Multiple concurrent predictions inform prediction error in the human auditory pathway

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

Abstract

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 male and female human participants listened to sequences of sounds: pure tones in the first experiment, 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, 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.

Details

Original languageEnglish
Article numberJN-RM-2219-22
JournalThe Journal of neuroscience : the official journal of the Society for Neuroscience
Volume44
Issue number1
Early online date10 Nov 2023
Publication statusPublished - 3 Jan 2024
Peer-reviewedYes

External IDs

ORCID /0000-0001-7989-5860/work/147142862
ORCID /0000-0002-8643-1543/work/147142951
unpaywall 10.1523/jneurosci.2219-22.2023
Scopus 85181586478

Keywords

Keywords

  • Acoustic Stimulation, Auditory Cortex/physiology, Auditory Pathways/physiology, Auditory Perception/physiology, Brain/physiology, Female, Humans, Male, Sound