Dichotic listening reveals functional specificity in prefrontal cortex: an fMRI study

www.elsevier.com/locate/ynimg NeuroImage 21 (2004) 211 – 218

Dichotic listening reveals functional specificity in prefrontal cortex: an fMRI study Tormod Thomsen, a,* Lars Morten Rimol, a Lars Ersland, a,b and Kenneth Hugdahl a,b a b

University of Bergen, Bergen, Norway Haukeland University Hospital, Bergen, Norway

Received 6 May 2003; revised 26 August 2003; accepted 26 August 2003

The present study used fMRI to investigate the relationship between stimulus presentation mode and attentional instruction in a free-report dichotic listening (DL) task with consonant – vowel (CV) syllables. Binaural and dichotic CV syllables were randomly presented to the subjects during four different instructional conditions: a passive listening instruction and three active instructions where subjects listened to both ears, right ear and left ear, respectively. The results showed that dichotic presentations activated areas in the superior temporal gyrus, middle and inferior frontal gyrus and the cingulate cortex to a larger extent than binaural presentations. Moreover, the results showed that increase of activation in these areas was differentially dependent on presentation mode and attentional instruction. Thus, it seems that speech perception, as studied with the DL procedure, involves a cortical network extending beyond primary speech perception areas in the brain, also including prefrontal cortex. D 2003 Elsevier Inc. All rights reserved. Keywords: Dichotic listening; Prefrontal cortex; fMRI

Introduction One of the most pervasive ideas in the history of the neurosciences has been the view that the two hemispheres of the brain evolved to be specialized for certain cognitive and behavioural functions, with language and speech perception as the most important lateralized functions in the human brain. The anatomical division of the two cerebral hemispheres along the longitudinal fissure is one of the most conspicuous landmarks in the brain (Davidson and Hugdahl, 1995). Thus, morphologically speaking, the left – right distinction is a fundamental property of the entire neural axis (Hellige, 1990). The evolution of language in humans, and the observation that language is organized in the left hemisphere, represents a functional correspondence to the anatomical division of the brain into the left and right hemispheres (Hugdahl,

* Corresponding author. Department of Biological and Medical Psychology, University of Bergen, Jonas Liesvei 91, N-5009 Bergen, Norway. Fax: +47-55-589874. E-mail address: [email protected] (T. Thomsen). Available online on ScienceDirect (www.sciencedirect.com.) 1053-8119/$ - see front matter D 2003 Elsevier Inc. All rights reserved. doi:10.1016/j.neuroimage.2003.08.039

2000). The most frequently used method to study language asymmetry is dichotic listening (DL) (O’Leary, 2002). DL literally means presenting two different auditory stimuli at the same time, one in each ear (Bryden, 1988; Hugdahl, 1995; Kimura, 1961). The typical finding for speech stimuli, such as consonant – vowel (CV) syllables, is more frequent reports of the right compared to left ear items, when controlling for hearing threshold differences between the ears. This is called a ‘right ear advantage’ (REA) (Hugdahl, 1995, 2002). The REA is a robust empirical effect that has been replicated in numerous laboratories (see Hugdahl, 2002 for an update). Moreover, by instructing subjects to attend exclusively to one ear [forced right (FR) or forced left (FL)], the REA can be modulated. Typically, the REA is increased in the FR instruction condition, and decreased or switched to a left ear advantage (LEA) in the FL instruction condition (Bryden et al., 1983; Hiscock and Kinsbourne, 1980; Hiscock et al., 1999; Hugdahl and Andersson, 1986). Thus, humans have the ability to overcome a default, stimulus-driven, REA by switching attention between the right and left ear channel. This can be seen as a rough, experimental, analogue to the well-known ‘‘cocktail party phenomenon’’, which also involves the use of attention in switching between multiple speech inputs (Cherry, 1953). However, although DL produces robust behavioural asymmetry effects, there is less evidence for a corresponding effect at the neuronal level. Brain imaging studies (PET and fMRI) related to DL (Hashimoto et al., 2000; Hugdahl et al., 1999, 2000; HundGeorgiadis et al., 2002; Jancke et al., 2001, 2003; O’Leary, 2002; O’Leary et al., 1996a,b; Sommer et al., 2001) have reported larger and more intense activations in the left superior and middle temporal gyri, mostly with bilateral foci. When subjects have been instructed to focus attention to either the left or right ear stimulus, additional activations in inferior parietal and prefrontal cortex have been reported, indicating the existence of an attentional cortical network (Jancke and Shah, 2002; Lipschutz et al., 2002). Thus, speech perception asymmetry, as revealed in the DL procedure, may not be uniquely localized to the temporal lobes. This study was designed to further explore how a dichotic presentation mode will result in specific brain activations compared to a binaural presentation mode, and how the attentional instruction influences brain activation. Previous studies of DL have shown that different clinical groups have difficulties with modulation of the REA in the FL condition (Loberg et al., 1999; O’Leary

