Evidence for causal top-down frontal contributions to predictive processes in speech perception

• Published in: Nature communications Vol. 8; no. 1; pp. 2154 - 16
• Main Authors: Cope, Thomas E., Sohoglu, E., Sedley, W., Patterson, K., Jones, P. S., Wiggins, J., Dawson, C., Grube, M., Carlyon, R. P., Griffiths, T. D., Davis, Matthew H., Rowe, James B.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 18-12-2017; Nature Publishing Group; Nature Portfolio
• Subjects: 631/378/2649/1594; 631/443/376; 692/617/375/365; Acoustic Stimulation; Aged; Brain Mapping; Cognitive ability; Electric power; Electroencephalography; Female; Frontal Lobe - physiopathology; Humanities and Social Sciences; Humans; Magnetoencephalography; Male; Mathematical models; multidisciplinary; Nerve Net - physiopathology; Neural coding; Neurodegeneration; Perception; Predictions; Primary Progressive Nonfluent Aphasia - physiopathology; Science; Science (multidisciplinary); Sensory integration; Somatosensory cortex; Speech; Speech - physiology; Speech perception; Speech Perception - physiology; Temporal lobe; Temporal Lobe - physiopathology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-017-01958-7

Perception relies on the integration of sensory information and prior expectations. Here we show that selective neurodegeneration of human frontal speech regions results in delayed reconciliation of predictions in temporal cortex. These temporal regions were not atrophic, displayed normal evoked magnetic and electrical power, and preserved neural sensitivity to manipulations of sensory detail. Frontal neurodegeneration does not prevent the perceptual effects of contextual information; instead, prior expectations are applied inflexibly. The precision of predictions correlates with beta power, in line with theoretical models of the neural instantiation of predictive coding. Fronto-temporal interactions are enhanced while participants reconcile prior predictions with degraded sensory signals. Excessively precise predictions can explain several challenging phenomena in frontal aphasias, including agrammatism and subjective difficulties with speech perception. This work demonstrates that higher-level frontal mechanisms for cognitive and behavioural flexibility make a causal functional contribution to the hierarchical generative models underlying speech perception.
The role of frontal lobes in speech perception is controversial. Here, the authors show that neurodegeneration of frontal speech regions delays prediction reconciliation in temporal cortex and results in inflexible prior expectations, indicating that fronto-temporal interactions determine predictive processes in speech.