Fast-conducting mechanoreceptors contribute to withdrawal behavior in normal and nerve injured rats
Fast-conducting peripheral high-threshold mechanoreceptors contribute to normal and nerve-injury-related withdrawal behavior. Fast-conducting myelinated high-threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles in normal withdr...
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| Published in | Pain (Amsterdam) Vol. 155; no. 12; pp. 2646 - 2655 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Philadelphia, PA
Elsevier B.V
01.12.2014
International Association for the Study of Pain Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Fast-conducting peripheral high-threshold mechanoreceptors contribute to normal and nerve-injury-related withdrawal behavior.
Fast-conducting myelinated high-threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles in normal withdrawal and in nerve injury–induced hyperalgesia are less well accepted. Modulation of this subpopulation of peripheral neurons would help define their roles in withdrawal behaviors. The optically active proton pump, ArchT, was placed in an adeno-associated virus-type 8 viral vector with the CAG promoter and was administered by intrathecal injection resulting in expression in myelinated neurons. Optical inhibition of peripheral neurons at the soma and transcutaneously was possible in the neurons expressing ArchT, but not in neurons from control animals. Receptive field characteristics and electrophysiology determined that inhibition was neuronal subtype–specific with only AHTMR neurons being inhibited. One week after nerve injury the AHTMR are hyperexcitable, but can still be inhibited at the soma and transcutaneously. Withdrawal thresholds to mechanical stimuli in normal and in hyperalgesic nerve-injured animals also were increased by transcutaneous light to the affected hindpaw. This suggests that AHTMR neurons play a role not only in threshold-related withdrawal behavior in the normal animal, but also in sensitized states after nerve injury. This is the first time this subpopulation of neurons has been reversibly modulated to test their contribution to withdrawal-related behaviors before and after nerve injury. This technique may prove useful to define the role of selective neuronal populations in different pain states. |
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| AbstractList | Fast-conducting peripheral high-threshold mechanoreceptors contribute to normal and nerve-injury-related withdrawal behavior. Fast-conducting myelinated high-threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles in normal withdrawal and in nerve injury–induced hyperalgesia are less well accepted. Modulation of this subpopulation of peripheral neurons would help define their roles in withdrawal behaviors. The optically active proton pump, ArchT, was placed in an adeno-associated virus-type 8 viral vector with the CAG promoter and was administered by intrathecal injection resulting in expression in myelinated neurons. Optical inhibition of peripheral neurons at the soma and transcutaneously was possible in the neurons expressing ArchT, but not in neurons from control animals. Receptive field characteristics and electrophysiology determined that inhibition was neuronal subtype–specific with only AHTMR neurons being inhibited. One week after nerve injury the AHTMR are hyperexcitable, but can still be inhibited at the soma and transcutaneously. Withdrawal thresholds to mechanical stimuli in normal and in hyperalgesic nerve-injured animals also were increased by transcutaneous light to the affected hindpaw. This suggests that AHTMR neurons play a role not only in threshold-related withdrawal behavior in the normal animal, but also in sensitized states after nerve injury. This is the first time this subpopulation of neurons has been reversibly modulated to test their contribution to withdrawal-related behaviors before and after nerve injury. This technique may prove useful to define the role of selective neuronal populations in different pain states. Fast-conducting myelinated high-threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles in normal withdrawal and in nerve injury-induced hyperalgesia are less well accepted. Modulation of this subpopulation of peripheral neurons would help define their roles in withdrawal behaviors. The optically active proton pump, ArchT, was placed in an adeno-associated virus-type 8 viral vector with the CAG promoter and was administered by intrathecal injection resulting in expression in myelinated neurons. Optical inhibition of peripheral neurons at the soma and transcutaneously was possible in the neurons expressing ArchT, but not in neurons from control animals. Receptive field characteristics and electrophysiology determined that inhibition was neuronal subtype-specific with only AHTMR neurons being inhibited. One week after nerve injury the AHTMR are hyperexcitable, but can still be inhibited at the soma and transcutaneously. Withdrawal thresholds to mechanical stimuli in normal and in hyperalgesic nerve-injured animals also were increased by transcutaneous light to the affected hindpaw. This suggests that AHTMR neurons play a role not only in threshold-related withdrawal behavior in the normal animal, but also in sensitized states after nerve injury. This is the first time this subpopulation of neurons has been reversibly modulated to test their contribution to withdrawal-related behaviors before and after nerve injury. This technique may prove useful to define the role of selective neuronal populations in different pain