Impact of behavioral control on the processing of nociceptive stimulation
How nociceptive signals are processed within the spinal cord, and whether these signals lead to behavioral signs of neuropathic pain, depends upon their relation to other events and behavior. Our work shows that these relations can have a lasting effect on spinal plasticity, inducing a form of lear...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2012-08-01
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| Series: | Frontiers in Physiology |
| Subjects: | |
| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fphys.2012.00262/full |
| _version_ | 1818150840314101760 |
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| author | James W Grau Russell eHuie Sandra M. Garraway Michelle A. Hook Eric D. Crown Kyle M. Baumbauer Kuan H. Lee Kevin C. Hoy Adam R Ferguson |
| author_facet | James W Grau Russell eHuie Sandra M. Garraway Michelle A. Hook Eric D. Crown Kyle M. Baumbauer Kuan H. Lee Kevin C. Hoy Adam R Ferguson |
| author_sort | James W Grau |
| collection | DOAJ |
| description | How nociceptive signals are processed within the spinal cord, and whether these signals lead to behavioral signs of neuropathic pain, depends upon their relation to other events and behavior. Our work shows that these relations can have a lasting effect on spinal plasticity, inducing a form of learning that alters the effect of subsequent nociceptive stimuli. The capacity of lower spinal systems to adapt, in the absence of brain input, is examined in spinally transected rats that receive a nociceptive shock to the tibialis anterior muscle of one hind leg. If shock is delivered whenever the leg is extended (controllable stimulation), it induces an increase in flexion duration that minimizes net shock exposure. This learning is not observed in subjects that receive the same amount of shock independent of leg position (uncontrollable stimulation). These two forms of stimulation have a lasting, and divergent, effect on subsequent learning: Controllable stimulation enables learning whereas uncontrollable stimulation disables it (learning deficit). Uncontrollable stimulation also enhances mechanical reactivity (allodynia). We review evidence that training with controllable stimulation engages a BDNF-dependent process that can both prevent and reverse the consequences of uncontrollable shock. We relate these effects to changes in BDNF protein and TrkB signaling. Controllable stimulation is also shown to counter the effects of peripheral inflammation (from intradermal capsaicin). A model is proposed that assumes nociceptive input is gated at an early stage, within the dorsal horn. his gate is sensitive to current environmental relations (between proprioceptive and nociceptive input), allowing stimulation to be classified as controllable or uncontrollable. We further propose that the status of this gate is affected by past experience and that a history of uncontrollable stimulation will promote the development of neuropathic pain. |
| first_indexed | 2024-12-11T13:29:19Z |
| format | Article |
| id | doaj.art-c33dd4934d824b7fae402c17305298a2 |
| institution | Directory Open Access Journal |
| issn | 1664-042X |
| language | English |
| last_indexed | 2024-12-11T13:29:19Z |
| publishDate | 2012-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Physiology |
| spelling | doaj.art-c33dd4934d824b7fae402c17305298a22022-12-22T01:05:22ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2012-08-01310.3389/fphys.2012.0026225528Impact of behavioral control on the processing of nociceptive stimulationJames W Grau0Russell eHuie1Sandra M. Garraway2Michelle A. Hook3Eric D. Crown4Kyle M. Baumbauer5Kuan H. Lee6Kevin C. Hoy7Adam R Ferguson8Texas A&M UniversityBrain and Spinal Injury Center (BASIC)Texas A&M UniversityTexas A&M UniversityAbbott LaboratoriesUniversity of Pittsburgh School of MedicineTexas A&M UniversityTexas A&M UniversityBrain and Spinal Injury Center (BASIC)How nociceptive signals are processed within the spinal cord, and whether these signals lead to behavioral signs of neuropathic pain, depends upon their relation to other events and behavior. Our work shows that these relations can have a lasting effect on spinal plasticity, inducing a form of learning that alters the effect of subsequent nociceptive stimuli. The capacity of lower spinal systems to adapt, in the absence of brain input, is examined in spinally transected rats that receive a nociceptive shock to the tibialis anterior muscle of one hind leg. If shock is delivered whenever the leg is extended (controllable stimulation), it induces an increase in flexion duration that minimizes net shock exposure. This learning is not observed in subjects that receive the same amount of shock independent of leg position (uncontrollable stimulation). These two forms of stimulation have a lasting, and divergent, effect on subsequent learning: Controllable stimulation enables learning whereas uncontrollable stimulation disables it (learning deficit). Uncontrollable stimulation also enhances mechanical reactivity (allodynia). We review evidence that training with controllable stimulation engages a BDNF-dependent process that can both prevent and reverse the consequences of uncontrollable shock. We relate these effects to changes in BDNF protein and TrkB signaling. Controllable stimulation is also shown to counter the effects of peripheral inflammation (from intradermal capsaicin). A model is proposed that assumes nociceptive input is gated at an early stage, within the dorsal horn. his gate is sensitive to current environmental relations (between proprioceptive and nociceptive input), allowing stimulation to be classified as controllable or uncontrollable. We further propose that the status of this gate is affected by past experience and that a history of uncontrollable stimulation will promote the development of neuropathic pain.http://journal.frontiersin.org/Journal/10.3389/fphys.2012.00262/fullLearningNociceptionRecovery of FunctionBDNFplasticityspinal cord injury |
| spellingShingle | James W Grau Russell eHuie Sandra M. Garraway Michelle A. Hook Eric D. Crown Kyle M. Baumbauer Kuan H. Lee Kevin C. Hoy Adam R Ferguson Impact of behavioral control on the processing of nociceptive stimulation Frontiers in Physiology Learning Nociception Recovery of Function BDNF plasticity spinal cord injury |
| title | Impact of behavioral control on the processing of nociceptive stimulation |
| title_full | Impact of behavioral control on the processing of nociceptive stimulation |
| title_fullStr | Impact of behavioral control on the processing of nociceptive stimulation |
| title_full_unstemmed | Impact of behavioral control on the processing of nociceptive stimulation |
| title_short | Impact of behavioral control on the processing of nociceptive stimulation |
| title_sort | impact of behavioral control on the processing of nociceptive stimulation |
| topic | Learning Nociception Recovery of Function BDNF plasticity spinal cord injury |
| url | http://journal.frontiersin.org/Journal/10.3389/fphys.2012.00262/full |
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