Dorsal posterior cingulate cortex responds to negative feedback information supporting learning and relearning of response policies.

Many challenges in life come without explicit instructions. Instead, humans need to test, select, and adapt their behavioral responses based on feedback from the environment. While reward-centric accounts of feedback processing primarily stress the reinforcing aspect of positive feedback, feedback's central function from an information-processing perspective is to offer an opportunity to correct errors, thus putting a greater emphasis on the informational content of negative feedback. Independent of its potential rewarding value, the informational value of performance feedback has recently been suggested to be neurophysiologically encoded in the dorsal portion of the posterior cingulate cortex (dPCC). To further test this association, we investigated multidimensional categorization and reversal learning by comparing negative and positive feedback in an event-related functional magnetic resonance imaging experiment. Negative feedback, compared with positive feedback, increased activation in the dPCC as well as in brain regions typically involved in error processing. Only in the dPCC, subarea d23, this effect was significantly enhanced in relearning, where negative feedback signaled the need to shift away from a previously established response policy. Together with previous findings, this result contributes to a more fine-grained functional parcellation of PCC subregions and supports the dPCC's involvement in the adaptation to behaviorally relevant information from the environment.

Predictive cues for auditory stream formation in humans and monkeys.

Auditory perception is improved when stimuli are predictable, and this effect is evident in a modulation of the activity of neurons in the auditory cortex as shown previously. Human listeners can better predict the presence of duration deviants embedded in stimulus streams with fixed interonset interval (isochrony) and repeated duration pattern (regularity), and neurons in the auditory cortex of macaque monkeys have stronger sustained responses in the 60-140 ms post-stimulus time window under these conditions. Subsequently, the question has arisen whether isochrony or regularity in the sensory input contributed to the enhancement of the neuronal and behavioural responses. Therefore, we varied the two factors isochrony and regularity independently and measured the ability of human subjects to detect deviants embedded in these sequences as well as measuring the responses of neurons the primary auditory cortex of macaque monkeys during presentations of the sequences. The performance of humans in detecting deviants was significantly increased by regularity. Isochrony enhanced detection only in the presence of the regularity cue. In monkeys, regularity increased the sustained component of neuronal tone responses in auditory cortex while isochrony had no consistent effect. Although both regularity and isochrony can be considered as parameters that would make a sequence of sounds more predictable, our results from the human and monkey experiments converge in that regularity has a greater influence on behavioural performance and neuronal responses.

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.

Localizing the human primary auditory cortex in vivo using structural MRI.

Currently there are no routine methods to delineate the primary auditory cortex (PAC) of humans in vivo. Due to the large differences in the location of the PAC between subjects, labels derived from post-mortem brains may be inaccurate when applied to different samples of in vivo brains. Recent magnetic resonance (MR) imaging studies suggested that MR-tissue properties can be used to define the location of the PAC region in vivo. The basis for such an approach is that the PAC region is more strongly myelinated than the secondary areas. We developed a fully automatic method to identify the PAC in conventional anatomical data using a combination of two complementary MR contrasts, i.e., T1 and T2, at 3T with 0.7mm isotropic resolution. Our algorithm maps the anatomical MR data to reconstructed cortical surfaces and uses a classification approach to create an artificial contrast that is highly sensitive to the effects of an increased myelination of the cortex. Consistent with the location of the PAC defined in post-mortem brains, we found a compact region on the medial two thirds of Heschl's gyrus in both hemispheres of all 39 subjects. With further improvements in signal-to-noise ratio of the anatomical data and manual correction of segmentation errors, the results suggest that the primary auditory cortex can be defined in the living brain of single subjects.

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).

Feedback that confirms reward expectation triggers auditory cortex activity.

Associative learning studies have shown that the anticipation of reward and punishment shapes the representation of sensory stimuli, which is further modulated by dopamine. Less is known about whether and how reward delivery activates sensory cortices and the role of dopamine at that time point of learning. We used an appetitive instrumental learning task in which participants had to learn that a specific class of frequency-modulated tones predicted a monetary reward following fast and correct responses in a succeeding reaction time task. These fMRI data were previously analyzed regarding the effect of reward anticipation, but here we focused on neural activity to the reward outcome relative to the reward expectation and tested whether such activation in the reward reception phase is modulated by L-DOPA. We analyzed neural responses at the time point of reward outcome under three different conditions: 1) when a reward was expected and received, 2) when a reward was expected but not received, and 3) when a reward was not expected and not received. Neural activity in auditory cortex was enhanced during feedback delivery either when an expected reward was received or when the expectation of obtaining no reward was correct. This differential neural activity in auditory cortex was only seen in subjects who learned the reward association and not under dopaminergic modulation. Our data provide evidence that auditory cortices are active at the time point of reward outcome. However, responses are not dependent on the reward itself but on whether the outcome confirmed the subject's expectations.

