skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Restoring auditory cortex plasticity in adult mice by restricting thalamic adenosine signaling

Abstract

Circuits in the auditory cortex are highly susceptible to acoustic influences during an early postnatal critical period. The auditory cortex selectively expands neural representations of enriched acoustic stimuli, a process important for human language acquisition. Adults lack this plasticity. We show in the murine auditory cortex that juvenile plasticity can be reestablished in adulthood if acoustic stimuli are paired with disruption of ecto-5'-nucleotidase–dependent adenosine production or A1–adenosine receptor signaling in the auditory thalamus. This plasticity occurs at the level of cortical maps and individual neurons in the auditory cortex of awake adult mice and is associated with long-term improvement of tone-discrimination abilities. We determined that, in adult mice, disrupting adenosine signaling in the thalamus rejuvenates plasticity in the auditory cortex and improves auditory perception.

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [1]
  1. St.Jude Children's Research Hospital, Memphis, TN (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Vanderbilt Univ., Nashville, TN (United States)
  4. St. Jude Children's Hospital, Memphis, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1376640
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Science
Additional Journal Information:
Journal Volume: 356; Journal Issue: 6345; Journal ID: ISSN 0036-8075
Publisher:
AAAS
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES

Citation Formats

Blundon, Jay A., Roy, Noah C., Teubner, Brett J. W., Yu, Jing, Eom, Tae-Yeon, Sample, K. Jake, Pani, Amar, Smeyne, Richard J., Han, Seung Baek, Kerekes, Ryan A., Rose, Derek C., Hackett, Troy A., Vuppala, Pradeep K., Freeman, Burgess B., and Zakharenko, Stanislav S. Restoring auditory cortex plasticity in adult mice by restricting thalamic adenosine signaling. United States: N. p., 2017. Web. doi:10.1126/science.aaf4612.
Blundon, Jay A., Roy, Noah C., Teubner, Brett J. W., Yu, Jing, Eom, Tae-Yeon, Sample, K. Jake, Pani, Amar, Smeyne, Richard J., Han, Seung Baek, Kerekes, Ryan A., Rose, Derek C., Hackett, Troy A., Vuppala, Pradeep K., Freeman, Burgess B., & Zakharenko, Stanislav S. Restoring auditory cortex plasticity in adult mice by restricting thalamic adenosine signaling. United States. doi:10.1126/science.aaf4612.
Blundon, Jay A., Roy, Noah C., Teubner, Brett J. W., Yu, Jing, Eom, Tae-Yeon, Sample, K. Jake, Pani, Amar, Smeyne, Richard J., Han, Seung Baek, Kerekes, Ryan A., Rose, Derek C., Hackett, Troy A., Vuppala, Pradeep K., Freeman, Burgess B., and Zakharenko, Stanislav S. Fri . "Restoring auditory cortex plasticity in adult mice by restricting thalamic adenosine signaling". United States. doi:10.1126/science.aaf4612. https://www.osti.gov/servlets/purl/1376640.
@article{osti_1376640,
title = {Restoring auditory cortex plasticity in adult mice by restricting thalamic adenosine signaling},
author = {Blundon, Jay A. and Roy, Noah C. and Teubner, Brett J. W. and Yu, Jing and Eom, Tae-Yeon and Sample, K. Jake and Pani, Amar and Smeyne, Richard J. and Han, Seung Baek and Kerekes, Ryan A. and Rose, Derek C. and Hackett, Troy A. and Vuppala, Pradeep K. and Freeman, Burgess B. and Zakharenko, Stanislav S.},
abstractNote = {Circuits in the auditory cortex are highly susceptible to acoustic influences during an early postnatal critical period. The auditory cortex selectively expands neural representations of enriched acoustic stimuli, a process important for human language acquisition. Adults lack this plasticity. We show in the murine auditory cortex that juvenile plasticity can be reestablished in adulthood if acoustic stimuli are paired with disruption of ecto-5'-nucleotidase–dependent adenosine production or A1–adenosine receptor signaling in the auditory thalamus. This plasticity occurs at the level of cortical maps and individual neurons in the auditory cortex of awake adult mice and is associated with long-term improvement of tone-discrimination abilities. We determined that, in adult mice, disrupting adenosine signaling in the thalamus rejuvenates plasticity in the auditory cortex and improves auditory perception.},
doi = {10.1126/science.aaf4612},
journal = {Science},
number = 6345,
volume = 356,
place = {United States},
year = {2017},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 5 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Adenosine A 1 receptors modulate anxiety in CD1 mice
journal, April 1998

  • Florio, C.; Prezioso, Anita; Papaioannou, Aristotele
  • Psychopharmacology, Vol. 136, Issue 4
  • DOI: 10.1007/s002130050572

