1. Neuroscience
Download icon

Behavioral training promotes multiple adaptive processes following acute hearing loss

  1. Peter Keating  Is a corresponding author
  2. Onayomi Rosenior-Patten
  3. Johannes C Dahmen
  4. Olivia Bell
  5. Andrew J King
  1. University of Oxford, United Kingdom
Short Report
  • Cited 15
  • Views 1,434
  • Annotations
Cite this article as: eLife 2016;5:e12264 doi: 10.7554/eLife.12264

Abstract

The brain possesses a remarkable capacity to compensate for changes in inputs resulting from a range of sensory impairments. Developmental studies of sound localization have shown that adaptation to asymmetric hearing loss can be achieved either by reinterpreting altered spatial cues or by relying more on those cues that remain intact. Adaptation to monaural deprivation in adulthood is also possible, but appears to lack such flexibility. Here we show, however, that appropriate behavioral training enables monaurally-deprived adult humans to exploit both of these adaptive processes. Moreover, cortical recordings in ferrets reared with asymmetric hearing loss suggest that these forms of plasticity have distinct neural substrates. An ability to adapt to asymmetric hearing loss using multiple adaptive processes is therefore shared by different species and may persist throughout the lifespan. This highlights the fundamental flexibility of neural systems, and may also point toward novel therapeutic strategies for treating sensory disorders.

Article and author information

Author details

  1. Peter Keating

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    For correspondence
    peter.keating@dpag.ox.ac.uk
    Competing interests
    No competing interests declared.
  2. Onayomi Rosenior-Patten

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  3. Johannes C Dahmen

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  4. Olivia Bell

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
  5. Andrew J King

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    Andrew J King, Reviewing editor, eLife.

Ethics

Animal experimentation: All procedures conformed to ethical standards approved by the Central University Research Ethics Committee (CUREC) at the University of Oxford. All work involving animals was performed under licenses granted by the UK Home Office under the Animals (Scientific Procedures) Act of 1986.

Human subjects: All procedures conformed to ethical standards approved by the Central University Research Ethics Committee (CUREC) at the University of Oxford. All human subjects provided informed written consent.

Reviewing Editor

  1. Thomas D Mrsic-Flogel, University of Basel, Switzerland

Publication history

  1. Received: October 12, 2015
  2. Accepted: March 23, 2016
  3. Accepted Manuscript published: March 23, 2016 (version 1)
  4. Version of Record published: April 20, 2016 (version 2)

Copyright

© 2016, Keating 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

  • 1,434
    Page views
  • 366
    Downloads
  • 15
    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)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Biochemistry and Chemical Biology
    2. Neuroscience
    Lloyd Davis et al.
    Tools and Resources Updated

    Synthetic strategies for optically controlling gene expression may enable the precise spatiotemporal control of genes in any combination of cells that cannot be targeted with specific promoters. We develop an improved genetic code expansion system in Caenorhabditis elegans and use it to create a photoactivatable Cre recombinase. We laser-activate Cre in single neurons within a bilaterally symmetric pair to selectively switch on expression of a loxP-controlled optogenetic channel in the targeted neuron. We use the system to dissect, in freely moving animals, the individual contributions of the mechanosensory neurons PLML/PLMR to the C. elegans touch response circuit, revealing distinct and synergistic roles for these neurons. We thus demonstrate how genetic code expansion and optical targeting can be combined to break the symmetry of neuron pairs and dissect behavioural outputs of individual neurons that cannot be genetically targeted.

    1. Neuroscience
    Mi-Seon Kong et al.
    Research Article

    Animals seeking survival needs must be able to assess different locations of threats in their habitat. However, the neural integration of spatial and risk information essential for guiding goal-directed behavior remains poorly understood. Thus, we investigated simultaneous activities of fear-responsive basal amygdala (BA) and place-responsive dorsal hippocampus (dHPC) neurons as rats left the safe nest to search for food in an exposed space and encountered a simulated 'predator'. In this realistic situation, BA cells increased their firing rates and dHPC place cells decreased their spatial stability near the threat. Importantly, only those dHPC cells synchronized with the predator-responsive BA cells remapped significantly as a function of escalating risk location. Moreover, optogenetic stimulation of BA neurons was sufficient to cause spatial avoidance behavior and disrupt place fields. These results suggest a dynamic interaction of BA's fear signalling cells and dHPC's spatial coding cells as animals traverse safe-danger areas of their environment.