The impact of task difficulty on the lateralization of processing in the human auditory cortex.

Perception of complex auditory stimuli like speech requires the simultaneous processing of different fundamental acoustic parameters. The contribution of left and right auditory cortex (AC) in the processing of these parameters differs. In addition, activity within the AC can vary positively or negatively with task performance depending on the type of task. This might affect the allocation of processing to the left and right AC. Here we studied with functional magnetic resonance imaging the impact of task difficulty on the degree of involvement of the left and right AC in two tasks that have previously been shown to differ in hemispheric involvement: categorization and sequential comparison of the direction of frequency modulations (FM). Task difficulty was manipulated by changing the speed of modulation and by that the frequency range covered by the FM. To study the impact of task-difficulty despite covarying the stimulus parameters, we utilized the contralateral noise procedure that allows comparing AC activation unconfounded by bottom-up driven activity. The easiest conditions confirmed the known right AC involvement during the categorization task and the left AC involvement during the comparison task. The involvement of the right AC increased with increasing task difficulty for both tasks presumably due to the common task component of categorizing FM direction. The involvement of left AC varied with task difficulty depending on the task. Thus, task difficulty has a strong impact on lateralized processing in AC. This connection must be taken into account when interpreting future results on lateralized processing in the AC.

Effect of sequential comparison on active processing of sound duration.

Previous studies on active duration processing on sounds showed opposing results regarding the predominant involvement of the left or right hemisphere. Duration of an acoustic event is normally judged relative to other sounds. This requires sequential comparison as auditory events unfold over time. We hypothesized that increasing the demand on sequential comparison in a task increases the involvement of the left auditory cortex. With the current fMRI study, we investigated the effect of sequential comparison in active duration discrimination by comparing a categorical with a comparative task. During the categorical task, the participant had to categorize the tones according to their duration (short vs long). During the comparative task, they had to decide for each tone whether its length matched the tone presented before. We used the contralateral noise procedure to reveal the degree of participation of the left and right auditory cortex during these tasks. We found that both tasks more strongly involve the left than the right auditory cortex. Furthermore, the left auditory cortex was more strongly involved during comparison than during categorization. Together with previous studies, this suggests that additional demand for sequential comparison during processing of different basic acoustic parameters leads to an increased recruitment of the left auditory cortex. In addition, the comparison task more strongly involved several brain areas outside the auditory cortex, which may also be related to the demand for additional cognitive resources as compared to the more efficient categorization of sounds. Hum Brain Mapp 38:4459-4469, 2017. © 2017 Wiley Periodicals, Inc.

Auditory intensity processing: Categorization versus comparison.

Intensity is an important parameter for the perception of complex auditory stimuli like speech. The results of previous studies on the processing of intensity are diverse since left-lateralized, right-lateralized and non-lateralized processing was suggested. A clear dependence of the lateralization on the kind of stimuli and/or task is not apparent. With the present functional magnetic resonance imaging (fMRI) study, we directly investigated the differences between a categorical and comparative task. To determine hemispheric involvement we used a method with contralateral noise presentation. Harmonic complexes were presented monaurally without and with contralateral noise. Both categorization and comparison of harmonic complexes according to their intensity more strongly involved the left than the right auditory cortex shown by a stronger effect of the additional noise on the activity in the left auditory cortex. Together with previous results, this suggests that left-lateralized processing of intensity in the auditory cortex can be observed independent of task and stimuli. The comparison task more strongly engaged the left auditory cortex than the categorization task probably due the additional need for sequential comparison and the right auditory cortex probably due to capacity reasons. Comparison also more strongly engaged areas associated with attentional processes and areas responsible for motor response selection. We suggest this to be caused by a more difficult response selection and by the need for continuous update of information in reference memory during the comparison task.

Division of labor between left and right human auditory cortices during the processing of intensity and duration.

Intensity and duration are important parameters for the processing of speech and music. Neuroimaging results on the processing of these parameters in tasks involving the discrimination of stimuli based on these parameters are controversial. Depending on the experimental approach, varying hypotheses on the involvement of the left and right auditory cortices (ACs) have been put forward. The aim of the present functional magnetic resonance imaging (fMRI) study was to find differences and commonalities in location and strength of brain activity during the processing of intensity and duration when the same stimuli have to be actively categorized according to these two parameters. For this we used a recently introduced method to determine lateralized processing in the AC with contralateral noise. Harmonic frequency modulated (FM) tone complexes were presented monaurally without and with contralateral noise. During categorization of the tones according to their intensity, contralateral noise increased activity mainly in the left AC, suggesting a special role for the left AC in this task. During categorization of tones according to their duration, contralateral noise increased activity in both the left and the right AC. This suggests that active categorization of FM tones according to their duration does not involve only the left AC as has been suggested, but also the right AC to a substantial degree. The area around Heschl's sulcus seems to be the most strongly involved during both intensity and duration categorization, albeit with different lateralization. Altogether the results of the present study support the view that the lateralized processing of the same stimuli in the human AC is strongly modulated by the given task (top-down effect).