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et al., 1996a). Therefore, we were particularly interested in describing possible differences in neuronal activation between the forced attention conditions (FR and FL). What makes this study somewhat different from other studies in this area is the use of an event-related fMRI design, with both dichotic and binaural presentations within each attentional condition. This allows for an unconfounded measure of activation related to presentation mode within each instruction condition. Furthermore, it allows for a better separation of areas activated in relation to presentation mode from those activated in relation to instruction. There were four different attentional conditions; passive listening (PL), non-forced (NF), forced right (FR) and forced left (FL). The use of an event-related fMRI protocol allows for randomized presentations of different stimulus types within a single scanning session, and thus overcomes the constraints on stimulus presentation encountered in the standard fMRI blockprotocol previously used in fMRI experiments of DL. Moreover, we used a visual free-report paradigm (Fig. 1) for collecting behavioural data rather than a target monitoring paradigm that has been used in all other fMRI studies of DL. The reason for this is that target monitoring differs from the free-report paradigm used in most behavioural DL studies. The use of a visual free-report paradigm therefore allows for a better comparison with data obtained outside the MR scanner. We also only included subjects with a behavioural REA when tested before the fMRI experiment (defined as more correct items reported from the right ear) since including subjects with both a REA and LEA may confound the fMRI brain activation results.

syllables would light up on the screen. First the upper left syllable would light up for 650 ms then the middle upper syllable etc., until all six syllables had been lit up. The subject pressed a response button located on the chest, when the correct syllable was lit up. The subjects were instructed to press according to a specific instruction for each condition: In the NF condition, they were instructed to press the button each time the CV syllable they had just heard was lit up on the LCD screens. The subjects were instructed to only press once for each pair of syllables, and to report the syllable they heard first or best. In the forced attention conditions (FR and FL), they were to respond each time the CV syllable they had just heard in the right or left ear, respectively, was lit up. In the PL condition, they were merely instructed to listen to the syllables. This LCD-guided free report was validated against the standard oral free report with the same results. To achieve a variable interstimulus interval (‘‘jittering’’), the time between each stimulus presentation varied between 5000 and 7000 ms. For each condition (PL, NF, FR and FL), there were 54 stimulus presentations,1 consisting of 30 dichotic and 24 binaural presentations. There were also 16 null events with no stimuli presented to allow for a better estimation of the hemodynamic response. The order of stimulus presentation was random, with different randomizations for the four different conditions. The PL and NF conditions were however always presented first. The reason for this was that the forced conditions otherwise would have produced carry-over effects to the PL and NF conditions, with the risk of biasing attention during the PL and NF conditions toward the previously attended ear. The presentation order of the FR and FL conditions was counterbalanced between subjects.

Methods MRI scanning The group consisted of 13 right-handed subjects (6 males and 7 females). All subjects were screened with audiometric testing to ensure normal hearing on both ears. Audiometry was completed for the frequencies of 250, 500, 1000, 2000 and 3000 Hz. Participants with an auditory threshold higher than 20 dB on any frequency, or an interaural difference larger than 10 dB, were excluded from the study. The subjects were also tested with DL outside the scanner, half of the subjects before scanning and half of the subjects afterwards. A criterion for being included in further analysis was a REA on both tests, both inside and outside the MR. To ensure that the subjects had understood the task, they were trained with a short test program before entering the scanner. The CV syllables used were /ba/, /da/, /ga/, /pa/, /ta/, and /ka/. All syllables had a duration of 400 – 500 ms. The stimuli were natural speech produced by an adult voice, and were digitally recorded, stored and edited before implemented in the E-prime programming software (Psychology Software Tools Inc.) that controlled the presentation of the stimuli and recording of responses. The intensity of the auditory stimuli/CV syllables was tested with a Bru¨el and Kjær Measuring Amplifier Type 2636, using filter ‘‘A’’. Stimuli presentation and a response screen were presented through MR compatible headphones and LCD screens (Magnetic Resonance Technology Inc.) that were connected to a PC outside the MR chamber, which contained the E-prime software. The headphones also served to attenuate noise effects from the MR magnet gradients, since they were equipped with special insulating materials. The six CV syllables were presented on the LCD screens in two rows with three syllables in each row (Fig. 1), throughout all four imaging runs. After each auditory stimulus presentation, the six