states.Fast-conducting myelinated high-threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles in normal withdrawal and in nerve injury-induced hyperalgesia are less well accepted. Modulation of this subpopulation of peripheral neurons would help define their roles in withdrawal behaviors. The optically active proton pump, ArchT, was placed in an adeno-associated virus-type 8 viral vector with the CAG promoter and was administered by intrathecal injection resulting in expression in myelinated neurons. Optical inhibition of peripheral neurons at the soma and transcutaneously was possible in the neurons expressing ArchT, but not in neurons from control animals. Receptive field characteristics and electrophysiology determined that inhibition was neuronal subtype-specific with only AHTMR neurons being inhibited. One week after nerve injury the AHTMR are hyperexcitable, but can still be inhibited at the soma and transcutaneously. Withdrawal thresholds to mechanical stimuli in normal and in hyperalgesic nerve-injured animals also were increased by transcutaneous light to the affected hindpaw. This suggests that AHTMR neurons play a role not only in threshold-related withdrawal behavior in the normal animal, but also in sensitized states after nerve injury. This is the first time this subpopulation of neurons has been reversibly modulated to test their contribution to withdrawal-related behaviors before and after nerve injury. This technique may prove useful to define the role of selective neuronal populations in different pain states. Fast conducting myelinated high threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles in normal withdrawal and in nerve injury induced hyperalgesia are less well accepted. Modulation of this subpopulation of peripheral neurons would help define their roles in withdrawal behaviors. The optically active proton pump, ArchT, was placed in an AAV8 viral vector with the CAG promoter and was administered by intrathecal injection resulting in expression in myelinated neurons. Optical inhibition of peripheral neurons at the soma and transcutaneously was possible in the neurons expressing ArchT, but not in neurons from control animals. Receptive field characteristics and electrophysiology determined that inhibition was neuronal subtype specific with only AHTMR neurons being inhibited. One week following nerve injury the AHTMR are hyperexcitable, but can still be inhibited at the soma and transcutaneously. Withdrawal thresholds to mechanical stimuli in normal and in hyperalgesic nerve injured animals were also increased by transcutaneous light to the affected hindpaw. This suggests that AHTMR neurons play a role not only in threshold related withdrawal behavior in the normal animal, but also in sensitized states after nerve injury. This is the first time this subpopulation of neurons has been reversibly modulated to test their contribution to withdrawal related behaviors before and after nerve injury. This technique may prove useful to define the role of selective neuronal populations in different pain states. Fast-conducting peripheral high-threshold mechanoreceptors contribute to normal and nerve-injury-related withdrawal behavior. Fast-conducting myelinated high-threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles in normal withdrawal and in nerve injury–induced hyperalgesia are less well accepted. Modulation of this subpopulation of peripheral neurons would help define their roles in withdrawal behaviors. The optically active proton pump, ArchT, was placed in an adeno-associated virus-type 8 viral vector with the CAG promoter and was administered by intrathecal injection resulting in expression in myelinated neurons. Optical inhibition of peripheral neurons at the soma and transcutaneously was possible in the neurons expressing ArchT, but not in neurons from control animals. Receptive field characteristics and electrophysiology determined that inhibition was neuronal subtype–specific with only AHTMR neurons being inhibited. One week after nerve injury the AHTMR are hyperexcitable, but can still be inhibited at the soma and transcutaneously. Withdrawal thresholds to mechanical stimuli in normal and in hyperalgesic nerve-injured animals also were increased by transcutaneous light to the affected hindpaw. This suggests that AHTMR neurons play a role not only in threshold-related withdrawal behavior in the normal animal, but also in sensitized states after nerve injury. This is the first time this subpopulation of neurons has been reversibly modulated to test their contribution to withdrawal-related behaviors before and after nerve injury. This technique may prove useful to define the role of selective neuronal populations in different pain states. Fast-conducting myelinated high-threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles in normal withdrawal and in nerve injury-induced hyperalgesia are less well accepted. Modulation of this subpopulation of peripheral neurons would help define their roles in withdrawal behaviors. The optically active proton pump, ArchT, was placed in an adeno-associated virus-type 8 viral vector with the CAG promoter and was administered by intrathecal injection resulting in expression in myelinated neurons. Optical inhibition of peripheral neurons at the soma and transcutaneously was possible in the neurons expressing ArchT, but not in neurons from control animals. Receptive field characteristics and electrophysiology determined that inhibition was neuronal subtype-specific with only AHTMR neurons being inhibited. One week after nerve injury the AHTMR are hyperexcitable, but can still be inhibited at the soma and transcutaneously. Withdrawal thresholds to mechanical stimuli in normal and in hyperalgesic nerve-injured animals also were increased by transcutaneous light to the affected hindpaw. This suggests that AHTMR neurons play a role not only in threshold-related withdrawal behavior in the normal animal, but also in sensitized states after nerve injury. This is the first time this subpopulation of neurons has been reversibly modulated to test their contribution to withdrawal-related behaviors before and after nerve injury. This technique may prove useful to define the role of selective neuronal populations in different pain states. |