Design, Synthesis and Biological Evaluation of a Novel Series of Potent, Orally Active Adenosine A<SUB>1</SUB> Receptor Antagonists with High Blood-Brain Barrier Permeability
journal, January 2001

  • Kuroda, Satoru; Takamura, Fujiko; Tenda, Yoshiyuki
  • CHEMICAL & PHARMACEUTICAL BULLETIN, Vol. 49, Issue 8
  • DOI: 10.1248/cpb.49.988

Feature-Dependent Sensitive Periods in the Development of Complex Sound Representation
journal, April 2009


Cortical remodelling induced by activity of ventral tegmental dopamine neurons
journal, July 2001

  • Bao, Shaowen; Chan, Vincent T.; Merzenich, Michael M.
  • Nature, Vol. 412, Issue 6842
  • DOI: 10.1038/35083586

Chronic treatment with DCPCX, an adenosine A1 antagonist, worsens long-term memory
journal, August 2013


Ultrasensitive fluorescent proteins for imaging neuronal activity
journal, July 2013

  • Chen, Tsai-Wen; Wardill, Trevor J.; Sun, Yi
  • Nature, Vol. 499, Issue 7458
  • DOI: 10.1038/nature12354

Induction of a physiological memory in the cerebral cortex by stimulation of the nucleus basalis.
journal, October 1996

  • Bakin, J. S.; Weinberger, N. M.
  • Proceedings of the National Academy of Sciences, Vol. 93, Issue 20
  • DOI: 10.1073/pnas.93.20.11219

Multiparametric Auditory Receptive Field Organization Across Five Cortical Fields in the Albino Rat
journal, May 2007

  • Polley, Daniel B.; Read, Heather L.; Storace, Douglas A.
  • Journal of Neurophysiology, Vol. 97, Issue 5
  • DOI: 10.1152/jn.01298.2006

Nonrigid registration using free-form deformations: application to breast MR images
journal, January 1999

  • Rueckert, D.; Sonoda, L. I.; Hayes, C.
  • IEEE Transactions on Medical Imaging, Vol. 18, Issue 8
  • DOI: 10.1109/42.796284

A synaptic memory trace for cortical receptive field plasticity
journal, November 2007

  • Froemke, Robert C.; Merzenich, Michael M.; Schreiner, Christoph E.
  • Nature, Vol. 450, Issue 7168
  • DOI: 10.1038/nature06289

Laminar Transformation of Frequency Organization in Auditory Cortex
journal, January 2013


Detection of adenosine receptor antagonists in rat brain using a modified radioreceptor assay
journal, December 1997


The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation
journal, December 1997

  • Stiebler, I.; Neulist, R.; Fichtel, I.
  • Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, Vol. 181, Issue 6
  • DOI: 10.1007/s003590050140

Developmental sensory experience balances cortical excitation and inhibition
journal, June 2010

  • Dorrn, Anja L.; Yuan, Kexin; Barker, Alison J.
  • Nature, Vol. 465, Issue 7300
  • DOI: 10.1038/nature09119

Presynaptic Gating of Postsynaptically Expressed Plasticity at Mature Thalamocortical Synapses
journal, November 2011


A critical period for long-term potentiation at thalamocortical synapses
journal, May 1995

  • Crair, Michael C.; Malenka, Robert C.
  • Nature, Vol. 375, Issue 6529
  • DOI: 10.1038/375325a0

Critical period plasticity in local cortical circuits
journal, November 2005

  • Hensch, Takao K.
  • Nature Reviews Neuroscience, Vol. 6, Issue 11
  • DOI: 10.1038/nrn1787

Latency and amplitude changes in the acoustic startle reflex of the rat produced by variation in auditory prestimulation☆
journal, June 1973


Presynaptic Gating of Postsynaptic Synaptic Plasticity: A Plasticity Filter in the Adult Auditory Cortex
journal, April 2013


CTEP: A Novel, Potent, Long-Acting, and Orally Bioavailable Metabotropic Glutamate Receptor 5 Inhibitor
journal, August 2011

  • Lindemann, Lothar; Jaeschke, Georg; Michalon, Aubin
  • Journal of Pharmacology and Experimental Therapeutics, Vol. 339, Issue 2
  • DOI: 10.1124/jpet.111.185660

Critical Period Window for Spectral Tuning Defined in the Primary Auditory Cortex (A1) in the Rat
journal, January 2007


A critical period for auditory thalamocortical connectivity
journal, July 2011

  • Barkat, Tania Rinaldi; Polley, Daniel B.; Hensch, Takao K.
  • Nature Neuroscience, Vol. 14, Issue 9
  • DOI: 10.1038/nn.2882

Gbx2 regulates thalamocortical axon guidance by modifying the LIM and Robo codes
journal, November 2012