We used an event-related fMRI design, which allows for a comparison of dichotic and binaural stimulus presentations across, within and between the different conditions. fMRI was performed with a 1.5-T Siemens Vision Plus scanner equipped with 25 mT/m gradients. Initial scanning of anatomy was done with a T1W MPRAGE pulse sequence. Thereafter, serial imaging with 270 BOLD sensitive EPI volume measurements was done for the PL and NF conditions, and 160 EPI volume measurements for the FR and FL conditions. Each volume measurement consisted of 24 axial slices covering most of the cerebrum, with a repetition time (TR) of 2.9 s, which in turn consisted of acquisition time (TA) 2.4 s + silent interval 0.5 s. Other scanning parameters were FA: 500; TE: 60 ms; slice thickness: 5 mm; FOV: 230 mm; matrix: 64  64.

Data analysis Image processing and data analysis was performed by Statistical Parametric Mapping (SPM2) analysis software package (Wellcome Department of Cognitive Neurology, London, UK, http://

1

In the PL and NF instructions, there were also 40 monaural presentations. These are not included because it is outside the theoretical focus for this article. However, we are planning to describe the effects of monaural compared to dichotic and binaural presentations in a separate paper.

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www.fil.ion.ac.uk) run under MATLAB6.5 (Mathworks Inc., Natick, MA, USA). Single-subject analyses were performed using contrasts according to the ‘‘General Linear Model’’ as implemented in the SPM2 package. The EPI images were realigned intra-individually to the first image in each time series on a voxel-by-voxel basis to correct for head movements. The realigned images were then normalised (4 mm3) into standard stereotaxic space (template provided by the Montreal Neurological Institute), and smoothed with an 8-mm fullwidth-at-half-maximum Gaussian kernel. The time series data were high-pass filtered to remove artefacts due to cardio-respiratory and other cyclical influences. On the basis of the contrast images from the single-subject analyses, group analyses were computed as second-level analysis. Areas with statistically significant changes in signal intensity were determined using the t-statistic on a voxel basis. Three types of analyses were done: (1) a within-subjects ANOVA comparing activation in the dichotic presentation mode with activation in the binaural presentation mode and vice versa, across all four conditions; (2) a within-subjects ANOVA comparing activation in the dichotic presentation mode with activation in the binaural presentation mode, within the four different conditions; and (3) a within-subjects ANOVA comparing activation in the dichotic presentation mode with activation in the binaural presentation mode, between the FR and FL conditions. The first type of analysis would show differences between presentation modes across instruction conditions. The second type of analysis would show differences between presentation modes within instruction conditions. Furthermore, we wanted to test, whether there were areas, which were activated during the FL condition but not during the FR condition. Therefore, in the third analysis, we calculated the (dichotic binaural) for the FL task and excluded those regions, by a masking procedure, which were significant ( P < 0.05 uncorrected) in the (dichotic binaural) contrast for the FR task.

Results Response accuracy data The response accuracy data showed that two of the subjects had a LEA. These subjects were excluded from further analyses. There are two possible errors that can be made in DL. For the NF, FR and FL conditions, there is the possibility of reporting a CV syllable that has not been presented in either ear. In the forced conditions, there is also the possibility of reporting the syllable presented in the ear opposite to the one indicated in the instruction (e.g. reporting the left ear syllable during FR). To compare the binaural and dichotic presentation mode for the different instruction conditions, we initially included reports from both ears in the forced conditions in a total accuracy score. The results of a repeated-measures analysis of variance (ANOVA) based on the design Mode of presentation (dichotic, binaural)  Attention instruction (NF, FR, FL) showed a significant main effect of presentation mode ( F(1,10) = 96.78, P < 0.0001), with significantly higher response accuracy for the binaural presentations (93%) compared to the dichotic presentations (73%) (Fig. 2). A planned comparison post hoc test showed a significant decrease in response accuracy for the dichotic stimuli in the FL condition (69%) compared to the NF condition (77%).

