1. Neuroscience

Dissociable laminar profiles of concurrent bottom-up and top-down modulation in the human visual cortex

  1. Samuel JD Lawrence
  2. David G Norris
  3. Floris P de Lange  Is a corresponding author
  1. Radboud University Nijmegen, Netherlands
https://doi.org/10.7554/eLife.44422
Share this article
Cite this article
  1. Samuel JD Lawrence
  2. David G Norris
  3. Floris P de Lange
(2019)
Dissociable laminar profiles of concurrent bottom-up and top-down modulation in the human visual cortex
eLife 8:e44422.
https://doi.org/10.7554/eLife.44422
  2. Download BibTeX
  3. Download .RIS

Abstract

Recent developments in human neuroimaging make it possible to non-invasively measure neural activity from different cortical layers. This can potentially reveal not only which brain areas are engaged by a task, but also how. Specifically, bottom-up and top-down responses are associated with distinct laminar profiles. Here, we measured lamina-resolved fMRI responses during a visual task designed to induce concurrent bottom-up and top-down modulations via orthogonal manipulations of stimulus contrast and feature-based attention. BOLD responses were modulated by both stimulus contrast (bottom-up) and by engaging feature-based attention (top-down). Crucially, these effects operated at different cortical depths: Bottom-up modulations were strongest in the middle cortical layer and weaker in deep and superficial layers, while top-down modulations were strongest in the superficial layers. As such, we demonstrate that laminar activity profiles can discriminate between concurrent top-down and bottom-up processing, and are diagnostic of how a brain region is activated.

Data availability

Data and code used for stimulus presentation and analysis are available online at the Donders Research Data Repository: https://data.donders.ru.nl/collections/di/dccn/DSC_3018028.04_752

The following data sets were generated

Article and author information

Author details

  1. Samuel JD Lawrence

    Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    No competing interests declared.

  2. David G Norris

    Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands
    Competing interests
    No competing interests declared.

  3. Floris P de Lange

    Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands
    For correspondence
    floris.delange@donders.ru.nl
    Competing interests
    Floris P de Lange, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6730-1452

Funding

Netherlands Organisation for Scientific Research (Vidi)

  • Floris P de Lange

European Research Council Starting Grant (CONTEXTVISION)

  • Floris P de Lange

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 participants gave written informed consent and the study was approved by the local ethics committees (CMO region Arnhem-Nijmegen, The Netherlands, and ethics committee of the University Duisburg-Essen, Germany). Protocol CMO 2014/288

Reviewing Editor

  1. Christian Büchel, University Medical Center Hamburg-Eppendorf, Germany

Version history

  1. Received: December 14, 2018
  2. Accepted: May 3, 2019
  3. Accepted Manuscript published: May 7, 2019 (version 1)
  4. Version of Record published: May 28, 2019 (version 2)

Copyright

© 2019, Lawrence 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

  • 2,744
    Page views
  • 431
    Downloads
  • 39
    Citations

Article citation count generated by polling the highest count across the following sources: Scopus, Crossref, 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. Samuel JD Lawrence
  2. David G Norris
  3. Floris P de Lange
(2019)
Dissociable laminar profiles of concurrent bottom-up and top-down modulation in the human visual cortex
eLife 8:e44422.
https://doi.org/10.7554/eLife.44422

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Associative memory neurons of encoding multi-modal signals are recruited by neuroligin-3-mediated new synapse formation

    Yang Xu, Tian-liang Cui ... Jin-Hui Wang
    Research Article

    The joint storage and reciprocal retrieval of learnt associated signals are presumably encoded by associative memory cells. In the accumulation and enrichment of memory contents in lifespan, a signal often becomes a core signal associatively shared for other signals. One specific group of associative memory neurons that encode this core signal likely interconnects multiple groups of associative memory neurons that encode these other signals for their joint storage and reciprocal retrieval. We have examined this hypothesis in a mouse model of associative learning by pairing the whisker tactile signal sequentially with the olfactory signal, the gustatory signal, and the tail-heating signal. Mice experienced this associative learning show the whisker fluctuation induced by olfactory, gustatory, and tail-heating signals, or the other way around, that is, memories to multi-modal associated signals featured by their reciprocal retrievals. Barrel cortical neurons in these mice become able to encode olfactory, gustatory, and tail-heating signals alongside the whisker signal. Barrel cortical neurons interconnect piriform, S1-Tr, and gustatory cortical neurons. With the barrel cortex as the hub, the indirect activation occurs among piriform, gustatory, and S1-Tr cortices for the second-order associative memory. These associative memory neurons recruited to encode multi-modal signals in the barrel cortex for associative memory are downregulated by neuroligin-3 knockdown. Thus, associative memory neurons can be recruited as the core cellular substrate to memorize multiple associated signals for the first-order and the second-order of associative memories by neuroligin-3-mediated synapse formation, which constitutes neuronal substrates of cognitive activities in the field of memoriology.

    1. Chromosomes and Gene Expression
    2. Neuroscience

    Avoiding false discoveries in single-cell RNA-seq by revisiting the first Alzheimer’s disease dataset

    Alan E Murphy, Nurun Fancy, Nathan Skene
    Research Article

    Mathys et al. conducted the first single-nucleus RNA-seq (snRNA-seq) study of Alzheimer’s disease (AD) (Mathys et al., 2019). With bulk RNA-seq, changes in gene expression across cell types can be lost, potentially masking the differentially expressed genes (DEGs) across different cell types. Through the use of single-cell techniques, the authors benefitted from increased resolution with the potential to uncover cell type-specific DEGs in AD for the first time. However, there were limitations in both their data processing and quality control and their differential expression analysis. Here, we correct these issues and use best-practice approaches to snRNA-seq differential expression, resulting in 549 times fewer DEGs at a false discovery rate of 0.05. Thus, this study highlights the impact of quality control and differential analysis methods on the discovery of disease-associated genes and aims to refocus the AD research field away from spuriously identified genes.

    1. Neuroscience

    Network-level changes in the brain underlie fear memory strength

    Josue Haubrich, Karim Nader
    Research Article

    The strength of a fear memory significantly influences whether it drives adaptive or maladaptive behavior in the future. Yet, how mild and strong fear memories differ in underlying biology is not well understood. We hypothesized that this distinction may not be exclusively the result of changes within specific brain regions, but rather the outcome of collective changes in connectivity across multiple regions within the neural network. To test this, rats were fear conditioned in protocols of varying intensities to generate mild or strong memories. Neuronal activation driven by recall was measured using c-fos immunohistochemistry in 12 brain regions implicated in fear learning and memory. The interregional coordinated brain activity was computed and graph-based functional networks were generated to compare how mild and strong fear memories differ at the systems level. Our results show that mild fear recall is supported by a well-connected brain network with small-world properties in which the amygdala is well-positioned to be modulated by other regions. In contrast, this connectivity is disrupted in strong fear memories and the amygdala is isolated from other regions. These findings indicate that the neural systems underlying mild and strong fear memories differ, with implications for understanding and treating disorders of fear dysregulation.