Fine-scale computations for adaptive processing in the human brain

Abstract

Adapting to the environment statistics by reducing brain responses to repetitive sensory information is key for efficient information processing. Yet, the fine-scale computations that support this adaptive processing in the human brain remain largely unknown. Here, we capitalize on the sub-millimetre resolution of ultra-high field imaging to examine fMRI signals across cortical depth and discern competing hypotheses about the brain mechanisms (feedforward vs. feedback) that mediate adaptive processing. We demonstrate layer-specific suppressive processing within visual cortex, as indicated by stronger BOLD decrease in superficial and middle than deeper layers for gratings that were repeatedly presented at the same orientation. Further, we show altered functional connectivity for adaptation: enhanced feedforward connectivity from V1 to higher visual areas, short-range feedback connectivity between V1 and V2 and long-range feedback occipito-parietal connectivity. Our findings provide evidence for a circuit of local recurrent and feedback interactions that mediate rapid brain plasticity for adaptive information processing.

Data availability

Source data have been provided for Figures 3, 4, and 5. Data can also be found on the Cambridge Data repository

Article and author information

Author details

  1. Elisa Zamboni

    Psychology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Valentin G Kemper

    Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Nuno Reis Goncalves

    Psychology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Ke Jia

    Psychology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Vasilis M Karlaftis

    Psychology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1285-1593
  6. Samuel J Bell

    Psychology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Joseph Giorgio

    Psychology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Reuben Rideaux

    Psychology, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8416-005X
  9. Rainer Goebel

    Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  10. Zoe Kourtzi

    Psychology, University of Cambridge, Cambridge, United Kingdom
    For correspondence
    zk240@cam.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9441-7832

Funding

Biotechnology and Biological Sciences Research Council (H012508)

  • Zoe Kourtzi

Biotechnology and Biological Sciences Research Council (BB/P021255/1)

  • Zoe Kourtzi

Wellcome Trust (205067/Z/16/Z)

  • Zoe Kourtzi

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

Reviewing Editor

  1. Ming Meng, South China Normal University, China

Ethics

Human subjects: Participants gave written informed consent. The study was approved by the local Ethical Committee of the Faculty of Psychology and Neuroscience at Maastricht University and the University of Cambridge Ethics Committee (ethics number PRE2018.003).

Version history

  1. Received: April 7, 2020
  2. Accepted: November 9, 2020
  3. Accepted Manuscript published: November 10, 2020 (version 1)
  4. Version of Record published: November 25, 2020 (version 2)

Copyright

© 2020, Zamboni 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

  • 1,315
    views
  • 193
    downloads
  • 7
    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. Elisa Zamboni
  2. Valentin G Kemper
  3. Nuno Reis Goncalves
  4. Ke Jia
  5. Vasilis M Karlaftis
  6. Samuel J Bell
  7. Joseph Giorgio
  8. Reuben Rideaux
  9. Rainer Goebel
  10. Zoe Kourtzi
(2020)
Fine-scale computations for adaptive processing in the human brain
eLife 9:e57637.
https://doi.org/10.7554/eLife.57637

Share this article

https://doi.org/10.7554/eLife.57637

Further reading

    1. Neuroscience
    Tara Ghafari, Cecilia Mazzetti ... Ole Jensen
    Research Article

    Evidence suggests that subcortical structures play a role in high-level cognitive functions such as the allocation of spatial attention. While there is abundant evidence in humans for posterior alpha band oscillations being modulated by spatial attention, little is known about how subcortical regions contribute to these oscillatory modulations, particularly under varying conditions of cognitive challenge. In this study, we combined MEG and structural MRI data to investigate the role of subcortical structures in controlling the allocation of attentional resources by employing a cued spatial attention paradigm with varying levels of perceptual load. We asked whether hemispheric lateralization of volumetric measures of the thalamus and basal ganglia predicted the hemispheric modulation of alpha-band power. Lateral asymmetry of the globus pallidus, caudate nucleus, and thalamus predicted attention-related modulations of posterior alpha oscillations. When the perceptual load was applied to the target and the distractor was salient caudate nucleus asymmetry predicted alpha-band modulations. Globus pallidus was predictive of alpha-band modulations when either the target had a high load, or the distractor was salient, but not both. Finally, the asymmetry of the thalamus predicted alpha band modulation when neither component of the task was perceptually demanding. In addition to delivering new insight into the subcortical circuity controlling alpha oscillations with spatial attention, our finding might also have clinical applications. We provide a framework that could be followed for detecting how structural changes in subcortical regions that are associated with neurological disorders can be reflected in the modulation of oscillatory brain activity.

    1. Neuroscience
    Annette Pisanski, Mitchell Prostebby ... Silvia Pagliardini
    Research Article

    The lateral parafacial area (pFL) is a crucial region involved in respiratory control, particularly in generating active expiration through an expiratory oscillatory network. Active expiration involves rhythmic abdominal (ABD) muscle contractions during late-expiration, increasing ventilation during elevated respiratory demands. The precise anatomical location of the expiratory oscillator within the ventral medulla’s rostro-caudal axis is debated. While some studies point to the caudal tip of the facial nucleus (VIIc) as the oscillator’s core, others suggest more rostral areas. Our study employed bicuculline (a γ-aminobutyric acid type A [GABA-A] receptor antagonist) injections at various pFL sites (–0.2 mm to +0.8 mm from VIIc) to investigate the impact of GABAergic disinhibition on respiration. These injections consistently elicited ABD recruitment, but the response strength varied along the rostro-caudal zone. Remarkably, the most robust and enduring changes in tidal volume, minute ventilation, and combined respiratory responses occurred at more rostral pFL locations (+0.6/+0.8 mm from VIIc). Multivariate analysis of the respiratory cycle further differentiated between locations, revealing the core site for active expiration generation with this experimental approach. Our study advances our understanding of neural mechanisms governing active expiration and emphasizes the significance of investigating the rostral pFL region.