Sensory experience during early sensitive periods shapes cross-modal temporal biases

  1. Stephanie Badde  Is a corresponding author
  2. Pia Ley
  3. Siddhart S Rajendran
  4. Idris Shareef
  5. Ramesh Kekunnaya
  6. Brigitte Röder
  1. New York University, United States
  2. University of Hamburg, Germany
  3. LV Prasad Eye Institute, India

Abstract

Typical human perception features stable biases such as perceiving visual events as later than synchronous auditory events. The origin of such perceptual biases is unknown. To investigate the role of early sensory experience, we tested whether a congenital, transient loss of pattern vision, caused by bilateral dense cataracts, has sustained effects on audio-visual and tactile-visual temporal biases and resolution. Participants judged the temporal order of successively presented, spatially separated events within and across modalities. Individuals with reversed congenital cataracts showed a bias towards perceiving visual stimuli as occurring earlier than auditory (Expt. 1) and tactile (Expt. 2) stimuli. This finding stood in stark contrast to normally sighted controls and sight-recovery individuals who had developed cataracts later in childhood: both groups exhibited the typical bias of perceiving vision as delayed compared to audition. These findings provide strong evidence that cross-modal temporal biases depend on sensory experience during an early sensitive period.

Data availability

All data have been deposited on Open Science Framework under CQN48.

The following data sets were generated

Article and author information

Author details

  1. Stephanie Badde

    Department of Psychology, New York University, New York, United States
    For correspondence
    stephanie.badde@nyu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4005-5503
  2. Pia Ley

    Department of Psychology, University of Hamburg, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Siddhart S Rajendran

    Department of Psychology, University of Hamburg, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Idris Shareef

    Child Sight Institute, Jasti V Ramanamma Children's Eye Care Center, LV Prasad Eye Institute, Hyderabad, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9258-2199
  5. Ramesh Kekunnaya

    Child Sight Institute, Jasti V Ramanamma Children's Eye Care Center, LV Prasad Eye Institute, Hyderabad, India
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5789-2300
  6. Brigitte Röder

    Biological Psychology and Neuropsychology, University of Hamburg, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

Deutsche Forschungsgemeinschaft (BA 5600/1-1)

  • Stephanie Badde

H2020 European Research Council (ERC-2009-AdG 249425 CriticalBrainChanges)

  • Brigitte Röder

Deutsche Forschungsgemeinschaft (DFG Ro 2625/10-1)

  • Brigitte Röder

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 or, if applicable, their legal guardian, provided written informed consent before beginning the experiment. The study was conducted in accordance with the ethical guidelines of the Declaration of Helsinki and was approved by the ethical board of the German Psychological Society as well as the local ethical committee of the LV Prasad Eye Institute.

Copyright

© 2020, Badde 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

  • 1,653
    views
  • 242
    downloads
  • 19
    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. Stephanie Badde
  2. Pia Ley
  3. Siddhart S Rajendran
  4. Idris Shareef
  5. Ramesh Kekunnaya
  6. Brigitte Röder
(2020)
Sensory experience during early sensitive periods shapes cross-modal temporal biases
eLife 9:e61238.
https://doi.org/10.7554/eLife.61238

Share this article

https://doi.org/10.7554/eLife.61238

Further reading

    1. Neuroscience
    Cristina Gil Avila, Elisabeth S May ... Markus Ploner
    Research Article

    Chronic pain is a prevalent and debilitating condition whose neural mechanisms are incompletely understood. An imbalance of cerebral excitation and inhibition (E/I), particularly in the medial prefrontal cortex (mPFC), is believed to represent a crucial mechanism in the development and maintenance of chronic pain. Thus, identifying a non-invasive, scalable marker of E/I could provide valuable insights into the neural mechanisms of chronic pain and aid in developing clinically useful biomarkers. Recently, the aperiodic component of the electroencephalography (EEG) power spectrum has been proposed to represent a non-invasive proxy for E/I. We, therefore, assessed the aperiodic component in the mPFC of resting-state EEG recordings in 149 people with chronic pain and 115 healthy participants. We found robust evidence against differences in the aperiodic component in the mPFC between people with chronic pain and healthy participants, and no correlation between the aperiodic component and pain intensity. These findings were consistent across different subtypes of chronic pain and were similarly found in a whole-brain analysis. Their robustness was supported by preregistration and multiverse analyses across many different methodological choices. Together, our results suggest that the EEG aperiodic component does not differentiate between people with chronic pain and healthy individuals. These findings and the rigorous methodological approach can guide future studies investigating non-invasive, scalable markers of cerebral dysfunction in people with chronic pain and beyond.

    1. Neuroscience
    Raven Star Wallace, Bronte Mckeown ... Jonathan Smallwood
    Research Article

    Movie-watching is a central aspect of our lives and an important paradigm for understanding the brain mechanisms behind cognition as it occurs in daily life. Contemporary views of ongoing thought argue that the ability to make sense of events in the ‘here and now’ depend on the neural processing of incoming sensory information by auditory and visual cortex, which are kept in check by systems in association cortex. However, we currently lack an understanding of how patterns of ongoing thoughts map onto the different brain systems when we watch a film, partly because methods of sampling experience disrupt the dynamics of brain activity and the experience of movie-watching. Our study established a novel method for mapping thought patterns onto the brain activity that occurs at different moments of a film, which does not disrupt the time course of brain activity or the movie-watching experience. We found moments when experience sampling highlighted engagement with multi-sensory features of the film or highlighted thoughts with episodic features, regions of sensory cortex were more active and subsequent memory for events in the movie was better—on the other hand, periods of intrusive distraction emerged when activity in regions of association cortex within the frontoparietal system was reduced. These results highlight the critical role sensory systems play in the multi-modal experience of movie-watching and provide evidence for the role of association cortex in reducing distraction when we watch films.