Multiple Concurrent Predictions Inform Prediction Error in the Human Auditory Pathway.

The key assumption of the predictive coding framework is that internal representations are used to generate predictions on how the sensory input will look like in the immediate future. These predictions are tested against the actual input by the so-called prediction error units, which encode the residuals of the predictions. What happens to prediction errors, however, if predictions drawn by different stages of the sensory hierarchy contradict each other? To answer this question, we conducted two fMRI experiments while female and male human participants listened to sequences of sounds: pure tones in the first experiment and frequency-modulated sweeps in the second experiment. In both experiments, we used repetition to induce predictions based on stimulus statistics (stats-informed predictions) and abstract rules disclosed in the task instructions to induce an orthogonal set of (task-informed) predictions. We tested three alternative scenarios: neural responses in the auditory sensory pathway encode prediction error with respect to (1) the stats-informed predictions, (2) the task-informed predictions, or (3) a combination of both. Results showed that neural populations in all recorded regions (bilateral inferior colliculus, medial geniculate body, and primary and secondary auditory cortices) encode prediction error with respect to a combination of the two orthogonal sets of predictions. The findings suggest that predictive coding exploits the non-linear architecture of the auditory pathway for the transmission of predictions. Such non-linear transmission of predictions might be crucial for the predictive coding of complex auditory signals like speech.Significance Statement Sensory systems exploit our subjective expectations to make sense of an overwhelming influx of sensory signals. It is still unclear how expectations at each stage of the processing pipeline are used to predict the representations at the other stages. The current view is that this transmission is hierarchical and linear. Here we measured fMRI responses in auditory cortex, sensory thalamus, and midbrain while we induced two sets of mutually inconsistent expectations on the sensory input, each putatively encoded at a different stage. We show that responses at all stages are concurrently shaped by both sets of expectations. The results challenge the hypothesis that expectations are transmitted linearly and provide for a normative explanation of the non-linear physiology of the corticofugal sensory system.

Predictive encoding of pure tones and FM-sweeps in the human auditory cortex.

Expectations substantially influence perception, but the neural mechanisms underlying this influence are not fully understood. A prominent view is that sensory neurons encode prediction error with respect to expectations on upcoming sensory input. Although the encoding of prediction error has been previously demonstrated in the human auditory cortex (AC), previous studies often induced expectations using stimulus repetition, potentially confounding prediction error with neural habituation. These studies also measured AC as a single population, failing to consider possible predictive specializations of different AC fields. Moreover, the few studies that considered prediction error to stimuli other than pure tones yielded conflicting results. Here, we used functional magnetic resonance imaging (fMRI) to systematically investigate prediction error to subjective expectations in auditory cortical fields Te1.0, Te1.1, Te1.2, and Te3, and two types of stimuli: pure tones and frequency modulated (FM) sweeps. Our results show that prediction error is elicited with respect to the participants' expectations independently of stimulus repetition and similarly expressed across auditory fields. Moreover, despite the radically different strategies underlying the decoding of pure tones and FM-sweeps, both stimulus modalities were encoded as prediction error in most fields of AC. Altogether, our results provide unequivocal evidence that predictive coding is the general encoding mechanism in AC.

Altered processing of communication signals in the subcortical auditory sensory pathway in autism.

Autism spectrum disorder (ASD) is characterised by social communication difficulties. These difficulties have been mainly explained by cognitive, motivational, and emotional alterations in ASD. The communication difficulties could, however, also be associated with altered sensory processing of communication signals. Here, we assessed the functional integrity of auditory sensory pathway nuclei in ASD in three independent functional magnetic resonance imaging experiments. We focused on two aspects of auditory communication that are impaired in ASD: voice identity perception, and recognising speech-in-noise. We found reduced processing in adults with ASD as compared to typically developed control groups (pairwise matched on sex, age, and full-scale IQ) in the central midbrain structure of the auditory pathway (inferior colliculus [IC]). The right IC responded less in the ASD as compared to the control group for voice identity, in contrast to speech recognition. The right IC also responded less in the ASD as compared to the control group when passively listening to vocal in contrast to non-vocal sounds. Within the control group, the left and right IC responded more when recognising speech-in-noise as compared to when recognising speech without additional noise. In the ASD group, this was only the case in the left, but not the right IC. The results show that communication signal processing in ASD is associated with reduced subcortical sensory functioning in the midbrain. The results highlight the importance of considering sensory processing alterations in explaining communication difficulties, which are at the core of ASD.

Correction: Modeling and MEG evidence of early consonance processing in auditory cortex.

[This corrects the article DOI: 10.1371/journal.pcbi.1006820.].

Adjudicating Between Local and Global Architectures of Predictive Processing in the Subcortical Auditory Pathway.

Predictive processing, a leading theoretical framework for sensory processing, suggests that the brain constantly generates predictions on the sensory world and that perception emerges from the comparison between these predictions and the actual sensory input. This requires two distinct neural elements: generative units, which encode the model of the sensory world; and prediction error units, which compare these predictions against the sensory input. Although predictive processing is generally portrayed as a theory of cerebral cortex function, animal and human studies over the last decade have robustly shown the ubiquitous presence of prediction error responses in several nuclei of the auditory, somatosensory, and visual subcortical pathways. In the auditory modality, prediction error is typically elicited using so-called oddball paradigms, where sequences of repeated pure tones with the same pitch are at unpredictable intervals substituted by a tone of deviant frequency. Repeated sounds become predictable promptly and elicit decreasing prediction error; deviant tones break these predictions and elicit large prediction errors. The simplicity of the rules inducing predictability make oddball paradigms agnostic about the origin of the predictions. Here, we introduce two possible models of the organizational topology of the predictive processing auditory network: (1) the global view, that assumes that predictions on the sensory input are generated at high-order levels of the cerebral cortex and transmitted in a cascade of generative models to the subcortical sensory pathways; and (2) the local view, that assumes that independent local models, computed using local information, are used to perform predictions at each processing stage. In the global view information encoding is optimized globally but biases sensory representations along the entire brain according to the subjective views of the observer. The local view results in a diminished coding efficiency, but guarantees in return a robust encoding of the features of sensory input at each processing stage. Although most experimental results to-date are ambiguous in this respect, recent evidence favors the global model.

