Causal links between parietal alpha activity and spatial auditory attention

  1. Yuqi Deng
  2. Robert MG Reinhart
  3. Inyong Choi
  4. Barbara G Shinn-Cunningham  Is a corresponding author
  1. Boston University, United States
  2. University of Iowa, United States
  3. Carnegie Mellon University, United States

Abstract

Both visual and auditory spatial selective attention result in lateralized alpha (8-14 Hz) oscillatory power in parietal cortex: alpha increases in the hemisphere ipsilateral to attentional focus. Brain stimulation studies suggest a causal relationship between parietal alpha and suppression of the representation of contralateral visual space. However, there is no evidence that parietal alpha controls auditory spatial attention. Here, we performed high definition transcranial alternating current stimulation (HD-tACS) on human subjects performing an auditory task in which they directed attention based on either spatial or nonspatial features. Alpha (10 Hz) but not theta (6 Hz) HD-tACS of right parietal cortex interfered with attending left but not right auditory space. Parietal stimulation had no effect for nonspatial auditory attention. Moreover, performance in post-stimulation trials returned rapidly to baseline. These results demonstrate a causal, frequency-, hemispheric-, and task-specific effect of parietal alpha brain stimulation on top-down control of auditory spatial attention.

Data availability

Data are available from Dryad at https://dx.doi.org/10.5061/dryad.c031nv7

The following data sets were generated

Article and author information

Author details

  1. Yuqi Deng

    Biomedical Engineering, Boston University, Boston, United States
    Competing interests
    No competing interests declared.
  2. Robert MG Reinhart

    Psychological and Brain Sciences, Boston University, Boston, United States
    Competing interests
    No competing interests declared.
  3. Inyong Choi

    Communication Sciences and Disorders, University of Iowa, Iowa, United States
    Competing interests
    No competing interests declared.
  4. Barbara G Shinn-Cunningham

    Carnegie Mellon Neuroscience Institute, Carnegie Mellon University, Pittsburgh, United States
    For correspondence
    bgsc@andrew.cmu.edu
    Competing interests
    Barbara G Shinn-Cunningham, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5096-5914

Funding

National Institutes of Health (R01 DC015988)

  • Barbara G Shinn-Cunningham

Office of Naval Research (N000141812069)

  • Barbara G Shinn-Cunningham

National Institutes of Health (R01 MH-114877)

  • Robert MG Reinhart

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

Ethics

Human subjects: All subjects gave informed consent, as approved by the Boston University Charles River Campus IRB, under protocol 3597E.

Copyright

© 2019, Deng 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

  • 2,309
    views
  • 334
    downloads
  • 62
    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. Yuqi Deng
  2. Robert MG Reinhart
  3. Inyong Choi
  4. Barbara G Shinn-Cunningham
(2019)
Causal links between parietal alpha activity and spatial auditory attention
eLife 8:e51184.
https://doi.org/10.7554/eLife.51184

Share this article

https://doi.org/10.7554/eLife.51184

Further reading

    1. Neuroscience
    Jack W Lindsey, Jeffrey Markowitz ... Ashok Litwin-Kumar
    Research Article

    Spiny projection neurons (SPNs) in dorsal striatum are often proposed as a locus of reinforcement learning in the basal ganglia. Here, we identify and resolve a fundamental inconsistency between striatal reinforcement learning models and known SPN synaptic plasticity rules. Direct-pathway (dSPN) and indirect-pathway (iSPN) neurons, which promote and suppress actions, respectively, exhibit synaptic plasticity that reinforces activity associated with elevated or suppressed dopamine release. We show that iSPN plasticity prevents successful learning, as it reinforces activity patterns associated with negative outcomes. However, this pathological behavior is reversed if functionally opponent dSPNs and iSPNs, which promote and suppress the current behavior, are simultaneously activated by efferent input following action selection. This prediction is supported by striatal recordings and contrasts with prior models of SPN representations. In our model, learning and action selection signals can be multiplexed without interference, enabling learning algorithms beyond those of standard temporal difference models.

    1. Neuroscience
    J Daniel Obray, Erik T Wilkes ... L Judson Chandler
    Research Article

    Binge drinking is common among adolescents despite mounting evidence linking it to various adverse health outcomes that include heightened pain perception. The prelimbic (PrL) cortex is vulnerable to insult from adolescent alcohol exposure and receives input from the basolateral amygdala (BLA) while sending projections to the ventrolateral periaqueductal gray (vlPAG) – two brain regions implicated in nociception. In this study, adolescent intermittent ethanol (AIE) exposure was carried out in male and female rats using a vapor inhalation procedure. Assessments of mechanical and thermal sensitivity revealed that AIE exposure-induced protracted mechanical allodynia. To investigate synaptic function at BLA inputs onto defined populations of PrL neurons, retrobeads and viral labeling were combined with optogenetics and slice electrophysiology. Recordings from retrobead labeled cells in the PrL revealed AIE reduced BLA-driven feedforward inhibition of neurons projecting from the PrL to the vlPAG, resulting in augmented excitation/inhibition (E/I) balance and increased intrinsic excitability. Consistent with this finding, recordings from virally tagged PrL parvalbumin interneurons (PVINs) demonstrated that AIE exposure reduced both E/I balance at BLA inputs onto PVINs and PVIN intrinsic excitability. These findings provide compelling evidence that AIE alters synaptic function and intrinsic excitability within a prefrontal nociceptive circuit.