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Articles, Development/Plasticity/Repair

BDNF-Dependent Plasticity Induced by Peripheral Inflammation in the Primary Sensory and the Cingulate Cortex Triggers Cold Allodynia and Reveals a Major Role for Endogenous BDNF As a Tuner of the Affective Aspect of Pain

Karine Thibault, Wee Khang Lin, Armelle Rancillac, Marie Fan, Thibaut Snollaerts, Vallier Sordoillet, Michel Hamon, George M. Smith, Zsolt Lenkei and Sophie Pezet
Journal of Neuroscience 29 October 2014, 34 (44) 14739-14751; https://doi.org/10.1523/JNEUROSCI.0860-14.2014
Karine Thibault
1Brain Plasticity Unit, ESPCI-ParisTech, 75005 Paris, France,
2Centre National de la Recherche Scientifique, UMR 8249, 75794 Paris cedex 16, France,
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Wee Khang Lin
3Department of Pharmacology, University of Oxford, Oxford OX1 3QT, United Kingdom,
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Armelle Rancillac
1Brain Plasticity Unit, ESPCI-ParisTech, 75005 Paris, France,
2Centre National de la Recherche Scientifique, UMR 8249, 75794 Paris cedex 16, France,
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Marie Fan
1Brain Plasticity Unit, ESPCI-ParisTech, 75005 Paris, France,
2Centre National de la Recherche Scientifique, UMR 8249, 75794 Paris cedex 16, France,
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Thibaut Snollaerts
4Organisation Nucléaire et Oncogenèse, INSERM U993, Département de Biologie Cellulaire et Infection, Institut Pasteur, 75015 Paris, France,
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Vallier Sordoillet
1Brain Plasticity Unit, ESPCI-ParisTech, 75005 Paris, France,
2Centre National de la Recherche Scientifique, UMR 8249, 75794 Paris cedex 16, France,
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Michel Hamon
5UMR894 INSERM-CPN-UPMC, Faculté de Médecine Pierre et Marie Curie, Site Pitié-Salpêtrière, 75634 Paris cedex 13, France, and
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George M. Smith
6Shriners Hospitals Pediatric Research Center, Temple University, School of Medicine, Philadelphia, Pennsylvania 19140-5104
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Zsolt Lenkei
1Brain Plasticity Unit, ESPCI-ParisTech, 75005 Paris, France,
2Centre National de la Recherche Scientifique, UMR 8249, 75794 Paris cedex 16, France,
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Sophie Pezet
1Brain Plasticity Unit, ESPCI-ParisTech, 75005 Paris, France,
2Centre National de la Recherche Scientifique, UMR 8249, 75794 Paris cedex 16, France,
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Abstract

Painful experiences are multilayered, composed of sensory, affective, cognitive and behavioral facets. Whereas it is well accepted that the development of chronic pain is due to maladaptive neuronal changes, the underlying molecular mechanisms, their relationship to the different pain modalities, and indeed the localization of these changes are still unknown. Brain-derived neurotrophic factor (BDNF) is an activity-dependent neuromodulator in the adult brain, which enhances neuronal excitability. In the spinal cord, BDNF underlies the development and maintenance of inflammatory and neuropathic pain. Here, we hypothesized that BDNF could be a trigger of some of these plastic changes. Our results demonstrate that BDNF is upregulated in the anterior cingulate cortex (ACC) and the primary sensory cortex (S1) in rats with inflammatory pain. Injections of recombinant BDNF (into the ACC) or a viral vector synthesizing BDNF (into the ACC or S1) triggered both neuronal hyperexcitability, as shown by elevated long-term potentiation, and sustained pain hypersensitivity. Finally, pharmacological blockade of BDNF-tropomyosin receptor kinase B (TrkB) signaling in the ACC, through local injection of cyclotraxin-B (a novel, highly potent, and selective TrkB antagonist) prevented neuronal hyperexcitability, the emergence of cold hypersensitivity, and passive avoidance behavior. These findings show that BDNF-dependent neuronal plasticity in the ACC, a structure known to be involved in the affective-emotional aspect of pain, is a key mechanism in the development and maintenance of the emotional aspect of chronic pain.

  • hyperexcitability
  • neurotrophic factor
  • pain
  • viral vector
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The Journal of Neuroscience: 34 (44)
Journal of Neuroscience
Vol. 34, Issue 44
29 Oct 2014
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BDNF-Dependent Plasticity Induced by Peripheral Inflammation in the Primary Sensory and the Cingulate Cortex Triggers Cold Allodynia and Reveals a Major Role for Endogenous BDNF As a Tuner of the Affective Aspect of Pain
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BDNF-Dependent Plasticity Induced by Peripheral Inflammation in the Primary Sensory and the Cingulate Cortex Triggers Cold Allodynia and Reveals a Major Role for Endogenous BDNF As a Tuner of the Affective Aspect of Pain
Karine Thibault, Wee Khang Lin, Armelle Rancillac, Marie Fan, Thibaut Snollaerts, Vallier Sordoillet, Michel Hamon, George M. Smith, Zsolt Lenkei, Sophie Pezet
Journal of Neuroscience 29 October 2014, 34 (44) 14739-14751; DOI: 10.1523/JNEUROSCI.0860-14.2014

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BDNF-Dependent Plasticity Induced by Peripheral Inflammation in the Primary Sensory and the Cingulate Cortex Triggers Cold Allodynia and Reveals a Major Role for Endogenous BDNF As a Tuner of the Affective Aspect of Pain
Karine Thibault, Wee Khang Lin, Armelle Rancillac, Marie Fan, Thibaut Snollaerts, Vallier Sordoillet, Michel Hamon, George M. Smith, Zsolt Lenkei, Sophie Pezet
Journal of Neuroscience 29 October 2014, 34 (44) 14739-14751; DOI: 10.1523/JNEUROSCI.0860-14.2014
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Keywords

  • hyperexcitability
  • neurotrophic factor
  • pain
  • viral vector

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