  • Chatterjee, M.; Li, K.; Chen, L.
  • Development, Vol. 139, Issue 24
  • DOI: 10.1242/dev.086991

Increased auditory cortical representation in musicians
journal, April 1998

  • Pantev, Christo; Oostenveld, Robert; Engelien, Almut
  • Nature, Vol. 392, Issue 6678
  • DOI: 10.1038/33918

Persistent and specific influences of early acoustic environments on primary auditory cortex
journal, October 2001

  • Zhang, Li I.; Bao, Shaowen; Merzenich, Michael M.
  • Nature Neuroscience, Vol. 4, Issue 11
  • DOI: 10.1038/nn745

Low, but not high, dose caffeine is a readily available probe for adenosine actions
journal, June 2017


Cortical Map Reorganization Enabled by Nucleus Basalis Activity
journal, March 1998


Linking Topography to Tonotopy in the Mouse Auditory Thalamocortical Circuit
journal, February 2011


BIRDSONG AND HUMAN SPEECH: Common Themes and Mechanisms
journal, March 1999


An acoustic startle-based method of assessing frequency discrimination in mice
journal, August 2011


Neurochemical Measurement of Adenosine in Discrete Brain Regions of Five Strains of Inbred Mice
journal, March 2014


Environmental Noise Retards Auditory Cortical Development
journal, April 2003


Specific disruption of thalamic inputs to the auditory cortex in schizophrenia models
journal, June 2014


Auditory map plasticity: diversity in causes and consequences
journal, February 2014


Musical training and language-related brain electrical activity in children
journal, May 2006


The Role and Regulation of Adenosine in the Central Nervous System
journal, March 2001


Timbre-specific enhancement of auditory cortical representations in musicians
journal, January 2001


Sensory Experience Restructures Thalamocortical Axons during Adulthood
journal, May 2012


Safety and Efficacy of Vagus Nerve Stimulation Paired With Tones for the Treatment of Tinnitus: A Case Series: Vagus Nerve Stimulation Paired with Tones in Tinnitus
journal, November 2013

  • De Ridder, Dirk; Vanneste, Sven; Engineer, Navzer D.
  • Neuromodulation: Technology at the Neural Interface, Vol. 17, Issue 2
  • DOI: 10.1111/ner.12127

Crucial Role for Ecto-5′-Nucleotidase (CD73) in Vascular Leakage during Hypoxia
journal, December 2004

  • Thompson, Linda F.; Eltzschig, Holger K.; Ibla, Juan C.
  • The Journal of Experimental Medicine, Vol. 200, Issue 11
  • DOI: 10.1084/jem.20040915

Synaptic plasticity as a cortical coding scheme
journal, December 2015


Reversing pathological neural activity using targeted plasticity
journal, January 2011

  • Engineer, Navzer D.; Riley, Jonathan R.; Seale, Jonathan D.
  • Nature, Vol. 470, Issue 7332
  • DOI: 10.1038/nature09656

Neuronal Plasticity: Beyond the Critical Period
journal, November 2014


Pharmacological Characterization of FR194921, a New Potent, Selective, and Orally Active Antagonist for Central Adenosine A1 Receptors
journal, January 2004

  • Maemoto, Takuya; Tada, Miho; Mihara, Takuma
  • Journal of Pharmacological Sciences, Vol. 96, Issue 1
  • DOI: 10.1254/jphs.FP0040359

Tissue-Nonspecific Alkaline Phosphatase Acts Redundantly with PAP and NT5E to Generate Adenosine in the Dorsal Spinal Cord
journal, July 2013


Safety, Feasibility, and Efficacy of Vagus Nerve Stimulation Paired With Upper-Limb Rehabilitation After Ischemic Stroke
journal, January 2016


Developmental language learning impairments
journal, August 2002


Influence of Musical Expertise on Segmental and Tonal Processing in Mandarin Chinese
journal, October 2011

  • Marie, Céline; Delogu, Franco; Lampis, Giulia
  • Journal of Cognitive Neuroscience, Vol. 23, Issue 10
  • DOI: 10.1162/jocn.2010.21585

Cortical Map Plasticity Improves Learning but Is Not Necessary for Improved Performance
journal, April 2011


Thalamocortical Long-Term Potentiation Becomes Gated after the Early Critical Period in the Auditory Cortex
journal, April 2013


RNAscope
journal, January 2012


A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
journal, December 2009

  • Madisen, Linda; Zwingman, Theresa A.; Sunkin, Susan M.
  • Nature Neuroscience, Vol. 13, Issue 1
  • DOI: 10.1038/nn.2467

Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor
journal, July 2001

  • Johansson, B.; Halldner, L.; Dunwiddie, T. V.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 16
  • DOI: 10.1073/pnas.161292398

Penetration of adenosine antagonists into mouse brain as determined by ex vivo binding
journal, February 1992