Suppression and facilitation of human neural responses

  1. Michael-Paul Schallmo  Is a corresponding author
  2. Alexander M Kale
  3. Rachel Millin
  4. Anastasia V Flevaris
  5. Zoran Brkanac
  6. Richard AE Edden
  7. Raphael A Bernier
  8. Scott Murray
  1. University of Washington, United States
  2. Johns Hopkins University, United States

Abstract

Efficient neural processing depends on regulating responses through suppression and facilitation of neural activity. Utilizing a well-known visual motion paradigm that evokes behavioral suppression and facilitation, and combining 5 different methodologies (behavioral psychophysics, computational modeling, functional MRI, pharmacology, and magnetic resonance spectroscopy), we provide evidence that challenges commonly held assumptions about the neural processes underlying suppression and facilitation. We show that: 1) both suppression and facilitation can emerge from a single, computational principle - divisive normalization; there is no need to invoke separate neural mechanisms, 2) neural suppression and facilitation in the motion-selective area MT mirror perception, but strong suppression also occurs in earlier visual areas, and 3) suppression is not primarily driven by GABA-mediated inhibition. Thus, while commonly used spatial suppression paradigms may provide insight into neural response magnitudes in visual areas, they should not be used to infer neural inhibition.

Data availability

The following data sets were generated

Article and author information

Author details

  1. Michael-Paul Schallmo

    Department of Psychology, University of Washington, Seattle, United States
    For correspondence
    schallmo@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8252-8607
  2. Alexander M Kale

    Department of Psychology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7668-2800
  3. Rachel Millin

    Department of Psychology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Anastasia V Flevaris

    Department of Psychology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Zoran Brkanac

    Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Richard AE Edden

    Department of Radiology and Radiological Science, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Raphael A Bernier

    Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Scott Murray

    Department of Psychology, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Eye Institute (F32 EY025121)

  • Michael-Paul Schallmo
  • Scott Murray

National Institute of Mental Health (R01 MH106520)

  • Raphael A Bernier
  • Scott Murray

National Institute of Biomedical Imaging and Bioengineering (P41 EB015909)

  • Richard AE Edden

National Eye Institute (T32 EY007031)

  • Michael-Paul Schallmo
  • Scott Murray

National Institute of Biomedical Imaging and Bioengineering (R01 EB016089)

  • Richard AE Edden

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: Subjects provided written informed consent prior to participation and were compensated for their time. All experimental procedures were approved by the University of Washington Institutional Review Board (protocol #s: 556, 1678, 28148), and conformed to the ethical principles for research on human subjects from the Declaration of Helsinki.

Reviewing Editor

  1. Nicholas Turk-Browne, Princeton University, United States

Publication history

  1. Received: July 11, 2017
  2. Accepted: January 26, 2018
  3. Accepted Manuscript published: January 29, 2018 (version 1)
  4. Version of Record published: February 14, 2018 (version 2)

Copyright

© 2018, Schallmo 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

  • 2,065
    Page views
  • 283
    Downloads
  • 27
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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. Michael-Paul Schallmo
  2. Alexander M Kale
  3. Rachel Millin
  4. Anastasia V Flevaris
  5. Zoran Brkanac
  6. Richard AE Edden
  7. Raphael A Bernier
  8. Scott Murray
(2018)
Suppression and facilitation of human neural responses
eLife 7:e30334.
https://doi.org/10.7554/eLife.30334

Further reading

    1. Neuroscience
    Arefeh Sherafati et al.
    Research Article Updated

    Cochlear implants are neuroprosthetic devices that can restore hearing in people with severe to profound hearing loss by electrically stimulating the auditory nerve. Because of physical limitations on the precision of this stimulation, the acoustic information delivered by a cochlear implant does not convey the same level of acoustic detail as that conveyed by normal hearing. As a result, speech understanding in listeners with cochlear implants is typically poorer and more effortful than in listeners with normal hearing. The brain networks supporting speech understanding in listeners with cochlear implants are not well understood, partly due to difficulties obtaining functional neuroimaging data in this population. In the current study, we assessed the brain regions supporting spoken word understanding in adult listeners with right unilateral cochlear implants (n=20) and matched controls (n=18) using high-density diffuse optical tomography (HD-DOT), a quiet and non-invasive imaging modality with spatial resolution comparable to that of functional MRI. We found that while listening to spoken words in quiet, listeners with cochlear implants showed greater activity in the left prefrontal cortex than listeners with normal hearing, specifically in a region engaged in a separate spatial working memory task. These results suggest that listeners with cochlear implants require greater cognitive processing during speech understanding than listeners with normal hearing, supported by compensatory recruitment of the left prefrontal cortex.

    1. Neuroscience
    Mohammad Ali Salehinejad et al.
    Research Article Updated

    Sleep strongly affects synaptic strength, making it critical for cognition, especially learning and memory formation. Whether and how sleep deprivation modulates human brain physiology and cognition is not well understood. Here we examined how overnight sleep deprivation vs overnight sufficient sleep affects (a) cortical excitability, measured by transcranial magnetic stimulation, (b) inducibility of long-term potentiation (LTP)- and long-term depression (LTD)-like plasticity via transcranial direct current stimulation (tDCS), and (c) learning, memory, and attention. The results suggest that sleep deprivation upscales cortical excitability due to enhanced glutamate-related cortical facilitation and decreases and/or reverses GABAergic cortical inhibition. Furthermore, tDCS-induced LTP-like plasticity (anodal) abolishes while the inhibitory LTD-like plasticity (cathodal) converts to excitatory LTP-like plasticity under sleep deprivation. This is associated with increased EEG theta oscillations due to sleep pressure. Finally, we show that learning and memory formation, behavioral counterparts of plasticity, and working memory and attention, which rely on cortical excitability, are impaired during sleep deprivation. Our data indicate that upscaled brain excitability and altered plasticity, due to sleep deprivation, are associated with impaired cognitive performance. Besides showing how brain physiology and cognition undergo changes (from neurophysiology to higher-order cognition) under sleep pressure, the findings have implications for variability and optimal application of noninvasive brain stimulation.