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.

Reviewing Editor

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

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.

Version 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

  • 2,351
    Page views
  • 308
    Downloads
  • 35
    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

Share this article

https://doi.org/10.7554/eLife.30334

Further reading

    1. Neuroscience
    Kiwamu Kudo, Kamalini G Ranasinghe ... Srikantan S Nagarajan
    Research Article

    Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.

    1. Medicine
    2. Neuroscience
    Luisa Fassi, Shachar Hochman ... Roi Cohen Kadosh
    Research Article

    In recent years, there has been debate about the effectiveness of treatments from different fields, such as neurostimulation, neurofeedback, brain training, and pharmacotherapy. This debate has been fuelled by contradictory and nuanced experimental findings. Notably, the effectiveness of a given treatment is commonly evaluated by comparing the effect of the active treatment versus the placebo on human health and/or behaviour. However, this approach neglects the individual’s subjective experience of the type of treatment she or he received in establishing treatment efficacy. Here, we show that individual differences in subjective treatment - the thought of receiving the active or placebo condition during an experiment - can explain variability in outcomes better than the actual treatment. We analysed four independent datasets (N = 387 participants), including clinical patients and healthy adults from different age groups who were exposed to different neurostimulation treatments (transcranial magnetic stimulation: Studies 1 and 2; transcranial direct current stimulation: Studies 3 and 4). Our findings show that the inclusion of subjective treatment can provide a better model fit either alone or in interaction with objective treatment (defined as the condition to which participants are assigned in the experiment). These results demonstrate the significant contribution of subjective experience in explaining the variability of clinical, cognitive, and behavioural outcomes. We advocate for existing and future studies in clinical and non-clinical research to start accounting for participants’ subjective beliefs and their interplay with objective treatment when assessing the efficacy of treatments. This approach will be crucial in providing a more accurate estimation of the treatment effect and its source, allowing the development of effective and reproducible interventions.