Focused attention in a simple dichotic listening task: an fMRI experiment

Abstract

Whole-head functional magnetic resonance imaging (fMRI) was used in nine neurologically intact subjects to measure the hemodynamic responses in the context of dichotic listening (DL). In order to eliminate the influence of verbal information processing, tones of different frequencies were used as stimuli. Three different dichotic listening tasks were used: the subjects were instructed to either concentrate on the stimuli presented in both ears (DIV), or only in the left (FL) or right (FR) ear and to monitor the auditory input for a specific target tone. When the target tone was detected, the subjects were required to indicate this by pressing a response button. Compared to the resting state, all dichotic listening tasks evoked strong hemodynamic responses within a distributed network comprising of temporal, parietal, and frontal brain areas. Thus, it is clear that dichotic listening makes use of various cognitive functions located within the dorsal and ventral stream of auditory information processing (i.e., the ‘what’ and ‘where’ streams). Comparing the three different dichotic listening conditions with each other only revealed a significant difference in the pre-SMA and within the left planum temporale area. The pre-SMA was generally more strongly activated during the DIV condition than during the FR and FL conditions. Within the planum temporale, the strongest activation was found during the FR condition and the weakest during the DIV condition. These findings were taken as evidence that even a simple dichotic listening task such as the one used here, makes use of a distributed neural network comprising of the dorsal and ventral stream of auditory information processing. In addition, these results support the previously made assumption that planum temporale activation is modulated by attentional strategies. Finally, the present findings uncovered that the pre-SMA, which is mostly thought to be involved in higher-order motor control processes, is also involved in cognitive processes operative during dichotic listening.

Introduction

Dichotic listening is a standard task in experimental and clinical neuropsychology which is mainly used to study auditory lateralization. For example using verbal material in right-handed subjects, stimuli presented to the right ear are more efficiently processed than those presented to the left ear (right ear advantage, REA). On the other hand if non-verbal stimuli are used, such as musical pieces, no ear advantage or a left ear advantage (LEA) is mostly the case. Several models have been proposed to describe these ear advantage effects on the basis of behavioural and lesion data (for a summary, see Refs. [13], [32]). A variant of the dichotic listening procedure has also been used, allowing the separation of attention and executive functions. In this paradigm, subjects are instructed to attend to one ear and to ignore information delivered to the other ear (focused attention condition). Using this instruction and keeping the physical stimulus parameters constant, one can study stimulus driven and instruction driven information processing [31], [29].

Although the dichotic listening test has intensively been used in the last four decades, the neural structures involved in the processing of dichotic stimuli are not yet fully understood. Some recent brain imaging studies have uncovered important information about the mechanisms and structures involved in the processing of dichotic stimuli [41], [47], [30], [45], [26], [4], [34]. Nevertheless, although these studies have furthered our understanding of the processes involved in dichotic listening, most studies have used complex stimuli like environmental sounds, words and syllables, or musical instruments making it impossible to separate the effects of attention that are independent from top-down processes, which may be controlled by specialised neural structures. For example, using verbal stimuli inevitably will require the participation of language relevant structures in the vicinity of perisylvian brain regions [74], [40], [72], [68], [8]. Musical stimuli on the other hand will evoke activity in the areas specialised for music processing [46].

Therefore, we designed the present study in which simple tones in a dichotic listening task were used keeping stimuli related to higher-order processing demands to a minimum. Using these stimuli we are now in a position to study the influence of directing attention to one ear independent of further demanding top-down processes. A further improvement in relation to previously published papers is that we have used functional magnetic resonance imaging (fMRI) to enable the examination of cortical activation (hemodynamic responses) with superior spatial resolution and strong statistical power. We will use three attention conditions. In the first condition, subjects are required to direct their attention to both ears simultaneously (divided attention, DIV). In two further conditions, they were instructed to focus attention to one ear and ignore information delivered to the other ear (focused attention right ear, FR; and focused attention left ear, FL). If attention is the main factor determining the outcome of dichotic listening, we predict that the auditory cortex contralateral to the attended ear will show enhanced activation, while the auditory cortex ipsilateral to the attended ear will show diminished activation [41], [4], [42].

With regard to stimuli presented to the unattended ear, we attempted to ascertain whether they would be simply neglected or less efficiently processed, or whether responses to these stimuli would be inhibited. Interestingly, older models of attention have tried to answer similar questions. For example Broadbent [12] argued that information in the neglected channel (ear) is basically filtered out (either completely or at least partly) and excluded from further processing (bottleneck theory, model 1). A second model supposes at least partial and implicit processing, allowing for the detection of information important to the subject (model 2). A third model assumes complete processing of the stimuli presented to the unattended ear, but inhibition of processes following auditory information processing, for example inhibition of responses to potentially important stimuli [5], [28], [66], [65] (model 3). On the basis of these models we have made the following predictions: (i) should model 1 prove to be correct, we predict that stimuli presented to the unattended ear will evoke only weak responses in the auditory cortex contralateral to the unattended ear. Because these stimuli are filtered out from further processing there will also be diminished or negligible activation in frontal brain areas housing working memory and further executive functions. (ii) Should model 2 be the case here, there will be mildly attenuated activation in the auditory cortex contralateral to the unattended ear because the auditory processor is analysing the incoming stimuli for possible relevance. If some of the stimuli are indeed relevant (as in our experiment), these will be transferred to the executive centres in the frontal cortex for response preparation. Thus, there will be weak activation in the frontal areas. (iii) If model 3 is correct, we predict no modulation of activity in the auditory cortices during the focused attention conditions. However, we predict strong modulations of activation in the frontal areas. These predictions are also consistent with other recent dichotic listening studies where attention has been manipulated [5], [28]. However, these authors also argued that attention may affect late-stage item localization and response selection, rather than the initial perception of the stimulus.