Neural modelling of the encoding of fast frequency modulation.

Frequency modulation (FM) is a basic constituent of vocalisation in many animals as well as in humans. In human speech, short rising and falling FM-sweeps of around 50 ms duration, called formant transitions, characterise individual speech sounds. There are two representations of FM in the ascending auditory pathway: a spectral representation, holding the instantaneous frequency of the stimuli; and a sweep representation, consisting of neurons that respond selectively to FM direction. To-date computational models use feedforward mechanisms to explain FM encoding. However, from neuroanatomy we know that there are massive feedback projections in the auditory pathway. Here, we found that a classical FM-sweep perceptual effect, the sweep pitch shift, cannot be explained by standard feedforward processing models. We hypothesised that the sweep pitch shift is caused by a predictive feedback mechanism. To test this hypothesis, we developed a novel model of FM encoding incorporating a predictive interaction between the sweep and the spectral representation. The model was designed to encode sweeps of the duration, modulation rate, and modulation shape of formant transitions. It fully accounted for experimental data that we acquired in a perceptual experiment with human participants as well as previously published experimental results. We also designed a new class of stimuli for a second perceptual experiment to further validate the model. Combined, our results indicate that predictive interaction between the frequency encoding and direction encoding neural representations plays an important role in the neural processing of FM. In the brain, this mechanism is likely to occur at early stages of the processing hierarchy.

Abstract rules drive adaptation in the subcortical sensory pathway.

The subcortical sensory pathways are the fundamental channels for mapping the outside world to our minds. Sensory pathways efficiently transmit information by adapting neural responses to the local statistics of the sensory input. The long-standing mechanistic explanation for this adaptive behaviour is that neural activity decreases with increasing regularities in the local statistics of the stimuli. An alternative account is that neural coding is directly driven by expectations of the sensory input. Here, we used abstract rules to manipulate expectations independently of local stimulus statistics. The ultra-high-field functional-MRI data show that abstract expectations can drive the response amplitude to tones in the human auditory pathway. These results provide first unambiguous evidence of abstract processing in a subcortical sensory pathway. They indicate that the neural representation of the outside world is altered by our prior beliefs even at initial points of the processing hierarchy.

Modeling and MEG evidence of early consonance processing in auditory cortex.

Pitch is a fundamental attribute of auditory perception. The interaction of concurrent pitches gives rise to a sensation that can be characterized by its degree of consonance or dissonance. In this work, we propose that human auditory cortex (AC) processes pitch and consonance through a common neural network mechanism operating at early cortical levels. First, we developed a new model of neural ensembles incorporating realistic neuronal and synaptic parameters to assess pitch processing mechanisms at early stages of AC. Next, we designed a magnetoencephalography (MEG) experiment to measure the neuromagnetic activity evoked by dyads with varying degrees of consonance or dissonance. MEG results show that dissonant dyads evoke a pitch onset response (POR) with a latency up to 36 ms longer than consonant dyads. Additionally, we used the model to predict the processing time of concurrent pitches; here, consonant pitch combinations were decoded faster than dissonant combinations, in line with the experimental observations. Specifically, we found a striking match between the predicted and the observed latency of the POR as elicited by the dyads. These novel results suggest that consonance processing starts early in human auditory cortex and may share the network mechanisms that are responsible for (single) pitch processing.

Insights on the Neuromagnetic Representation of Temporal Asymmetry in Human Auditory Cortex.

Communication sounds are typically asymmetric in time and human listeners are highly sensitive to this short-term temporal asymmetry. Nevertheless, causal neurophysiological correlates of auditory perceptual asymmetry remain largely elusive to our current analyses and models. Auditory modelling and animal electrophysiological recordings suggest that perceptual asymmetry results from the presence of multiple time scales of temporal integration, central to the auditory periphery. To test this hypothesis we recorded auditory evoked fields (AEF) elicited by asymmetric sounds in humans. We found a strong correlation between perceived tonal salience of ramped and damped sinusoids and the AEFs, as quantified by the amplitude of the N100m dynamics. The N100m amplitude increased with stimulus half-life time, showing a maximum difference between the ramped and damped stimulus for a modulation half-life time of 4 ms which is greatly reduced at 0.5 ms and 32 ms. This behaviour of the N100m closely parallels psychophysical data in a manner that: i) longer half-life times are associated with a stronger tonal percept, and ii) perceptual differences between damped and ramped are maximal at 4 ms half-life time. Interestingly, differences in evoked fields were significantly stronger in the right hemisphere, indicating some degree of hemispheric specialisation. Furthermore, the N100m magnitude was successfully explained by a pitch perception model using multiple scales of temporal integration of auditory nerve activity patterns. This striking correlation between AEFs, perception, and model predictions suggests that the physiological mechanisms involved in the processing of pitch evoked by temporal asymmetric sounds are reflected in the N100m.