Foveal vision anticipates defining features of eye movement targets

  1. Lisa M Kroell  Is a corresponding author
  2. Martin Rolfs  Is a corresponding author
  1. Humboldt-Universität zu Berlin, Germany

Abstract

High-acuity foveal processing is vital for human vision. Nonetheless, little is known about how the preparation of large-scale rapid eye movements (saccades) affects visual sensitivity in the center of gaze. Based on findings from passive fixation tasks, we hypothesized that during saccade preparation, foveal processing anticipates soon-to-be fixated visual features. Using a dynamic large-field noise paradigm, we indeed demonstrate that defining features of an eye movement target are enhanced in the pre-saccadic center of gaze. Enhancement manifested as higher Hit Rates for foveal probes with target-congruent orientation and a sensitization to incidental, target-like orientation information in foveally presented noise. Enhancement was spatially confined to the center of gaze and its immediate vicinity, even after parafoveal task performance had been raised to a foveal level. Moreover, foveal enhancement during saccade preparation was more pronounced and developed faster than enhancement during passive fixation. Based on these findings, we suggest a crucial contribution of foveal processing to trans-saccadic visual continuity: Foveal processing of saccade targets commences before the movement is executed and thereby enables a seamless transition once the center of gaze reaches the target.

Data availability

All data (psychophysical data, timing data, eye movement data, stimulus information) along with all experimental scripts are available on the Open Science Framework: https://osf.io/v9gsq/

The following data sets were generated

Article and author information

Author details

  1. Lisa M Kroell

    Department of Psychology, Humboldt-Universität zu Berlin, Berlin, Germany
    For correspondence
    lisa.maria.kroell@hu-berlin.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3508-5214
  2. Martin Rolfs

    Department of Psychology, Humboldt-Universität zu Berlin, Berlin, Germany
    For correspondence
    martin.rolfs@hu-berlin.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8214-8556

Funding

Deutsche Forschungsgemeinschaft (RO3579/8-1)

  • Martin Rolfs

Deutsche Forschungsgemeinschaft (RO3579/9-1)

  • Martin Rolfs

Deutsche Forschungsgemeinschaft (RO3579/12-1)

  • Martin Rolfs

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

Ethics

Human subjects: Participants gave written informed consent before the experiments. All studies complied with the Declaration of Helsinki in its latest version and were approved by the Ethics Committee of the Department of Psychology at Humboldt-Universität zu Berlin (reference number: 2018-09).

Reviewing Editor

  1. Krystel R Huxlin, University of Rochester, United States

Publication history

  1. Preprint posted: January 12, 2022 (view preprint)
  2. Received: February 23, 2022
  3. Accepted: September 3, 2022
  4. Accepted Manuscript published: September 9, 2022 (version 1)
  5. Accepted Manuscript updated: September 13, 2022 (version 2)
  6. Version of Record published: October 18, 2022 (version 3)

Copyright

© 2022, Kroell & Rolfs

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

  • 1,228
    Page views
  • 306
    Downloads
  • 1
    Citations

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

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. Lisa M Kroell
  2. Martin Rolfs
(2022)
Foveal vision anticipates defining features of eye movement targets
eLife 11:e78106.
https://doi.org/10.7554/eLife.78106

Further reading

    1. Neuroscience
    Yonatan Sanz Perl, Sol Fittipaldi ... Enzo Tagliazucchi
    Research Article

    The treatment of neurodegenerative diseases is hindered by lack of interventions capable of steering multimodal whole-brain dynamics towards patterns indicative of preserved brain health. To address this problem, we combined deep learning with a model capable of reproducing whole-brain functional connectivity in patients diagnosed with Alzheimer’s disease (AD) and behavioral variant frontotemporal dementia (bvFTD). These models included disease-specific atrophy maps as priors to modulate local parameters, revealing increased stability of hippocampal and insular dynamics as signatures of brain atrophy in AD and bvFTD, respectively. Using variational autoencoders, we visualized different pathologies and their severity as the evolution of trajectories in a low-dimensional latent space. Finally, we perturbed the model to reveal key AD- and bvFTD-specific regions to induce transitions from pathological to healthy brain states. Overall, we obtained novel insights on disease progression and control by means of external stimulation, while identifying dynamical mechanisms that underlie functional alterations in neurodegeneration.

    1. Neuroscience
    Andrea Alamia, Lucie Terral ... Rufin VanRullen
    Research Article Updated

    Previous research has associated alpha-band [8–12 Hz] oscillations with inhibitory functions: for instance, several studies showed that visual attention increases alpha-band power in the hemisphere ipsilateral to the attended location. However, other studies demonstrated that alpha oscillations positively correlate with visual perception, hinting at different processes underlying their dynamics. Here, using an approach based on traveling waves, we demonstrate that there are two functionally distinct alpha-band oscillations propagating in different directions. We analyzed EEG recordings from three datasets of human participants performing a covert visual attention task (one new dataset with N = 16, two previously published datasets with N = 16 and N = 31). Participants were instructed to detect a brief target by covertly attending to the screen’s left or right side. Our analysis reveals two distinct processes: allocating attention to one hemifield increases top-down alpha-band waves propagating from frontal to occipital regions ipsilateral to the attended location, both with and without visual stimulation. These top-down oscillatory waves correlate positively with alpha-band power in frontal and occipital regions. Yet, different alpha-band waves propagate from occipital to frontal regions and contralateral to the attended location. Crucially, these forward waves were present only during visual stimulation, suggesting a separate mechanism related to visual processing. Together, these results reveal two distinct processes reflected by different propagation directions, demonstrating the importance of considering oscillations as traveling waves when characterizing their functional role.