Stimulus relevance modulates contrast adaptation in visual cortex

  1. Andreas J Keller  Is a corresponding author
  2. Rachael Houlton
  3. Björn M Kampa
  4. Nicholas A Lesica
  5. Thomas D Mrsic-Flogel
  6. Georg B Keller
  7. Fritjof Helmchen
  1. University of Zurich and ETH Zurich, Switzerland
  2. University College London, United Kingdom
  3. University of Zurich, Switzerland
  4. Friedrich Miescher Institute for Biomedical Research, Switzerland

Abstract

A general principle of sensory processing is that neurons adapt to sustained stimuli by reducing their response over time. Most of our knowledge on adaptation in single cells is based on experiments in anesthetized animals. How responses adapt in awake animals, when stimuli may be behaviorally relevant or not, remains unclear. Here we show that contrast adaptation in mouse primary visual cortex depends on the behavioral relevance of the stimulus. Cells that adapted to contrast under anesthesia maintained or even increased their activity in awake naïve mice. When engaged in a visually guided task, contrast adaptation re-occurred for stimuli that were irrelevant for solving the task. However, contrast adaptation was reversed when stimuli acquired behavioral relevance. Regulation of cortical adaptation by task demand may allow dynamic control of sensory-evoked signal flow in the neocortex.

Article and author information

Author details

  1. Andreas J Keller

    Institute of Neuroinformatics, University of Zurich and ETH Zurich, Zurich, Switzerland
    For correspondence
    andi@ini.ethz.ch
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7997-6118
  2. Rachael Houlton

    Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  3. Björn M Kampa

    Brain Research Institute, University of Zurich, Zurich, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4343-2634
  4. Nicholas A Lesica

    Ear Institute, University College London, London, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5238-4462
  5. Thomas D Mrsic-Flogel

    Department of Neuroscience, Physiology and Pharmacology, University College London, London, United Kingdom
    Competing interests
    Thomas D Mrsic-Flogel, Reviewing editor, eLife.
  6. Georg B Keller

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1401-0117
  7. Fritjof Helmchen

    Brain Research Institute, University of Zurich, Zurich, Switzerland
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8867-9569

Funding

FP7 EU (Grant 269921)

  • Björn M Kampa
  • Fritjof Helmchen

Novartis Research Foundation

  • Georg B Keller

European Research Council (Grant 616509)

  • Thomas D Mrsic-Flogel

Wellcome Trust (Grant 095074)

  • Thomas D Mrsic-Flogel

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

Ethics

Animal experimentation: All experiments and surgical procedures were carried out in accordance with the UK Animal (Scientific Procedures) Act under project license 70/7573, approved by the Cantonal Veterinary Office of Zurich, Switzerland, under license number 62/2011, or by the Cantonal Veterinary Office of Basel-Stadt, Switzerland, under license number 2537.

Reviewing Editor

  1. David Kleinfeld, University of California, San Diego, United States

Publication history

  1. Received: September 16, 2016
  2. Accepted: January 27, 2017
  3. Accepted Manuscript published: January 28, 2017 (version 1)
  4. Version of Record published: February 8, 2017 (version 2)

Copyright

© 2017, Keller 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.

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  1. Andreas J Keller
  2. Rachael Houlton
  3. Björn M Kampa
  4. Nicholas A Lesica
  5. Thomas D Mrsic-Flogel
  6. Georg B Keller
  7. Fritjof Helmchen
(2017)
Stimulus relevance modulates contrast adaptation in visual cortex
eLife 6:e21589.
https://doi.org/10.7554/eLife.21589
  1. Further reading

Further reading

    1. Developmental Biology
    2. Neuroscience
    Matthew P Bostock, Anadika R Prasad ... Vilaiwan M Fernandes
    Research Article Updated

    Defining the origin of neuronal diversity is a major challenge in developmental neurobiology. The Drosophila visual system is an excellent paradigm to study how cellular diversity is generated. Photoreceptors from the eye disc grow their axons into the optic lobe and secrete Hedgehog (Hh) to induce the lamina, such that for every unit eye there is a corresponding lamina unit made up of post-mitotic precursors stacked into columns. Each differentiated column contains five lamina neuron types (L1-L5), making it the simplest neuropil in the optic lobe, yet how this diversity is generated was unknown. Here, we found that Hh pathway activity is graded along the distal-proximal axis of lamina columns, and further determined that this gradient in pathway activity arises from a gradient of Hh ligand. We manipulated Hh pathway activity cell autonomously in lamina precursors and non-cell autonomously by inactivating the Hh ligand and by knocking it down in photoreceptors. These manipulations showed that different thresholds of activity specify unique cell identities, with more proximal cell types specified in response to progressively lower Hh levels. Thus, our data establish that Hh acts as a morphogen to pattern the lamina. Although this is the first such report during Drosophila nervous system development, our work uncovers a remarkable similarity with the vertebrate neural tube, which is patterned by Sonic Hh. Altogether, we show that differentiating neurons can regulate the neuronal diversity of their distant target fields through morphogen gradients.

    1. Developmental Biology
    2. Neuroscience
    Anadika R Prasad, Inês Lago-Baldaia ... Vilaiwan M Fernandes
    Research Article Updated

    Neural circuit formation and function require that diverse neurons are specified in appropriate numbers. Known strategies for controlling neuronal numbers involve regulating either cell proliferation or survival. We used the Drosophila visual system to probe how neuronal numbers are set. Photoreceptors from the eye-disc induce their target field, the lamina, such that for every unit eye there is a corresponding lamina unit (column). Although each column initially contains ~6 post-mitotic lamina precursors, only 5 differentiate into neurons, called L1-L5; the ‘extra’ precursor, which is invariantly positioned above the L5 neuron in each column, undergoes apoptosis. Here, we showed that a glial population called the outer chiasm giant glia (xgO), which resides below the lamina, secretes multiple ligands to induce L5 differentiation in response to epidermal growth factor (EGF) from photoreceptors. By forcing neuronal differentiation in the lamina, we uncovered that though fated to die, the ‘extra’ precursor is specified as an L5. Therefore, two precursors are specified as L5s but only one differentiates during normal development. We found that the row of precursors nearest to xgO differentiate into L5s and, in turn, antagonise differentiation signalling to prevent the ‘extra’ precursors from differentiating, resulting in their death. Thus, an intricate interplay of glial signals and feedback from differentiating neurons defines an invariant and stereotyped pattern of neuronal differentiation and programmed cell death to ensure that lamina columns each contain exactly one L5 neuron.