Response to short-term deprivation of the human adult visual cortex measured with 7T BOLD

  1. Paola Binda
  2. Jan W Kurzawski
  3. Claudia Lunghi
  4. Laura Biagi
  5. Michela Tosetti
  6. Maria Concetta Morrone  Is a corresponding author
  1. University of Pisa, Italy
  2. IRCCS Stella Maris, Italy

Abstract

Sensory deprivation during the post-natal 'critical period' leads to structural reorganization of the developing visual cortex. In adulthood, the visual cortex retains some flexibility and adapts to sensory deprivation. Here we show that short-term (2h) monocular deprivation in adult humans boosts the BOLD response to the deprived eye, changing ocular dominance of V1 vertices, consistent with homeostatic plasticity. The boost is strongest in V1, present in V2, V3 and V4 but absent in V3a and hMT+. Assessment of spatial frequency tuning in V1 by a population Receptive-Field technique shows that deprivation primarily boosts high spatial frequencies, consistent with a primary involvement of the parvocellular pathway. Crucially, the V1 deprivation effect correlates across participants with the perceptual increase of the deprived eye dominance assessed with binocular rivalry, suggesting a common origin. Our results demonstrate that visual cortex, particularly the ventral pathway, retains a high potential for homeostatic plasticity in the human adult.

Data availability

BOLD responses and pRF fits as shown in all figures (main and supplementary) have been deposited on Dryad, through a link provided with the current submission (doi:10.5061/dryad.tp24j18). Custom Matlab code, used for pRF fitting, is included as Source code file 1.

The following data sets were generated

Article and author information

Author details

  1. Paola Binda

    Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  2. Jan W Kurzawski

    IRCCS Stella Maris, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2781-1236
  3. Claudia Lunghi

    Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  4. Laura Biagi

    IRCCS Stella Maris, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  5. Michela Tosetti

    IRCCS Stella Maris, Pisa, Italy
    Competing interests
    The authors declare that no competing interests exist.
  6. Maria Concetta Morrone

    Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy
    For correspondence
    concetta@in.cnr.it
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1025-0316

Funding

European Research Council (ERC ECSPLAIN 338866)

  • Paola Binda
  • Jan W Kurzawski
  • Maria Concetta Morrone

Ministero dell'Istruzione, dell'Università e della Ricerca (PRIN2015)

  • Claudia Lunghi
  • Maria Concetta Morrone

European Research Council (ERA-NET Neuro-DREAM)

  • Claudia Lunghi
  • Maria Concetta Morrone

European Union Horizon 2020 Research and Innovation Programme (NextGenVis 641805)

  • Jan W Kurzawski

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

Ethics

Human subjects: Experimental procedures are in line with the declaration of Helsinki and were approved by the regional ethics committee [Comitato Etico Pediatrico Regionale-Azienda Ospedaliero-Universitaria Meyer-Firenze (FI)] and by the Italian Ministry of Health, under the protocol 'Plasticità e multimodalità delle prime aree visive: studio in risonanza magnetica a campo ultra alto (7T)'.

Reviewing Editor

  1. Tatiana Pasternak, University of Rochester, United States

Publication history

  1. Received: July 11, 2018
  2. Accepted: November 26, 2018
  3. Accepted Manuscript published: November 26, 2018 (version 1)
  4. Version of Record published: December 18, 2018 (version 2)

Copyright

© 2018, Binda 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

  • 1,945
    Page views
  • 314
    Downloads
  • 37
    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. Paola Binda
  2. Jan W Kurzawski
  3. Claudia Lunghi
  4. Laura Biagi
  5. Michela Tosetti
  6. Maria Concetta Morrone
(2018)
Response to short-term deprivation of the human adult visual cortex measured with 7T BOLD
eLife 7:e40014.
https://doi.org/10.7554/eLife.40014
  1. Further reading

Further reading

    1. Neuroscience
    Carlotta Pribbenow, Yi-chun Chen ... David Owald
    Research Article Updated

    In vertebrates, several forms of memory-relevant synaptic plasticity involve postsynaptic rearrangements of glutamate receptors. In contrast, previous work indicates that Drosophila and other invertebrates store memories using presynaptic plasticity of cholinergic synapses. Here, we provide evidence for postsynaptic plasticity at cholinergic output synapses from the Drosophila mushroom bodies (MBs). We find that the nicotinic acetylcholine receptor (nAChR) subunit α5 is required within specific MB output neurons for appetitive memory induction but is dispensable for aversive memories. In addition, nAChR α2 subunits mediate memory expression and likely function downstream of α5 and the postsynaptic scaffold protein discs large (Dlg). We show that postsynaptic plasticity traces can be induced independently of the presynapse, and that in vivo dynamics of α2 nAChR subunits are changed both in the context of associative and non-associative (familiarity) memory formation, underlying different plasticity rules. Therefore, regardless of neurotransmitter identity, key principles of postsynaptic plasticity support memory storage across phyla.

    1. Neuroscience
    Frédéric Roux, George Parish ... Simon Hanslmayr
    Research Article Updated

    Theta and gamma oscillations in the medial temporal lobe are suggested to play a critical role for human memory formation via establishing synchrony in neural assemblies. Arguably, such synchrony facilitates efficient information transfer between neurons and enhances synaptic plasticity, both of which benefit episodic memory formation. However, to date little evidence exists from humans that would provide direct evidence for such a specific role of theta and gamma oscillations for episodic memory formation. Here, we investigate how oscillations shape the temporal structure of neural firing during memory formation in the medial temporal lobe. We measured neural firing and local field potentials in human epilepsy patients via micro-wire electrode recordings to analyze whether brain oscillations are related to co-incidences of firing between neurons during successful and unsuccessful encoding of episodic memories. The results show that phase-coupling of neurons to faster theta and gamma oscillations correlates with co-firing at short latencies (~20–30 ms) and occurs during successful memory formation. Phase-coupling at slower oscillations in these same frequency bands, in contrast, correlates with longer co-firing latencies and occurs during memory failure. Thus, our findings suggest that neural oscillations play a role for the synchronization of neural firing in the medial temporal lobe during the encoding of episodic memories.