Asymmetries and hemispheric interaction in the auditory system of elderly people.

Age-related changes of asymmetries in the auditory system and decreasing efficiency of hemispheric interaction have been discussed for some time. This mini-review discusses recent neuroimaging studies on alterations in lateralization of cortical processing and structural changes concerning the division of labor and interaction between hemispheres during auditory processing in elderly people with the focus on people without severe hearing loss. Several changes of asymmetries in anatomy, function and neurotransmitter concentration were observed in auditory cortical areas of older compared to younger adults. It was shown that connections between left and right auditory cortex are reduced during aging. Functionally, aging seems to lead to a reduction in asymmetry of auditory processing. However, the results do not always point into the same direction. Furthermore, correlations between function, anatomy and behavior in the left and right hemisphere appear to differ between younger and older adults. The changes in auditory cortex asymmetries with aging might be due to compensation of declining processing capacities, but at the same time these mechanisms could impair the balanced division of labor between the two hemispheres that is required for the processing of complex auditory stimuli such as speech. Neuroimaging studies are essential to follow the slow changes with aging as in the beginning no behavioral effects might be visible due to compensation. Future studies should control well for peripheral hearing loss and cognitive decline. Furthermore, for the interpretability of results it is necessary to use specific tasks with well-controlled task difficulty.

Effect of age on lateralized auditory processing.

The lateralization of processing in the auditory cortex for different acoustic parameters differs depending on stimuli and tasks. Thus, processing complex auditory stimuli requires an efficient hemispheric interaction. Anatomical connectivity decreases with aging and consequently affects the functional interaction between the left and right auditory cortex and lateralization of auditory processing. Here we studied with magnetic resonance imaging the effect of aging on the lateralization of processing and hemispheric interaction during two tasks utilizing the contralateral noise procedure. Categorization of tones according to their direction of frequency modulations (FM) is known to be processed mainly in the right auditory cortex. Sequential comparison of the same tones according to their FM direction strongly involves additionally the left auditory cortex and therefore a stronger hemispheric interaction than the categorization task. The results showed that older adults more strongly recruit the auditory cortex especially during the comparison task that requires stronger hemispheric interaction. This was the case although the task difficulty was adapted to achieve similar performance as the younger adults. Additionally, functional connectivity from auditory cortex to other brain areas was stronger in older than younger adults especially during the comparison task. Diffusion tensor imaging data showed a reduction in fractional anisotropy and an increase in mean diffusivity in the corpus callosum of older adults compared to younger adults. These changes indicate a reduction of anatomical interhemispheric connections in older adults that makes larger processing capacity necessary when tasks require functional hemispheric interaction.

Interaction between bottom-up and top-down effects during the processing of pitch intervals in sequences of spoken and sung syllables.

The processing of pitch intervals may be differentially influenced when musical or speech stimuli carry the pitch information. Most insights into the neural basis of pitch interval processing come from studies on music perception. However, music, in contrast to speech, contains a stable set of pitch intervals. To converge the investigation of pitch interval processing in music and speech, we used sequences of the same spoken or sung syllables. The pitch of these syllables varied either by semitone steps like in music or by smaller intervals. Participants had to differentiate the sequences according to their different sizes of pitch intervals or to the direction of the last frequency step in the sequence. The results depended strongly on the specific task demands. Whereas the interval-size task itself recruited more regions in right lateralized fronto-parietal brain network, stronger activity on semitone than on non-semitone sequences was found in the left hemisphere (mainly in frontal cortex) during this task. These effects were also influenced by the speech mode (spoken or sung syllables). Our findings suggest that the processing of pitch intervals in sequences of syllables depends on an interaction between bottom-up (speech mode, pitch interval) and top-down effects (task).

Effect of cochlear implant side on early speech processing in adults with single-sided deafness.