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There were no significant differences between the FR and the NF and FL conditions. We also conducted a second ANOVA on the dichotic presentation mode alone, with response accuracy split for reports from the right and left ear (Fig. 3). This showed a trend toward a main effect of instruction ( F(2,20) = 3.23, P = 0.06). On the basis of a hypothesized interaction between instruction and ear, a Tukey HSD post hoc test was performed as a stand-alone test. This showed a significant decrease in response accuracy for the FL condition (34.7%) compared to the NF condition (38.7%). There were no significant differences between FR and the other conditions. There was a significant main effect of ear ( F(1,10) = 9.97, P < 0.05), with more correct reports from the right ear (42%) compared to the left ear (30.0%). There was also a significant interaction between instruction condition and ear ( F(2,20) = 19.0, P < 0.001). This showed significant differences both within and between conditions. There was a significant REA for both the NF (45% right ear vs. 32% left ear) and FR (48.3% right ear vs. 25.3% left ear) conditions. The comparison between conditions showed more correct reports from the right ear in the NF (45%) and FR (48.3%) conditions compared to the FL (32.7%) condition, and more correct reports from the left ear in the FL (36.7%) instruction compared to the FR (25.3%) condition. There was also a significant difference between the forced conditions, with more correct reports from the right ear in the FR condition (48.3%) compared with correct reports from the left ear in the FL condition (36.7%).

fMRI activations [Dichotic presentations, all instructions] [Binaural presentations, all instructions] Significant activations are shown in Fig. 4, with the corresponding Talairach and Tournoux (1988) coordinates and anatomical localizations in Table 1. There were six significant clusters that passed the P-threshold and cluster size ( P = 0.05 corrected, 10 voxels). These were located in the left superior temporal gyrus, in the vicinity of planum temporale (PT), bilaterally in the cingulate gyrus, bilaterally in the inferior frontal gyrus and left middle frontal gyrus. [Binaural presentations, all instructions] [Dichotic presentations, all instructions] There was one area in the left superior temporal gyrus (x = 47, y = 60, z = 29; t = 5.22, 22 voxels) that passed the Pthreshold and cluster size ( P = 0.05 corrected, 10 voxels) when comparing binaural to dichotic presentations. [Dichotic PL] [Binaural PL] There were no significant clusters that passed the P-threshold and cluster size ( P = 0.001 uncorrected, 10 voxels). [Dichotic NF] [Binaural NF] Significant activations are shown in Fig. 5, with the corresponding Talairach and Tournoux (1988) coordinates and anatom-

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Fig. 1. Example of the stimulus display.

ical localizations in Table 2. There were five significant clusters that passed the P-threshold and cluster size ( P = 0.001 uncorrected, 10 voxels). These were located in the left cingulate gyrus, bilaterally in the inferior frontal gyrus and left middle frontal gyrus. [Dichotic FR] [Binaural FR] Significant activations are shown in Fig. 6a, with the corresponding Talairach and Tournoux (1988) coordinates and anatomical localizations in Table 3. There were six significant clusters that passed the P-threshold and cluster size ( P = 0.001 uncorrected, 10 voxels). These were located in the left superior temporal gyrus, in the vicinity of PT, bilaterally in the cingulate gyrus, bilaterally in the inferior frontal gyrus and left middle frontal gyrus.

Fig. 3. Mean percentage response accuracy % AC of reported syllables to the left and right ear for dichotic presentations and for the different attentional conditions.

gyrus/anterior cingulate, bilaterally in the inferior frontal gyrus and left middle frontal gyrus. [Dichotic FR Binaural FR] [Dichotic FL Binaural FL] There were no significant clusters that passed the P-threshold and cluster size ( P = 0.001 uncorrected, 10 voxels). [Dichotic FL Binaural FL] masked exclusively by [Dichotic FR Binaural FR] Significant activations are shown in Fig. 7, with the corresponding Talairach and Tournoux (1988) coordinates and anatomical localizations in Table 5. There were four significant clusters that passed the mask P-value of 0.05 uncorrected, and P-threshold and cluster size ( P = 0.001 uncorrected, 10 voxels). These were

[Dichotic FL] [Binaural FL] Significant activations are shown in Fig. 6b, with the corresponding Talairach and Tournoux (1988) coordinates and anatomical localizations in Table 4. There were six significant clusters that passed the P-threshold and cluster size ( P = 0.001 uncorrected, 10 voxels). These were located in the left superior temporal gyrus in the vicinity of PT, bilaterally in the cingulate

Fig. 2. Mean response accuracy and standard deviation of reported syllables during the two presentation modes (dichotic and binaural) and for the different attentional conditions.