Cross-modal pattern of brain activations associated with the processing of self- and significant other's name.

Previous neuroimaging studies have shown that the patterns of brain activity during the processing of personally relevant names (e.g., own name, friend's name, partner's name, etc.) and the names of famous people (e.g., celebrities) are different. However, it is not known how the activity in this network is influenced by the modality of the presented stimuli. In this fMRI study, we investigated the pattern of brain activations during the recognition of aurally and visually presented full names of the subject, a significant other, a famous person and unknown individuals. In both modalities, we found that the processing of self-name and the significant other's name was associated with increased activation in the medial prefrontal cortex (MPFC). Acoustic presentations of these names also activated bilateral inferior frontal gyri (IFG). This pattern of results supports the role of MPFC in the processing of personally relevant information, irrespective of their modality.

Learning-dependent plasticity in human auditory cortex during appetitive operant conditioning.

Animal experiments provide evidence that learning to associate an auditory stimulus with a reward causes representational changes in auditory cortex. However, most studies did not investigate the temporal formation of learning-dependent plasticity during the task but rather compared auditory cortex receptive fields before and after conditioning. We here present a functional magnetic resonance imaging study on learning-related plasticity in the human auditory cortex during operant appetitive conditioning. Participants had to learn to associate a specific category of frequency-modulated tones with a reward. Only participants who learned this association developed learning-dependent plasticity in left auditory cortex over the course of the experiment. No differential responses to reward predicting and nonreward predicting tones were found in auditory cortex in nonlearners. In addition, learners showed similar learning-induced differential responses to reward-predicting and nonreward-predicting tones in the ventral tegmental area and the nucleus accumbens, two core regions of the dopaminergic neurotransmitter system. This may indicate a dopaminergic influence on the formation of learning-dependent plasticity in auditory cortex, as it has been suggested by previous animal studies.

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).

Forgetting of emotional information is hard: an fMRI study of directed forgetting.

Strong evidence suggests that memory for emotional information is much better than for neutral one. Thus, one may expect that forgetting of emotional information is difficult and requires considerable effort. The aim of this item-method directed forgetting functional magnetic resonance imaging study was to investigate this hypothesis both at behavioral and neural levels. Directed forgetting effects were observed for both neutral and emotionally negative International Affective Picture System images. Moreover, recognition rate of negative to-be-forgotten images was higher than in case of neutral ones. In the study phase, intention to forget and successful forgetting of emotionally negative images were associated with widespread activations extending from the anterior to posterior regions mainly in the right hemisphere, whereas in the case of neutral images, they were associated with just one cluster of activation in the right lingual gyrus. Therefore, forgetting of emotional information seems to be a demanding process that strongly activates a distributed neural network in the right hemisphere. In the test phase, in turn, successfully forgotten images--either neutral or emotionally negative--were associated with virtually no activation, even at the lowered P value threshold. These results suggest that intentional inhibition during encoding may be an efficient strategy to cope with emotionally negative memories.

Neural Mechanisms Underlying the Effects of Novel Sounds on Task Performance in Children With and Without ADHD.

Distractibility is one of the key features of attention deficit hyperactivity disorder (ADHD) and has been associated with alterations in the neural orienting and alerting networks. Task-irrelevant stimuli are thus expected to have detrimental effects on the performance of patients with ADHD. However, task-irrelevant presentation of novel sounds seems to have the opposite effect and improve subsequent attentional performance particularly in patients with ADHD. Here, we aimed to understand the neural modulations of the attention networks underlying these improvements. Fifty boys (25 with ADHD) participated in a functional magnetic resonance imaging (fMRI) study in which unique (novel) or repeatedly presented (familiar) sounds were placed before a visual flanker task in 2/3 of the trials. We found that presenting any sound improved task performance in all participants, but the underlying neural mechanisms differed for the type of sound. Familiar sounds led to a stronger increase in activity in the left posterior insula in patients with ADHD compared to typically developing peers. Novel sounds led to activations of the fronto-temporoparietal ventral attention network, likewise in ADHD and TD. These changes in signaling by novelty in the right inferior frontal gyrus were directly related to improved response speed showing that neural orienting network activity following novel sounds facilitated subsequent attentional performance. This mechanism of behavioral enhancement by short distractions could potentially be useful for cognitive trainings or homework situations.

