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REPORT
1Département de Psychologie, Université de Montréal, Montreal; 2Institut Universitaire de Gériatrie de Montréal, Montreal; and 3Douglas Hospital Research Centre, McGill University, Montreal, Canada
Submitted 30 March 2005; accepted in final form 28 May 2005
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Romanski et al. 2005). These neurons associated with auditory activity were located in area 47/12 that is, according to the anatomical boundaries identified by Petrides and Pandya (2002), outside of the human homologue of Broca's area.
In the human brain, various parts of the left prefrontal cortex have been shown to be activated during several tasks such as auditory working memory, semantic, and phonological processing. One important prefrontal region involved in speech processing is Broca's area (Bookheimer 2002; Friederici 2002; Gelfand and Bookheimer 2003), traditionally defined as pars opercularis and pars triangularis of the left inferior prefrontal gyrus [Brodmann areas (BAs) 44 and 45]. However, it is still unclear whether Broca's area constitutes an auditory field homologous to the one identified in the macaque brain (Romanski and Goldman-Rakic 2002; Romanski et al. 2005). We measured auditory-related activity in prefrontal cortex of normal human volunteers during listening to several categories of natural sounds. Our objective was to study prefrontal region's involvement in voice processing.
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METHODS |
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In the first fMRI experiment, participants were scanned while passively listening to several categories of natural sounds that included human vocalizations and nonhuman sounds from the environment (see Fig. 1A for the average frequency distribution and the spectrogram of a representative sample for each category). Instructions were to carefully listen to the stimuli. Human vocalizations consisted of 48 speech stimuli (e.g., phonemes, sentences of 1st and foreign languages) and nonlinguistic vocalizations (e.g., coughs, clearing throat). Nonhuman sounds category was composed of 48 nonhuman animal vocalizations (24 cat vocalizations and 24 mixed-animal vocalizations: alligator, antelope, bird, camel, chimpanzee, chinchilla, cow, dog, donkey, eagle, elephant, frog, hippopotamus, horse, kangaroo, koala, moose, pig, raccoon, rooster, sea lion, sheep, turtle, and whale) and 48 nonvocal sounds (e.g., musical instruments, environmental sounds such as toilet flushing, car horn). Null-events were included as a baseline (n = 48). Mean duration of human vocal stimuli was 1.2 ± 0.2 (SD) s and nonhuman stimuli was 1.45 ± 0.3 s.
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). Stimuli were 96 emotional nonlinguistic vocalizations (24 stimuli for each category: laugh, sexual vocalization, cry, and fearful scream) and emotionally neutral vocalizations (e.g., cough, clearing throat). Figure 1B shows the average frequency distribution and the spectrogram of a representative sample for each stimulus category. Null-events were also included as a baseline (n = 48). Mean durations were as follows: laughs, 1.6 ± 0.4 s; sexual vocalizations, 1.6 ± 0.4 s; cries, 1.7 ± 0.4 s; fearful screams, 1.7 ± 0.4 s; neutral vocalizations, 1.5 ± 0.4 s. Each human vocalization was produced by a different adult speaker (24 male and 24 female speakers). An independent group of individuals (n = 60) had previously judged all stimuli in terms of emotional valence (whether the speaker was expressing a positive, negative, or a neutral emotion) using visual analog scales (1–100) (Fecteau et al. 2005). The order of stimulus presentation was counterbalanced across participants. Participants in the fMRI experiment also rated the vocalizations on valence after their scanning session. As found with the independent group of participants who previously rated the stimuli, significant differences in valence ratings between stimuli of positive valence, negative valence, and neutral stimuli were observed (pairwise comparisons between laughs and neutral vocalizations, sexual and neutral vocalizations, cries and neutral vocalizations, fearful screams and neutral vocalizations; P < 0.0001). In both fMRI experiments, stimuli were presented in a pseudo-randomized order with an average stimulus onset asynchrony of 4.3 s. They were presented binaurally through pneumatic headphones, acting as a low-pass filter with a cut-off frequency around 2 kHz, sealed by foam ear inserts, and further shielded by plastic ear defenders that provided an attenuation of fMRI scanning noise of about 30 dB. Stimuli were delivered using MCF (DigiVox, Montreal, Canada), with a sound-pressure level of 85–90 dB.