OBJECTIVE: In binaurally deaf subjects, speech processing particularly benefits from a cochlear implant (CI) in the right ear, which is contralateral to the commonly left speech-dominant hemisphere. However, it is unclear whether such effects of implantation side also occur in speech processing in patients with single-sided deafness (SSD). METHODS: Lateralization of N1 responses was analyzed with a high-density electroencephalogram (EEG) in fourteen adults with postlingually acquired left or right SSD who received a CI in adulthood. During recording, patients performed a speech and a pure-tone discrimination task. Lateralization of N1 responses was assessed by side-specific global field power (GFP) and compared (a) between normal hearing and CI-implanted ears within subjects and (b) between implantation sides across subjects. RESULTS: N1 responses were stronger in the contralateral than in the ipsilateral hemisphere during stimulation of the normal hearing ear (except for left speech stimulation), and was bilateral symmetric with CI stimulation on either side. A significant correlation between speech discrimination performance and left lateralization was found across subjects for the left CI ear. CONCLUSIONS: CI stimulation altered auditory processing across hemispheres. Speech discrimination in left CI-implanted SSD patients improved with left lateralization of the N1 response. SIGNIFICANCE: Side-specific rehabilitation in SSD patients might improve speech processing across hemispheres.

Effect of Contralateral Noise on Speech Intelligibility.

In patients with strong asymmetric hearing loss, standard clinical practice involves testing speech intelligibility in the ear with the higher hearing threshold by simultaneously presenting noise to the other ear. However, psychoacoustic and functional magnetic resonance imaging (fMRI) studies indicate that this approach may be problematic as contralateral noise has a disruptive effect on task processing. Furthermore, fMRI studies have revealed that the effect of contralateral noise on brain activity depends on the lateralization of task processing. The effect of contralateral noise is stronger when task-relevant stimuli are presented ipsilaterally to the hemisphere that is processing the task. In the present study, we tested the effect of four different levels of contralateral noise on speech intelligibility using the Oldenburg sentence test (OLSA). Cortical lateralization of speech processing was assessed upfront by using a visual speech test with fMRI. Contralateral OLSA noise of 65 or 80 dB SPL significantly reduced word intelligibility irrespective of which ear the speech was presented to. In participants with left-lateralized speech processing, 50 dB SPL contralateral OLSA noise led to a significant reduction in speech intelligibility when speech was presented to the left ear, i.e. when speech was presented ipsilaterally to the hemisphere that is mainly processing speech. Thus, contralateral noise, as used in standard clinical practice, not only prevents listeners from using the information in the better-hearing ear but may also have the unintended effect of hampering central processing of speech.

Dorsal posterior cingulate cortex encodes the informational value of feedback in human-computer interaction.

In communication between humans as well as in human-computer interaction, feedback is ubiquitous. It is essential for keeping up the dialogue between interaction partners, evaluating the adequacy of an action, or improving task performance. While the neuroscientific view on feedback has largely focused on its function as reward, more general definitions also emphasise its function as information about aspects of one's task performance. Using fMRI in a computer-controlled auditory categorisation task, we studied the neural correlates of the informational value of computer-given feedback independent of reward. Feedback about the correctness of a decision, compared with feedback only indicating the registration of a decision, increases activation of the dorsal posterior cingulate cortex, supporting this region's role in adapting to behaviourally relevant information. Both conditions elicit equally strong activation of the dorsal striatum which does not support an interpretation of feedback information as a type of reward. Instead, we suggest that it reflects a more fundamental aspect of human interaction behaviour, namely the establishment of a state that enables us to continue with the next step of the interaction.

Delays in Human-Computer Interaction and Their Effects on Brain Activity.

The temporal contingency of feedback is an essential requirement of successful human-computer interactions. The timing of feedback not only affects the behavior of a user but is also accompanied by changes in psychophysiology and neural activity. In three fMRI experiments we systematically studied the impact of delayed feedback on brain activity while subjects performed an auditory categorization task. In the first fMRI experiment, we analyzed the effects of rare and thus unexpected delays of different delay duration on brain activity. In the second experiment, we investigated if users can adapt to frequent delays. Therefore, delays were presented as often as immediate feedback. In a third experiment, the influence of interaction outage was analyzed by measuring the effect of infrequent omissions of feedback on brain activity. The results show that unexpected delays in feedback presentation compared to immediate feedback stronger activate inter alia bilateral the anterior insular cortex, the posterior medial frontal cortex, the left inferior parietal lobule and the right inferior frontal junction. The strength of this activation increases with the duration of the delay. Thus, delays interrupt the course of an interaction and trigger an orienting response that in turn activates brain regions of action control. If delays occur frequently, users can adapt, delays become expectable, and the brain activity in the observed network diminishes over the course of the interaction. However, introducing rare omissions of expected feedback reduces the system's trustworthiness which leads to an increase in brain activity not only in response to such omissions but also following frequently occurring and thus expected delays.