Fig. 4. Regions activated during the dichotic presentations minus the binaural presentations.

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stimuli. This is in agreement with previous findings of differences between active and PL (Hall et al., 2000; Pedersen et al., 2000). Inferior frontal gyrus An increase of activation bilaterally in the inferior frontal gyrus in the vicinity of the insula was observed when comparing dichotic with binaural presentations across the active instruction conditions. Brain imaging studies of speech perception have frequently reported insula activation (Friederici et al., 2000; Griffiths et al., 1994; Hall et al., 2000; Hashimoto et al., 2000; Heim et al., 2002; Lipschutz et al., 2002; Wise et al., 1999).

Fig. 5. Regions activated during the NF dichotic presentations minus the NF binaural presentations.

located bilaterally in the anterior cingulate, left inferior frontal gyrus and left middle frontal gyrus.

Discussion The behavioural data indicated that processing of dichotic stimuli overall was more effortful than processing of binaural stimuli. There were no differences between attentional instructions when averaging responses from binaural and dichotic presentations. However, there was an interaction between instruction and presentation mode, with a decrease in response accuracy for dichotic presentations in the FL condition compared to the NF and FR conditions. This is reflected both in number of correct reports from the left ear in the FL condition compared to correct reports from the right ear in the FR condition, and in the difference in total number of CV syllables reported in the FL compared to the NF condition. Thus, the behavioural results indicate an interaction between presentation mode and attentional instruction, with processing of dichotically presented speech stimuli being more effortful in the FL condition compared to the NF and FR conditions. These results are in accordance with results from the University of Bergen DL-database consisting of data from more than 1400 subjects, collected at independent laboratories (Hugdahl, 2002). Moreover, the behavioural data validate the experimental design in terms of investigating differences in the neuronal network underlying processing of dichotic presentations in the FL condition compared to the NF and FR conditions. PL vs. active processing For the PL condition, there were no differences in activation between the binaural and dichotic presentations. Our results therefore indicate that differences between dichotic and binaural presentation modes are dependent on active processing of the

Fig. 6. (a) Regions activated during the FR dichotic presentations minus the FR binaural presentations. (b) Regions activated during the FL dichotic presentations minus the FL binaural presentations.

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T. Thomsen et al. / NeuroImage 21 (2004) 211–218 Table 1 Dichotic

binaural presentations across instructions

Coordinates x

y 61 6

a

Cluster size

Anatomical localization

6.18 7.59 7.07 6.94 7.29 7.29 5.73

59 613a

Left superior temporal gyrus Left cingulate gyrus Right cingulate gyrus Right inferior frontal gyrus Left inferior frontal gyrus Left middle frontal gyrus Left middle frontal gyrus

z 44 19 23 25 25 17 10

6 32 30 42 46

t-Value

15 40 38 8 5 19 44

221 306 192 48

Voxels belonging to the same cluster.

Table 2 NF dichotic NF binaural Coordinates

Fig. 7. Regions activated during the FL dichotic minus FL binaural masked exclusively by FR dichotic minus FR binaural.