We used a 1.5-T MRI system (Magnetom Vision, Siemens Electric, Erlangen, Germany). Functional scans were acquired with a single-shot echoplanar gradient-echo pulse sequence (TR = 2.6, TE = 40 ms, flip angle = 90°, field of view = 215 mm, matrix = 128 x 128). The 28 axial slices (resolution 3.75 x 3.75 mm in plane, 5 mm between planes) in each volume were aligned with the AC-PC line, covering the whole brain. A total of 320 volumes were acquired in each session. In addition, T1-weighted anatomical images were obtained for each participant, (1 mm x 1 mm x 1 mm resolution). Scanner noise was continuous throughout the experiment providing a constant auditory background. Image processing and statistical analysis were performed using SPM99 (Wellcome Department of Cognitive Neurology). Data analysis was performed in a two-stage mixed-effects analysis (equivalent to a random effects analysis) in which BOLD responses for each participant were first modeled using a synthetic hemodynamic function in the context of the fixed-effects general linear model. Subject-specific linear contrasts on the parameter estimates were entered into a second-level analysis to perform between-subjects analyses, resulting in a t-statistic for each voxel. These t-statistics (transformed to Z-statistics) constitute a statistical parametric map (SPM). SPMs were thresholded at P = 0.001. All statistical comparisons involved comparisons between all experimental conditions and null-events and between some of the experimental conditions: experiment 1, human voice (speech and nonlinguistic vocalizations) versus nonhuman sounds (cat vocalizations, mixed-animal vocalizations, nonvocal sounds); experiment 2, emotional nonlinguistic vocalizations (laughs, sexual vocalizations, cries, fearful screams) versus neutral nonlinguistic vocalizations.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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DISCUSSION |
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). Using prosody, a similar finding has recently been reported in the temporal lobe, showing greater activation for emotional compared with neutral prosody within a voice-selective area along the STS (Grandjean et al. 2005). A converging result has also been obtained by Wildgruber et al. (2005), showing enhanced activity in bilateral BA 47 associated with emotional prosody compared with rest.
Importantly, the voice-sensitive prefrontal region found in this study is distinct from Broca's area. When the speech stimuli were contrasted with the nonlinguistic vocalizations, greater responses in Broca's area (BA 44; –50, 18, 26; 184 mm3; t = 5.03; z-score = 3.74; P < 0.0001 uncorrected) were observed. Activations within Broca's area are associated with naming, phonological, syntactic, semantic processes (Bookheimer 2002; Friederici 2002), verbal working memory (Prabhakaran et al. 2000), and action understanding and imitation (Nishitani et al. 2005). In contrast, BA 47 has been linked to semantic processes (Dapretto and Bookheimer 1999; Petersen et al. 1990) and voiced speech production (Schulz et al. 2005). A recent report by Rama and Courtney (2005) showed enhanced activity in BA 45/47 associated with voice delays processing, whereas face delays processing elicited greater activity in BA 44/45, suggesting an across-modality dissociation (voice vs. face) in working memory within the ventral prefrontal cortex. Recent studies also suggested a role of BA 47 in visual spatial selectivity in the human brain (Rizzuto et al. 2005), as well as the involvement of the ventral prefrontal cortex in auditory spatial selectivity and monkey-call selectivity in the macaque brain (Cohen et al. 2004). Thus more work is needed to fully characterize the functional role of BA 47 (Fiez 1997; Price 1998).
An important issue is the possible effect of participants' experience with the sounds categories: studies in the visual domain have shown the importance of expertise with object categories in the activation of the face-selective fusiform cortex (see Tarr and Gauthier 2000 for review). Therefore we cannot rule out the possibility that left BA 47 responses to human voice that we observed may have been modulated by stimulus familiarity or expertise. Also, it will be important to better characterize the role of acoustic structure on the voice-related activation. Indeed, Romanski et al. (2005) observed similar neuronal responses to functionally different, but acoustically similar vocalizations. The low-pass filtering by the pneumatic auditory stimulation system, attenuating frequencies above 2 kHz and thus particularly influencing higher-pitched animal vocalizations, could have influenced the present pattern of results.
Our findings suggest that the region in left BA 47 outlined in this study is involved in the processing of human voices. It may therefore be part of a human counterpart of the auditory domain in the prefrontal monkey brain extending over areas 12 and 45 described by Romanski and colleagues (Romanski and Goldman-Rakic 2002; Romanski et al. 2005). Indeed, area 12 in the monkey brain is similar in topography and cytoarchitecture to part of the human BA 47 (Petrides and Pandya 2002) and projections from auditory superior temporal region in the human and the monkey brain target BA 47/12 and BA 45 (Petrides and Pandya 1988). In summary, this study showed that a region in the left BA 47 is involved in human voice processing, suggesting the existence of an auditory domain in the left human prefrontal cortex distinct from Broca's area.
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GRANTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: S. Fecteau, Dept. de Psychologie, Univ. de Montréal, C.P. 6128, Succ. Centre-ville, Montreal, Quebec H3C 3J7, Canada (E-mail: shirley.fecteau{at}umontreal.ca)
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REFERENCES |
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