Temporal lobe perceptual predictions for speech are instantiated in motor cortex and reconciled by inferior frontal cortex
Thomas E. Cope,
Ediz Sohoglu,
Katie A. Peterson,
P. Simon Jones,
Catarina Rua,
Luca Passamonti,
William Sedley,
Brechtje Post,
Jan Coebergh,
Christopher R. Butler,
Peter Garrard,
Khaled Abdel-Aziz,
Masud Husain,
Timothy D. Griffiths,
Karalyn Patterson,
Matthew H. Davis,
James B. Rowe
Affiliations
Thomas E. Cope
Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, UK; Medical Research Council Cognition and Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, UK; Cambridge University Hospitals NHS Trust, Cambridge CB2 0QQ, UK; Corresponding author
Ediz Sohoglu
Medical Research Council Cognition and Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, UK; School of Psychology, University of Sussex, Brighton BN1 9RH, UK
Katie A. Peterson
Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, UK; Department of Radiology, University of Cambridge, Cambridge CB2 0QQ, UK
P. Simon Jones
Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, UK
Catarina Rua
Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, UK
Luca Passamonti
Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, UK
William Sedley
Biosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK
Brechtje Post
Theoretical and Applied Linguistics, Faculty of Modern & Medieval Languages & Linguistics, University of Cambridge, Cambridge CB3 9DA, UK
Jan Coebergh
Ashford and St Peter’s Hospital, Ashford TW15 3AA, UK; St George’s Hospital, London SW17 0QT, UK
Christopher R. Butler
Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, UK; Faculty of Medicine, Department of Brain Sciences, Imperial College London, London W12 0NN, UK
Peter Garrard
St George’s Hospital, London SW17 0QT, UK; Molecular and Clinical Sciences Research Institute, St. George’s, University of London, London SW17 0RE, UK
Khaled Abdel-Aziz
Ashford and St Peter’s Hospital, Ashford TW15 3AA, UK; St George’s Hospital, London SW17 0QT, UK
Masud Husain
Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, UK
Timothy D. Griffiths
Biosciences Institute, Newcastle University, Newcastle upon Tyne NE2 4HH, UK
Karalyn Patterson
Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, UK; Medical Research Council Cognition and Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, UK
Matthew H. Davis
Medical Research Council Cognition and Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, UK
James B. Rowe
Department of Clinical Neurosciences, University of Cambridge, Cambridge CB2 0SZ, UK; Medical Research Council Cognition and Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, UK; Cambridge University Hospitals NHS Trust, Cambridge CB2 0QQ, UK
Summary: Humans use predictions to improve speech perception, especially in noisy environments. Here we use 7-T functional MRI (fMRI) to decode brain representations of written phonological predictions and degraded speech signals in healthy humans and people with selective frontal neurodegeneration (non-fluent variant primary progressive aphasia [nfvPPA]). Multivariate analyses of item-specific patterns of neural activation indicate dissimilar representations of verified and violated predictions in left inferior frontal gyrus, suggestive of processing by distinct neural populations. In contrast, precentral gyrus represents a combination of phonological information and weighted prediction error. In the presence of intact temporal cortex, frontal neurodegeneration results in inflexible predictions. This manifests neurally as a failure to suppress incorrect predictions in anterior superior temporal gyrus and reduced stability of phonological representations in precentral gyrus. We propose a tripartite speech perception network in which inferior frontal gyrus supports prediction reconciliation in echoic memory, and precentral gyrus invokes a motor model to instantiate and refine perceptual predictions for speech.