Anterior insula activation in DL has been related to common factors between DL and auditory motion perception, such as spatial attention or interaural stimulus differences (Hashimoto et al., 2000). When looking at uniquely activated areas in the FL condition compared to the FR condition, we found no additional activation in this area. Our findings therefore suggest that increase of activation in this area is related to stimulus discrimination, rather than increase in cognitive load, with a possible role in discriminating between the different CV syllables when presented dichotically. Middle frontal gyrus There were two activated clusters in the left middle frontal gyrus during the active instruction conditions. One cluster was located in the vicinity of the frontal eye fields (FEF). The other cluster was located more inferior and anterior, near the opercular gyrus in the vicinity of Broca’s area. The extent of this cluster increased with cognitive load. In the NF condition, the cluster was rather small (36 voxels) compared with the FR condition (91 voxels) and with the FL condition (384 voxels). In the FL condition, the cluster also extended into the opercular gyrus and also into more dorsal and lateral regions of the left middle frontal gyrus. When looking at uniquely activated areas in the FL condition compared to the FR condition, there was also activation of these areas, although the clusters were rather small (46 and 26 voxels). FEF activation has frequently been reported in studies of visual attention, and more recently also in auditory attention studies (Lipschutz et al., 2002; Tzourio et al., 1997; Zatorre et al., 1999). Our data confirm these findings. The more inferior cluster activated in all instruction conditions was located in the part of the frontal lobe most often referred to as dorsolateral prefrontal cortex (DLPFC), which is believed to have a key role in planning and executive control (Frith, 2000). Although a variety of cognitive tasks have shown activation of this region, its specific function remains unclear (Burgess et al., 2000; Duncan

x

y

6 34 36 42 46

21 19 23 17 12

t-Value

Cluster size

Anatomical localization

4.05 4.11 3.98 3.72 3.55

118 142 141 36 18

Left cingulate gyrus Left inferior frontal gyrus Right inferior frontal gyrus Left middle frontal gyrus Left middle frontal gyrus

z 39 9 13 19 44

Table 3 FR dichotic FR binaural Coordinates x

y 59 6

44 18 21 25 25 6 18

8 30 32 40 44 a

t-Value

Cluster size

Anatomical localization

4.26 4.32 5.19 4.19 4.26 4.20 4.11

116 452a

Left superior temporal gyrus Left cingulate gyrus Right cingulate gyrus Left inferior frontal gyrus Right inferior frontal gyrus Left middle frontal gyrus Left middle frontal gyrus

z 15 41 38 5 6 46 19

166 114 72 91

Voxels belonging to the same cluster.

and Owen, 2000). It has been argued that the DLPFC is involved in specifying a set of responses suitable for a given task and to bias these for selection (Nathaniel-James and Frith, 2002). The increase in cluster size with cognitive load in this region supports this hypothesis. The finding that this area is uniquely activated in the FL condition compared to the FR condition indicates an important Table 4 FL dichotic FL binaural Coordinates x

y 59 8 10

8 30 34 42 36 a

t-Value

Cluster size

Anatomical localization

4.17 5.94 4.92 5.29 5.56 4.61 4.98 3.58

47 1017a

Left superior temporal gyrus Left cingulate gyrus Left anterior cingulate Right cingulate gyrus Left inferior frontal gyrus Right inferior frontal gyrus Left middle frontal gyrus Left middle frontal gyrus

z 44 18 28 27 25 25 17 4

15 42 24 28 6 8 19 48

452 211 384 16

Voxels belonging to the same cluster.

T. Thomsen et al. / NeuroImage 21 (2004) 211–218 Table 5 (FL dichotic FL binaural) masked exclusively by (FR dichotic FR binaural) Coordinates x

y

z

t-Value Cluster Anatomical localization size

10 12 55 38

28 23 28 13

24 28 17 25

4.92 3.63 3.90 3.79

79 26 26 46

Left cingulate gyrus/Anterior cingulate Right cingulate gyrus/Anterior cingulate Left inferior/middle frontal gyrus Left inferior frontal gyrus