Why do humans have unique auditory event-related fields? Evidence from computational modeling and MEG experiments.

Auditory event-related fields (ERFs) measured with magnetoencephalography (MEG) are useful for studying the neuronal underpinnings of auditory cognition in human cortex. They have a highly subject-specific morphology, albeit certain characteristic deflections (e.g., P1m, N1m, and P2m) can be identified in most subjects. Here, we explore the reason for this subject-specificity through a combination of MEG measurements and computational modeling of auditory cortex. We test whether ERF subject-specificity can predominantly be explained in terms of each subject having an individual cortical gross anatomy, which modulates the MEG signal, or whether individual cortical dynamics is also at play. To our knowledge, this is the first time that tools to address this question are being presented. The effects of anatomical and dynamical variation on the MEG signal is simulated in a model describing the core-belt-parabelt structure of the auditory cortex, and with the dynamics based on the leaky-integrator neuron model. The experimental and simulated ERFs are characterized in terms of the N1m amplitude, latency, and width. Also, we examine the waveform grand-averaged across subjects, and the standard deviation of this grand average. The results show that the intersubject variability of the ERF arises out of both the anatomy and the dynamics of auditory cortex being specific to each subject. Moreover, our results suggest that the latency variation of the N1m is largely related to subject-specific dynamics. The findings are discussed in terms of how learning, plasticity, and sound detection are reflected in the auditory ERFs. The notion of the grand-averaged ERF is critically evaluated.

Differential category learning processes: The neural basis of comparison-based learning and induction.

Findings from numerous studies suggest that multiple neural systems are involved in category learning. Specifically, it is often argued that acquiring a representation of different category structures (e.g., rule-based vs. prototype-based representation) involves different computational challenges, which are resolved by different neural circuitries in the human brain. Here we present an alternative approach for studying neural mechanisms of category learning: We refer to the idea that any category learning task involves mapping common features shared by same-category members, distinctive features discriminating members of different categories, or both. We argue that since these processes are psychologically and computationally distinct, they differ in their usability for category learning. Our participants learned novel categories of complex visual stimuli by comparing either pairs of objects from the same novel category or pairs of objects from different categories. Object pairs were chosen so that the objective amount of information they contained was identical in the two category learning conditions, equally enabling learning the predefined objective category structure. We find that the neural circuitry involved in detecting important between-categories differences is associated mainly with the dorsal striatum (bilaterally) and the right hippocampus. On the other hand, mapping within-category similarities and differences is restricted to high-level visual brain areas. We suggest that multiple neural mechanisms are involved in category learning enabling us to face different computational challenges associated with different basic types of induction processes that differ in their usability for learning different category structures.

Machine learning identifies the dynamics and influencing factors in an auditory category learning experiment.

Human learning is one of the main topics in psychology and cognitive neuroscience. The analysis of experimental data, e.g. from category learning experiments, is a major challenge due to confounding factors related to perceptual processing, feedback value, response selection, as well as inter-individual differences in learning progress due to differing strategies or skills. We use machine learning to investigate (Q1) how participants of an auditory category-learning experiment evolve towards learning, (Q2) how participant performance saturates and (Q3) how early we can differentiate whether a participant has learned the categories or not. We found that a Gaussian Mixture Model describes well the evolution of participant performance and serves as basis for identifying influencing factors of task configuration (Q1). We found early saturation trends (Q2) and that CatBoost, an advanced classification algorithm, can separate between participants who learned the categories and those who did not, well before the end of the learning session, without much degradation of separation quality (Q3). Our results show that machine learning can model participant dynamics, identify influencing factors of task design and performance trends. This will help to improve computational models of auditory category learning and define suitable time points for interventions into learning, e.g. by tutorial systems.

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.