Auditory intensity processing: Effect of MRI background noise.

Studies on active auditory intensity discrimination in humans showed equivocal results regarding the lateralization of processing. Whereas experiments with a moderate background found evidence for right lateralized processing of intensity, functional magnetic resonance imaging (fMRI) studies with background scanner noise suggest more left lateralized processing. With the present fMRI study, we compared the task dependent lateralization of intensity processing between a conventional continuous echo planar imaging (EPI) sequence with a loud background scanner noise and a fast low-angle shot (FLASH) sequence with a soft background scanner noise. To determine the lateralization of the processing, we employed the contralateral noise procedure. Linearly frequency modulated (FM) tones were presented monaurally with and without contralateral noise. During both the EPI and the FLASH measurement, the left auditory cortex was more strongly involved than the right auditory cortex while participants categorized the intensity of FM tones. This was shown by a strong effect of the additional contralateral noise on the activity in the left auditory cortex. This means a massive reduction in background scanner noise still leads to a significant left lateralized effect. This suggests that the reversed lateralization in fMRI studies with loud background noise in contrast to studies with softer background cannot be fully explained by the MRI background noise.

Delayed system response times affect immediate physiology and the dynamics of subsequent button press behavior.

System response time research is an important issue in human-computer interactions. Experience with technical devices and general rules of human-human interactions determine the user's expectation, and any delay in system response time may lead to immediate physiological, emotional, and behavioral consequences. We investigated such effects on a trial-by-trial basis during a human-computer interaction by measuring changes in skin conductance (SC), heart rate (HR), and the dynamics of button press responses. We found an increase in SC and a deceleration of HR for all three delayed system response times (0.5, 1, 2 s). Moreover, the data on button press dynamics was highly informative since subjects repeated a button press with more force in response to delayed system response times. Furthermore, the button press dynamics could distinguish between correct and incorrect decisions and may thus even be used to infer the uncertainty of a user's decision.

Left auditory cortex is involved in pairwise comparisons of the direction of frequency modulated tones.

Evaluating series of complex sounds like those in speech and music requires sequential comparisons to extract task-relevant relations between subsequent sounds. With the present functional magnetic resonance imaging (fMRI) study, we investigated whether sequential comparison of a specific acoustic feature within pairs of tones leads to a change in lateralized processing in the auditory cortex (AC) of humans. For this we used the active categorization of the direction (up vs. down) of slow frequency modulated (FM) tones. Several studies suggest that this task is mainly processed in the right AC. These studies, however, tested only the categorization of the FM direction of each individual tone. In the present study we ask the question whether the right lateralized processing changes when, in addition, the FM direction is compared within pairs of successive tones. For this we use an experimental approach involving contralateral noise presentation in order to explore the contributions made by the left and right AC in the completion of the auditory task. This method has already been applied to confirm the right-lateralized processing of the FM direction of individual tones. In the present study, the subjects were required to perform, in addition, a sequential comparison of the FM direction in pairs of tones. The results suggest a division of labor between the two hemispheres such that the FM direction of each individual tone is mainly processed in the right AC whereas the sequential comparison of this feature between tones in a pair is probably performed in the left AC.

Human striatum is differentially activated by delayed, omitted, and immediate registering feedback.

The temporal contingency of feedback during conversations is an essential requirement of a successful dialog. In the current study, we investigated the effects of delayed and omitted registering feedback on fMRI activation and compared both unexpected conditions to immediate feedback. In the majority of trials of an auditory task, participants received an immediate visual feedback which merely indicated that a button press was registered but not whether the response was correct or not. In a minority of trials, and thus unexpectedly, the feedback was omitted, or delayed by 500 ms. The results reveal a response hierarchy of activation strength in the dorsal striatum and the substantia nigra: the response to the delayed feedback was larger compared to immediate feedback and immediate feedback showed a larger activation compared to the omission of feedback. This suggests that brain regions typically involved in reward processing are also activated by non-rewarding, registering feedback. Furthermore, the comparison with immediate feedback revealed that both omitted and delayed feedback significantly modulated activity in a network of brain regions that reflects attentional demand and adjustments in cognitive and action control, i.e., the posterior medial frontal cortex (pMFC), right dorsolateral prefrontal cortex (dlPFC), bilateral anterior insula (aI), inferior frontal gyrus (Gfi), and inferior parietal lobe (Lpi). This finding emphasizes the importance of immediate feedback in human-computer interaction, as the effects of delayed feedback on brain activity in the described network seem to be similar to that of omitted feedback.