Asymmetric coding of reward prediction errors in human insula and dorsomedial prefrontal cortex.

The signed value and unsigned salience of reward prediction errors (RPEs) are critical to understanding reinforcement learning (RL) and cognitive control. Dorsomedial prefrontal cortex (dMPFC) and insula (INS) are key regions for integrating reward and surprise information, but conflicting evidence for both signed and unsigned activity has led to multiple proposals for the nature of RPE representations in these brain areas. Recently developed RL models allow neurons to respond differently to positive and negative RPEs. Here, we use intracranially recorded high frequency activity (HFA) to test whether this flexible asymmetric coding strategy captures RPE coding diversity in human INS and dMPFC. At the region level, we found a bias towards positive RPEs in both areas which paralleled behavioral adaptation. At the local level, we found spatially interleaved neural populations responding to unsigned RPE salience and valence-specific positive and negative RPEs. Furthermore, directional connectivity estimates revealed a leading role of INS in communicating positive and unsigned RPEs to dMPFC. These findings support asymmetric coding across distinct but intermingled neural populations as a core principle of RPE processing and inform theories of the role of dMPFC and INS in RL and cognitive control.

Musicianship and melodic predictability enhance neural gain in auditory cortex during pitch deviance detection.

When listening to music, pitch deviations are more salient and elicit stronger prediction error responses when the melodic context is predictable and when the listener is a musician. Yet, the neuronal dynamics and changes in connectivity underlying such effects remain unclear. Here, we employed dynamic causal modeling (DCM) to investigate whether the magnetic mismatch negativity response (MMNm)-and its modulation by context predictability and musical expertise-are associated with enhanced neural gain of auditory areas, as a plausible mechanism for encoding precision-weighted prediction errors. Using Bayesian model comparison, we asked whether models with intrinsic connections within primary auditory cortex (A1) and superior temporal gyrus (STG)-typically related to gain control-or extrinsic connections between A1 and STG-typically related to propagation of prediction and error signals-better explained magnetoencephalography responses. We found that, compared to regular sounds, out-of-tune pitch deviations were associated with lower intrinsic (inhibitory) connectivity in A1 and STG, and lower backward (inhibitory) connectivity from STG to A1, consistent with disinhibition and enhanced neural gain in these auditory areas. More predictable melodies were associated with disinhibition in right A1, while musicianship was associated with disinhibition in left A1 and reduced connectivity from STG to left A1. These results indicate that musicianship and melodic predictability, as well as pitch deviations themselves, enhance neural gain in auditory cortex during deviance detection. Our findings are consistent with predictive processing theories suggesting that precise and informative error signals are selected by the brain for subsequent hierarchical processing.

Perceptual learning of tone patterns changes the effective connectivity between Heschl's gyrus and planum temporale.

Learning of complex auditory sequences such as music can be thought of as optimizing an internal model of regularities through unpredicted events (or "prediction errors"). We used dynamic causal modeling (DCM) and parametric empirical Bayes on functional magnetic resonance imaging (fMRI) data to identify modulation of effective brain connectivity that takes place during perceptual learning of complex tone patterns. Our approach differs from previous studies in two aspects. First, we used a complex oddball paradigm based on tone patterns as opposed to simple deviant tones. Second, the use of fMRI allowed us to identify cortical regions with high spatial accuracy. These regions served as empirical regions-of-interest for the analysis of effective connectivity. Deviant patterns induced an increased blood oxygenation level-dependent response, compared to standards, in early auditory (Heschl's gyrus [HG]) and association auditory areas (planum temporale [PT]) bilaterally. Within this network, we found a left-lateralized increase in feedforward connectivity from HG to PT during deviant responses and an increase in excitation within left HG. In contrast to previous findings, we did not find frontal activity, nor did we find modulations of backward connections in response to oddball sounds. Our results suggest that complex auditory prediction errors are encoded by changes in feedforward and intrinsic connections, confined to superior temporal gyrus.

Musical prediction error responses similarly reduced by predictive uncertainty in musicians and non-musicians.

Auditory prediction error responses elicited by surprising sounds can be reliably recorded with musical stimuli that are more complex and realistic than those typically employed in EEG or MEG oddball paradigms. However, these responses are reduced as the predictive uncertainty of the stimuli increases. In this study, we investigate whether this effect is modulated by musical expertise. Magnetic mismatch negativity (MMNm) responses were recorded from 26 musicians and 24 non-musicians while they listened to low- and high-uncertainty melodic sequences in a musical multi-feature paradigm that included pitch, slide, intensity and timbre deviants. When compared to non-musicians, musically trained participants had significantly larger pitch and slide MMNm responses. However, both groups showed comparable reductions in pitch and slide MMNm amplitudes in the high-uncertainty condition compared with the low-uncertainty condition. In a separate, behavioural deviance detection experiment, musicians were more accurate and confident about their responses than non-musicians, but deviance detection in both groups was similarly affected by the uncertainty of the melodies. In both experiments, the interaction between uncertainty and expertise was not significant, suggesting that the effect is comparable in both groups. Consequently, our results replicate the modulatory effect of predictive uncertainty on prediction error; show that it is present across different types of listeners; and suggest that expertise-related and stimulus-driven modulations of predictive precision are dissociable and independent.

Reduced prediction error responses in high-as compared to low-uncertainty musical contexts.

Theories of predictive processing propose that prediction error responses are modulated by the certainty of the predictive model or precision. While there is some evidence for this phenomenon in the visual and, to a lesser extent, the auditory modality, little is known about whether it operates in the complex auditory contexts of daily life. Here, we examined how prediction error responses behave in a more complex and ecologically valid auditory context than those typically studied. We created musical tone sequences with different degrees of pitch uncertainty to manipulate the precision of participants' auditory expectations. Magnetoencephalography was used to measure the magnetic counterpart of the mismatch negativity (MMNm) as a neural marker of prediction error in a multi-feature paradigm. Pitch, slide, intensity and timbre deviants were included. We compared high-entropy stimuli, consisting of a set of non-repetitive melodies, with low-entropy stimuli consisting of a simple, repetitive pitch pattern. Pitch entropy was quantitatively assessed with an information-theoretic model of auditory expectation. We found a reduction in pitch and slide MMNm amplitudes in the high-entropy as compared to the low-entropy context. No significant differences were found for intensity and timbre MMNm amplitudes. Furthermore, in a separate behavioral experiment investigating the detection of pitch deviants, similar decreases were found for accuracy measures in response to more fine-grained increases in pitch entropy. Our results are consistent with a precision modulation of auditory prediction error in a musical context, and suggest that this effect is specific to features that depend on the manipulated dimension-pitch information, in this case.