Abstract

Generative models, such as predictive coding, posit that perception results from a combination of sensory input and prior prediction, each weighted by its precision (inverse variance), with incongruence between these termed prediction error (deviation from prediction) or surprise (negative log probability of the sensory input). However, direct evidence for such a system, and the physiological basis of its computations, is lacking. Using an auditory stimulus whose pitch value changed according to specific rules, we controlled and separated the three key computational variables underlying perception, and discovered, using direct recordings from human auditory cortex, that surprise due to prediction violations is encoded by local field potential oscillations in the gamma band (>30 Hz), changes to predictions in the beta band (12-30 Hz), and that the precision of predictions appears to quantitatively relate to alpha band oscillations (8-12 Hz). These results confirm oscillatory codes for critical aspects of generative models of perception.

Article and author information

Author details

  1. William Sedley

    Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
    For correspondence
    willsedley@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Phillip E Gander

    Human Brain Research Laboratory, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Sukhbinder Kumar

    Institute of Neuroscience, Newcastle University, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Christopher K Kovach

    Human Brain Research Laboratory, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Hiroyuki Oya

    Human Brain Research Laboratory, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Hiroto Kawasaki

    Human Brain Research Laboratory, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Matthew A Howard

    Human Brain Research Laboratory, University of Iowa, Iowa City, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Timothy D Griffiths

    Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Human subjects: The study was approved by the University of Iowa Institutional Review Board, and with full informed written consent from all participants.

Copyright

© 2016, Sedley et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 4,789
    views
  • 1,030
    downloads
  • 151
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. William Sedley
  2. Phillip E Gander
  3. Sukhbinder Kumar
  4. Christopher K Kovach
  5. Hiroyuki Oya
  6. Hiroto Kawasaki
  7. Matthew A Howard
  8. Timothy D Griffiths
(2016)
Neural Signatures of Perceptual Inference
eLife 5:e11476.
https://doi.org/10.7554/eLife.11476

Share this article

https://doi.org/10.7554/eLife.11476

Further reading

    1. Neuroscience
    2. Physics of Living Systems
    Moritz Schloetter, Georg U Maret, Christoph J Kleineidam
    Research Article

    Neurons generate and propagate electrical pulses called action potentials which annihilate on arrival at the axon terminal. We measure the extracellular electric field generated by propagating and annihilating action potentials and find that on annihilation, action potentials expel a local discharge. The discharge at the axon terminal generates an inhomogeneous electric field that immediately influences target neurons and thus provokes ephaptic coupling. Our measurements are quantitatively verified by a powerful analytical model which reveals excitation and inhibition in target neurons, depending on position and morphology of the source-target arrangement. Our model is in full agreement with experimental findings on ephaptic coupling at the well-studied Basket cell-Purkinje cell synapse. It is able to predict ephaptic coupling for any other synaptic geometry as illustrated by a few examples.

    1. Neuroscience
    Gergely F Turi, Sasa Teng ... Yueqing Peng
    Research Article

    Synchronous neuronal activity is organized into neuronal oscillations with various frequency and time domains across different brain areas and brain states. For example, hippocampal theta, gamma, and sharp wave oscillations are critical for memory formation and communication between hippocampal subareas and the cortex. In this study, we investigated the neuronal activity of the dentate gyrus (DG) with optical imaging tools during sleep-wake cycles in mice. We found that the activity of major glutamatergic cell populations in the DG is organized into infraslow oscillations (0.01–0.03 Hz) during NREM sleep. Although the DG is considered a sparsely active network during wakefulness, we found that 50% of granule cells and about 25% of mossy cells exhibit increased activity during NREM sleep, compared to that during wakefulness. Further experiments revealed that the infraslow oscillation in the DG was correlated with rhythmic serotonin release during sleep, which oscillates at the same frequency but in an opposite phase. Genetic manipulation of 5-HT receptors revealed that this neuromodulatory regulation is mediated by Htr1a receptors and the knockdown of these receptors leads to memory impairment. Together, our results provide novel mechanistic insights into how the 5-HT system can influence hippocampal activity patterns during sleep.