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      Predictive Top-Down Integration of Prior Knowledge during Speech Perception

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          Abstract

          A striking feature of human perception is that our subjective experience depends not only on sensory information from the environment but also on our prior knowledge or expectations. The precise mechanisms by which sensory information and prior knowledge are integrated remain unclear, with longstanding disagreement concerning whether integration is strictly feedforward or whether higher-level knowledge influences sensory processing through feedback connections. Here we used concurrent EEG and MEG recordings to determine how sensory information and prior knowledge are integrated in the brain during speech perception. We manipulated listeners' prior knowledge of speech content by presenting matching, mismatching, or neutral written text before a degraded (noise-vocoded) spoken word. When speech conformed to prior knowledge, subjective perceptual clarity was enhanced. This enhancement in clarity was associated with a spatiotemporal profile of brain activity uniquely consistent with a feedback process: activity in the inferior frontal gyrus was modulated by prior knowledge before activity in lower-level sensory regions of the superior temporal gyrus. In parallel, we parametrically varied the level of speech degradation, and therefore the amount of sensory detail, so that changes in neural responses attributable to sensory information and prior knowledge could be directly compared. Although sensory detail and prior knowledge both enhanced speech clarity, they had an opposite influence on the evoked response in the superior temporal gyrus. We argue that these data are best explained within the framework of predictive coding in which sensory activity is compared with top-down predictions and only unexplained activity propagated through the cortical hierarchy.

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          Author and article information

          Journal
          J Neurosci
          J. Neurosci
          jneuro
          jneurosci
          J. Neurosci
          The Journal of Neuroscience
          Society for Neuroscience
          0270-6474
          1529-2401
          20 June 2012
          : 32
          : 25
          : 8443-8453
          Affiliations
          [1]Medical Research Council Cognition and Brain Sciences Unit, Cambridge CB2 7EF, United Kingdom
          Author notes
          Correspondence should be addressed to either Ediz Sohoglu or Matthew H. Davis, Medical Research Council Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge CB2 7EF, UK. e.sohoglu@ 123456gmail.com , matt.davis@ 123456mrc-cbu.cam.ac.uk

          Author contributions: E.S., J.E.P., R.P.C., and M.H.D. designed research; E.S. performed research; E.S. analyzed data; E.S., J.E.P., R.P.C., and M.H.D. wrote the paper.

          J. E. Peelle's present address Center for Cognitive Neuroscience and Department of Neurology, University of Pennsylvania, Philadelphia, PA 19104.

          Article
          PMC6620994 PMC6620994 6620994 3779290
          10.1523/JNEUROSCI.5069-11.2012
          6620994
          22723684
          7dc4d257-d0ba-4961-888a-7a82aad0a57c
          Copyright © 2012 the authors 0270-6474/12/328443-11$15.00/0
          History
          : 6 October 2011
          : 19 March 2012
          : 20 April 2012
          Categories
          Articles
          Behavioral/Systems/Cognitive

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