1. Neuroscience

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
https://doi.org/10.7554/eLife.40014
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

Reviewing Editor

  1. Tatiana Pasternak, University of Rochester, United States

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)'.

Version 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

  • 2,408
    views
  • 374
    downloads
  • 65
    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. 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

Share this article

https://doi.org/10.7554/eLife.40014

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Short-term plasticity in the human visual thalamus

    Jan W Kurzawski, Claudia Lunghi ... Paola Binda
    Research Advance Updated

    While there is evidence that the visual cortex retains a potential for plasticity in adulthood, less is known about the subcortical stages of visual processing. Here, we asked whether short-term ocular dominance plasticity affects the human visual thalamus. We addressed this question in normally sighted adult humans, using ultra-high field (7T) magnetic resonance imaging combined with the paradigm of short-term monocular deprivation. With this approach, we previously demonstrated transient shifts of perceptual eye dominance and ocular dominance in visual cortex (Binda et al., 2018). Here, we report evidence for short-term plasticity in the ventral division of the pulvinar (vPulv), where the deprived eye representation was enhanced over the nondeprived eye. This vPulv plasticity was similar as previously seen in visual cortex and it was correlated with the ocular dominance shift measured behaviorally. In contrast, there was no effect of monocular deprivation in two adjacent thalamic regions: dorsal pulvinar and Lateral Geniculate Nucleus. We conclude that the visual thalamus retains potential for short-term plasticity in adulthood; the plasticity effect differs across thalamic subregions, possibly reflecting differences in their corticofugal connectivity.

    1. Developmental Biology
    2. Neuroscience

    A unique multi-synaptic mechanism involving acetylcholine and GABA regulates dopamine release in the nucleus accumbens through early adolescence in male rats

    Melody C Iacino, Taylor A Stowe ... Mark J Ferris
    Research Article Updated

    Adolescence is characterized by changes in reward-related behaviors, social behaviors, and decision-making. These behavioral changes are necessary for the transition into adulthood, but they also increase vulnerability to the development of a range of psychiatric disorders. Major reorganization of the dopamine system during adolescence is thought to underlie, in part, the associated behavioral changes and increased vulnerability. Here, we utilized fast scan cyclic voltammetry and microdialysis to examine differences in dopamine release as well as mechanisms that underlie differential dopamine signaling in the nucleus accumbens (NAc) core of adolescent (P28-35) and adult (P70-90) male rats. We show baseline differences between adult and adolescent-stimulated dopamine release in male rats, as well as opposite effects of the α6 nicotinic acetylcholine receptor (nAChR) on modulating dopamine release. The α6-selective blocker, α-conotoxin, increased dopamine release in early adolescent rats, but decreased dopamine release in rats beginning in middle adolescence and extending through adulthood. Strikingly, blockade of GABAA and GABAB receptors revealed that this α6-mediated increase in adolescent dopamine release requires NAc GABA signaling to occur. We confirm the role of α6 nAChRs and GABA in mediating this effect in vivo using microdialysis. Results herein suggest a multisynaptic mechanism potentially unique to the period of development that includes early adolescence, involving acetylcholine acting at α6-containing nAChRs to drive inhibitory GABA tone on dopamine release.

    1. Neuroscience

    The scheduling of adolescence with Netrin-1 and UNC5C

    Daniel Hoops, Robert Kyne ... Cecilia Flores
    Short Report

    Dopamine axons are the only axons known to grow during adolescence. Here, using rodent models, we examined how two proteins, Netrin-1 and its receptor, UNC5C, guide dopamine axons toward the prefrontal cortex and shape behaviour. We demonstrate in mice (Mus musculus) that dopamine axons reach the cortex through a transient gradient of Netrin-1-expressing cells – disrupting this gradient reroutes axons away from their target. Using a seasonal model (Siberian hamsters; Phodopus sungorus) we find that mesocortical dopamine development can be regulated by a natural environmental cue (daylength) in a sexually dimorphic manner – delayed in males, but advanced in females. The timings of dopamine axon growth and UNC5C expression are always phase-locked. Adolescence is an ill-defined, transitional period; we pinpoint neurodevelopmental markers underlying this period.