role in focusing of attention to a specific stimulus source, or in ignoring the stimulus presentations to the right ear in the FL condition when deciding on the correct response. Previous imaging studies have implicated Broca’s area in phonological, semantic and syntactic processing (Caplan et al., 2000; Poldrack et al., 2001; Roskies et al., 2001; Thompson-Schill et al., 1999). A subdivision of Broca’s area has been proposed (Chein et al., 2002), with two sub-regions of the left inferior frontal cortex showing distinct patterns of activity during a verbal working memory task: a dorsal inferior frontal region associated with manipulations in difficulty and performance, and a more ventral region involved in short-term maintenance of non-words as compared to words. The proposed dorsal region is spatially consistent with the activations observed in the FL condition of the present study, and when looking at uniquely activated areas in the FL condition compared to the FR condition. Cingulate gyrus The cingulate gyrus was activated in all active instruction conditions. The activated cluster in the NF condition, however, was small and seen only in the left hemisphere. The FR condition yielded bilateral activation in the cingulate gyrus, while the cingulate activation in the FL condition also extended toward the anterior regions. Only the anterior region of the cingulate gyrus was activated when looking at uniquely activated areas in the FL condition compared to the FR condition. The cingulate gyrus is known to be involved in attentional control aspects of cognitive processing, such as task management and planning (Devinsky et al., 1995; Posner and Petersen, 1990; Stuss and Benson, 1986). However, its specific contribution to cognition remains uncertain (Botwinick et al., 1999). Activation in the anterior cingulate, close to the activation in the NF and FR conditions in our study, has been reported in relation to the processing conflict involved in perceiving two similar syllables dichotically (Lipschutz et al., 2002), and in relation to response conflicts as opposed to stimulus conflicts (van Veen et al., 2001). A reasonable conclusion is therefore that activation in the superior parts of the cingulate gyrus reflects processing of a stimulus conflict when two different stimuli are presented, as in the dichotic situation, while the more inferior anterior cingulate activation is related to a response conflict caused by an instruction to report the syllables from the ‘‘wrong ear’’ in the FL condition. Superior temporal gyrus An area in left posterior superior temporal gyrus in the vicinity of PT was activated in the FR and FL conditions when comparing the binaural and dichotic presentation modes. Previous studies have observed similar attentional modulation of activity in

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this region of the auditory cortex (Jancke and Shah, 2002; Lipschutz et al., 2002; O’Leary et al., 1996b). However, there are diverging results both with respect to laterality and under which instructional conditions the activity is observed. The left PT area has been suggested to be specialized for rapidly changing acoustic cues subserving the categorical perception of acoustic stimuli (Jancke and Shah, 2002).The increase in activation during the dichotic presentation mode in the forced conditions in our study may reflect an additional need for this type of processing with increasing attentional load. In summary, the present findings show that stimuli presented dichotically cause specific brain activations compared to binaural presentations. This has previously been reported in other brain imaging studies of DL (Jancke and Shah, 2002; Lipschutz et al., 2002). However, by using dichotic and binaural stimuli within each attentional condition, our study allows for an unconfounded measure of brain areas involved in processing of dichotic presentations in the FL vs. the FR condition. An unsolved problem is however still the degree of specificity for a frontal lobe circuitry controlling the forced attention effect in DL. Furthermore, the question of how specifically these activations are linked to the use of CV syllables remains a challenge for future studies. However, a reasonable conclusion is that speech perception as studied with the DL procedure involves a cortical network extending beyond primary speech perception areas in the brain, particularly under conditions of instructions of active deployment of attention in auditory space, constituting an analogue to the ‘‘cocktail party phenomenon’’. Also, the present findings show the importance of active processing of the stimulus, demonstrated in the comparison of presentation modes in the PL condition. DL is frequently used as a clinical tool for investigating cognitive deficits in different neurological and psychiatric patient groups (Hugdahl, 2002). The correspondence of increase in brain activation with increase in processing load in the present study may shed new light on possible neuronal correlates for these disorders. Acknowledgments ˚ sa Hammar and Jarle Nyttingnes in planning The assistance of A the study is greatly acknowledged. References Botwinick, M., Nystrøm, L.E., Fissel, K., Carter, C.S., Cohen, J.D., 1999. Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402, 179 – 181. Bryden, M.P., 1988. An overview of the dichotic listening procedure and its relation to cerebral organisation. In: Hugdahl, K. (Ed.), Handbook of Dichotic Listening: Theory, Methods and Research. Wiley & Sons, Chichester, UK, pp. 1 – 44. Bryden, M.P., Munhall, K., Allard, F., 1983. Attentional biases and the right-ear effect in dichotic listening. Brain Lang. 18, 236 – 248. Burgess, P.W., Veitch, E., de Lacy Costello, A., Shallice, T., 2000. The cognitive and neuroanatomical correlates of multitasking. Neuropsychologia 38, 848 – 863. Caplan, D., Waters, A.N., Olivieri, A., 2000. Activation of Broca’s area by syntactic processing under conditions of concurrent articulation. Hum. Brain Mapp. 9, 65 – 71. Chein, J.M., Fissell, K., Jacobs, S., Fiez, J.A., 2002. Functional heterogeneity within Broca’s area during verbal working memory. Physiol. Behav. 77, 635 – 639.

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