| Author | Eisenach, James C. Boyden, Edward S. Houle, Timothy T. Peters, Christopher M. Hayashida, Kenichiro Ririe, Douglas G. Harris, Michael H. Boada, M. Danilo Martin, Thomas J. |
| AuthorAffiliation | Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA The Synthetic Neurobiology Group, Media Lab, Massachusetts Institute of Technology, Cambridge, MA, USA |
| AuthorAffiliation_xml | – name: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA The Synthetic Neurobiology Group, Media Lab, Massachusetts Institute of Technology, Cambridge, MA, USA – name: a Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA – name: b The Synthetic Neurobiology Group, Media Lab, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA |
| Author_xml | – sequence: 1 givenname: M. Danilo surname: Boada fullname: Boada, M. Danilo organization: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA – sequence: 2 givenname: Thomas J. surname: Martin fullname: Martin, Thomas J. organization: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA – sequence: 3 givenname: Christopher M. surname: Peters fullname: Peters, Christopher M. organization: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA – sequence: 4 givenname: Kenichiro surname: Hayashida fullname: Hayashida, Kenichiro organization: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA – sequence: 5 givenname: Michael H. surname: Harris fullname: Harris, Michael H. organization: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA – sequence: 6 givenname: Timothy T. surname: Houle fullname: Houle, Timothy T. organization: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA – sequence: 7 givenname: Edward S. surname: Boyden fullname: Boyden, Edward S. organization: The Synthetic Neurobiology Group, Media Lab, Massachusetts Institute of Technology, Cambridge, MA, USA – sequence: 8 givenname: James C. surname: Eisenach fullname: Eisenach, James C. organization: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA – sequence: 9 givenname: Douglas G. surname: Ririe fullname: Ririe, Douglas G. email: dririe@wakehealth.edu organization: Department of Anesthesiology, Wake Forest School of Medicine, Winston-Salem, NC, USA |
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| Copyright | 2014 International Association for the Study of Pain International Association for the Study of Pain 2015 INIST-CNRS Copyright © 2014 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. 2014 Elsevier B.V. on behalf of International Association for the Study of Pain. All rights reserved. 2014 |
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| Keywords | Nociceptor A fiber Pain C fiber Withdrawal Electrophysiology Nerve injury Sensory neuron Mechanotransduction Optogenetics Neuropathic Hyperalgesia Nervous system diseases Rat Mechanoreceptor Rodentia Vertebrata Mammalia Animal Withdrawal behavior Lesion |
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| Snippet | Fast-conducting peripheral high-threshold mechanoreceptors contribute to normal and nerve-injury-related withdrawal behavior.
Fast-conducting myelinated... Fast-conducting peripheral high-threshold mechanoreceptors contribute to normal and nerve-injury-related withdrawal behavior. Fast-conducting myelinated... Fast-conducting myelinated high-threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles... Fast conducting myelinated high threshold mechanoreceptors (AHTMR) are largely thought to transmit acute nociception from the periphery. However, their roles... |
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| SubjectTerms | A fiber Analysis of Variance Animals Biological and medical sciences C fiber Dependovirus - genetics Disease Models, Animal Electrophysiology Fundamental and applied biological sciences. Psychology Ganglia, Spinal - cytology Glial Fibrillary Acidic Protein - metabolism Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Hyperalgesia Hyperalgesia - pathology Hyperalgesia - physiopathology Male Mechanoreceptors - physiology Mechanotransduction Medical sciences Membrane Potentials - physiology Nerve Fibers, Myelinated - physiology Nerve injury Nervous system (semeiology, syndromes) Nervous system as a whole Neural Conduction - physiology Neurofilament Proteins - metabolism Neurology Neuropathic Nociceptor Optogenetics Pain Pain Measurement Pain Threshold - physiology Peripheral Nerve Injuries - pathology Peripheral Nerve Injuries - physiopathology Proton Pumps - genetics Proton Pumps - metabolism Rats Rats, Sprague-Dawley Rats, Transgenic Sensory neuron Somesthesis and somesthetic pathways (proprioception, exteroception, nociception); interoception; electrolocation. Sensory receptors Time Factors Vertebrates: nervous system and sense organs Withdrawal |
| Title | Fast-conducting mechanoreceptors contribute to withdrawal behavior in normal and nerve injured rats |
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