Cerebral activation associated with speech sound discrimination during the diotic listening task: An fMRI study
Introduction
Selective listening is an auditory process that enables one to attend to a specific speech of interest among a mixture of parallel conversations. Accomplishment of this ability, commonly known as the cocktail party effect, requires not only appropriate orientation and sustainment of auditory attention but also a multitude of concomitant cognitive processes including sound discrimination, human voice recognition, language processing, and so forth. To reveal the underlying neural mechanisms, the so-called dichotic listening paradigm has long been used as an effective measure in combination with neuroimaging studies (Pugh et al., 1996, Beaman et al., 2007). In this paradigm, two different auditory stimuli are presented simultaneously, but with one of the stimuli delivered to one ear and the second to the other ear (Kimura, 1961, Bryden, 1988). The types of auditory stimuli ranged from simple tones (Jäncke et al., 2003, Petkov et al., 2004) to syllables (Lipschutz et al., 2002), to meaningful words (Grady et al., 1997, Jäncke et al., 2001), and to sentences (Hashimoto et al., 2000). Previous imaging studies based on this paradigm and using positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) have revealed brain regions implicated in selective listening. Robust activity is observed in the bilateral temporal lobes, including the superior temporal gyrus (STG) (Tzourio et al., 1997, Alho et al., 1999, Hugdahl et al., 1999, Zatorre et al., 1999, Hashimoto et al., 2000, Jäncke et al., 2001, van den Noort et al., 2008) during dichotic listening tasks. These areas are well known to be involved in auditory perception (van den Noort et al., 2008). In addition, significant activation is found in the lateral frontal (Hashimoto et al., 2000, Lipschutz et al., 2002, Thomsen et al., 2004) and parietal cortices (Hashimoto et al., 2000, Lipschutz et al., 2002, van den Noort et al., 2008). Mid-ventrolateral (BA 45/47) and mid-dorsolateral areas (BA 9/46) in the lateral frontal cortex are involved in pruning out unwanted information by responding selectively to relevant information (Lipschutz et al., 2002). The parietal cortex, especially the temporoparietal junction extending toward the inferior parietal lobe (IPL), plays a major role in attentional orientation during dichotic listening (Lipschutz et al., 2002). Therefore, the dichotic listening paradigm has a major advantage in specifying brain areas involved in the selective listening process, although speech discrimination under the constantly changing auditory conditions as encountered in daily life is far from such dichotic listening settings.
While the dichotic listening paradigm is one extreme abstraction of selective listening processes that we encounter in daily life, another experimental paradigm, the diotic listening paradigm, has also been used in previous studies, albeit less frequently, to investigate auditory attention under more natural listening settings. The task consists of binaural presentation of target stimuli superimposed by distracting stimuli (Scott et al., 2004, Shafiro and Gygi, 2007), so that the listening condition is more compatible with that in our daily life where the speech of interest and other conversations are typically mixed together and delivered to both ears. Previously, an fMRI study based on this paradigm reported that discrimination of human speech is associated with blood oxygenation level-dependent (BOLD) activation in Wernicke's area (BA22), Broca's area (BA44/45) and the frontal association cortex (BA6, 9/46, 32, 13/47), suggesting that the neural networks for executing semantic, syntactic, and prosodic processing are implicated in speech discrimination (Nakai et al., 2005). Given that constantly changing auditory environments are encountered in daily life, it is still unclear which brain regions critically work in response to change of challenge level in speech sound discrimination paradigms.
Here we present an fMRI study based on the diotic listening paradigm to evaluate brain activity involved in auditory selective attention. We found that hemodynamic activities in some temporal subregions showed significant correlations with performance accuracy of speech sound discrimination.
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Subjects
Twenty healthy volunteers, 10 males and 10 females, participated in the study (mean age ± SD, 24.9 ± 2.0 years). All subjects were right-handed according to the Edinburgh handedness inventory (mean laterality quotients ± SD, 89.7 ± 15.7) (Oldfield, 1971) and were native speakers of Japanese with normal hearing. None had a previous history of any neurological or psychiatric disorders. All subjects gave written informed consent prior to participation in the experiment. The present study was approved by
fMRI data
To assess the areas activated in selective listening attention under this designed experiment, the BOLD signal changes in both Si–N and Sc–N contrasts were examined. In Si–N contrast, as shown in Fig. 2A, the bilateral STG, middle temporal gyrus (MTG), middle frontal gyrus (MFG), superior parietal lobule (SPL), left precentral gyrus, right inferior frontal gyrus (IFG), precuneus and IPL were significantly activated (Table 1 and Fig. 2A). In Sc–N contrast, there was significant activation in the
Cortical network in auditory selective attention
By means of fMRI with a diotic experimental paradigm based rather on actual human conversation, cortical hemodynamic response was observed robustly in the bilateral STG and MTG and substantially in the bilateral MFG, right IFG and SPL in both Si and Sc conditions. Brain imaging (PET and fMRI) combined with dichotic listening task (O’Leary et al., 1996, Hugdahl et al., 1999, Hugdahl et al., 2000, Hashimoto et al., 2000, Jäncke et al., 2001, Jäncke et al., 2003, Hund-Georgiadis et al., 2002) has
Acknowledgments
We thank the staffs of Asai hospital for their assistance in collecting the demographic data. Funding for this study was provided by a Grant-in-Aid for Science Research (C) from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), Japan, to H.S. (no. 1659028), a Grant-in-Aid for Encouragement of Young Scientists (B) from the Japan Society for the Promotion of Science (JSPS) to N.Y. (no. 18790852) and to Y.I. (no. 17790821).
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Present address: Department of Neuropsychiatry, Graduate School of Medicine, University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo 113-8655, Japan.