- region in auditory processing is less well understood than alent bilateral STG activation during music and language that of the STS. processing (Creutzfeldt and Ojemann, 1989). It has also been The differential contributions of the left and right STG/ suggested that the left STG may be critically involved in STS to timbre processing are not clear. Lesion studies have making distinctions between voiced and unvoiced consonants provided very little information on this issue, partly because (Liegeois-Chauvel et al., 1999). Conversely, the right STG is of the large extent of the excisions (Liegeois-Chauvel et al., involved in processing vocal sounds, whether speech or non- 1998). It is possible that the right hemisphere bias for timbre speech, compared to nonvocal environmental sounds (Belin et processing observed in lesion studies may arise partly be- al., 2000). cause more posterior left STG regions that contribute to The present study marks an important step in charting out timbre processing are generally spared in temporal lobecto- the neural bases of timbre perception, a critical structuring mies. One important reason that the contribution of the left force in music (McAdams, 1999), as well as in the identifica- NEURAL CORRELATES OF TIMBRE 1753 tion of sound sources in general (McAdams, 1993). This study Duvernoy, H. M., Bourgouin, P., Cabanis, E. 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