Organization of sensory input to the nociceptive‐specific cutaneous trunk muscle reflex in rat, an effective experimental system for examining nociception and plasticity

Journal of Comparative Neurology - Tập 522 Số 5 - Trang 1048-1071 - 2014
Jeffrey C. Petruska1,2, Darrell F. Barker3, Sandra M. Garraway4, Robert Trainer5, James W. Fransen1, Peggy A. Seidman5, Roy G. Soto5, Lorne M. Mendell3, Richard D. Johnson6
1Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, Kentucky, 40202
2Department of Neurological Surgery, Kentucky Spinal Cord Injury Research Center, University of Louisville, Louisville, Kentucky, 40202
3Department of Neurobiology and Behavior, SUNY Stony Brook, Stony Brook, New York, 11794-5230
4Department of Physiology, Emory University School of Medicine, Atlanta, Georgia, 30322-3110
5Department of Anesthesiology, SUNY Stony Brook School of Medicine, Stony Brook, New York, 11794-8081
6Department of Physiological Sciences, University of Florida, Gainesville, Florida, 32210-0144

Tóm tắt

ABSTRACTDetailed characterization of neural circuitries furthers our understanding of how nervous systems perform specific functions and allows the use of those systems to test hypotheses. We have characterized the sensory input to the cutaneous trunk muscle (CTM; also cutaneus trunci [rat] or cutaneus maximus [mouse]) reflex (CTMR), which manifests as a puckering of the dorsal thoracolumbar skin and is selectively driven by noxious stimuli. CTM electromyography and neurogram recordings in naïve rats revealed that CTMR responses were elicited by natural stimuli and electrical stimulation of all segments from C4 to L6, a much greater extent of segmental drive to the CTMR than previously described. Stimulation of some subcutaneous paraspinal tissue can also elicit this reflex. Using a selective neurotoxin, we also demonstrate differential drive of the CTMR by trkA‐expressing and nonexpressing small‐diameter afferents. These observations highlight aspects of the organization of the CTMR system that make it attractive for studies of nociception and anesthesiology and plasticity of primary afferents, motoneurons, and the propriospinal system. We use the CTMR system to demonstrate qualitatively and quantitatively that experimental pharmacological treatments can be compared with controls applied either to the contralateral side or to another segment, with the remaining segments providing controls for systemic or other treatment effects. These data indicate the potential for using the CTMR system as both an invasive and a noninvasive quantitative assessment tool providing improved statistical power and reduced animal use. J. Comp. Neurol. 522:1048–1071, 2014. © 2013 Wiley Periodicals, Inc.

Từ khóa


Tài liệu tham khảo

10.1046/j.0953-816x.2001.01811.x

Ashkenaz DM, 1935, The viscero‐pannicular reflex, Am J Physiol, 112, 573, 10.1152/ajplegacy.1935.112.4.573

Bailey CS, 1984, Cutaneous innervation of the thorax and abdomen of the dog, Am J Vet Res, 45, 1689

10.1006/exnr.1997.6734

10.1002/dneu.20401

Bates B, 2007, Bates' guide to physical examination and history taking, 595

10.1159/000145386

10.1523/JNEUROSCI.18-08-03059.1998

10.1097/ALN.0b013e3181a915e7

10.1016/0022-510X(91)90159-5

10.1002/cne.902960408

10.1089/neu.1991.8.103

10.1002/jnr.1254

10.1002/cne.902960409

Borgens RB, 2002, Behavioral recovery from spinal cord injury following delayed application of polyethylene glycol, J Exp Biol, 205, 1, 10.1242/jeb.205.1.1

10.1111/j.1460-9568.2011.07950.x

10.1006/mcne.1998.0719

10.1016/j.neuron.2005.08.015

10.1097/ALN.0b013e318182c26b

10.1007/BF00495150

10.3109/07853899509031965

10.1097/AAP.0b013e31820c2c30

10.1038/nature04223

10.1038/nrn894

10.1016/S0959-4388(03)00090-4

10.1146/annurev.neuro.26.041002.131022

10.1093/bja/aen088

10.1002/(SICI)1096-9861(19971103)387:4<489::AID-CNE2>3.0.CO;2-Z

10.1523/JNEUROSCI.12-04-01454.1992

10.1152/jn.00371.2002

10.1002/cne.902610409

10.1097/00000542-198907000-00014

10.1097/00000542-200507000-00018

10.1523/JNEUROSCI.2185-06.2006

10.1523/JNEUROSCI.0249-05.2005

10.1113/jphysiol.2005.086199

10.1523/JNEUROSCI.1072-06.2006

10.1038/nn.3295

10.1002/(SICI)1096-9861(19971229)389:4<545::AID-CNE1>3.0.CO;2-0

10.1006/dbio.1997.8658

10.1046/j.1460-9568.2003.02982.x

Gerner P, 2006, Doxepin by topical application and intrathecal route in rats, Anesth Analg, 102, 283, 10.1213/01.ane.0000183639.37428.4d

10.1152/jn.2000.83.5.3076

10.1152/jn.1997.77.1.502

10.1097/00000542-200602000-00024

10.1016/j.expneurol.2009.12.033

10.1002/cne.20209

10.1152/jn.1989.62.6.1260

10.1016/0304-3959(89)90135-8

10.1016/0006-8993(81)90886-6

10.1097/00001756-200307180-00003

10.1016/0306-4522(95)00334-F

10.1523/JNEUROSCI.19-12-05138.1999

10.1097/00000542-200201000-00023

Khan MA, 2002, Use of a charged lidocaine derivative, tonicaine, for prolonged infiltration anesthesia, Reg Anesth Pain Med, 27, 173

Krogh JE, 1979, The cutaneus trunci muscle in spinal reflexes, Electromyogr Clin Neurophysiol, 19, 157

10.1016/0006-8993(84)90970-3

Lawson SN, 1987, The morphological consequences of neonatal treatment with capsaicin on primary afferent neurones in adult rats, Acta Physiol Hung, 69, 315

10.1097/01.anes.0000270758.77314.b4

10.1113/jphysiol.2008.166306

10.1152/jn.00748.2005

10.1523/JNEUROSCI.1726-06.2006

10.1073/pnas.1121138109

10.1002/dneu.20605

10.1523/JNEUROSCI.17-21-08476.1997

10.1002/(SICI)1096-9861(19970519)381:4<428::AID-CNE3>3.0.CO;2-4

10.1002/cne.903610305

10.1016/S0896-6273(00)80966-6

10.1016/j.pain.2007.03.021

10.1002/cne.21185

10.1016/0306-4522(81)90032-4

Nagy JI, 1983, Dose‐dependent effects of capsaicin on primary sensory neurons in the neonatal rat, J Neurosci, 3, 399, 10.1523/JNEUROSCI.03-02-00399.1983

10.1002/(SICI)1096-9861(19990719)410:1<73::AID-CNE7>3.0.CO;2-3

10.1080/08990229771187

10.1016/S0891-0618(00)00080-6

10.1097/00001756-200011090-00037

10.1152/jn.2000.84.5.2365

10.1016/S0306-4522(02)00409-8

Petruska JC, 2005, BDNF sensitizes the nociceptive‐specific CTM reflex, Soc Neurosci Abstr Abstract Viewer/Itinerary Planner, 982

Petruska JC, 2008, Dexmedetomidine extension of local anesthetic effect of bupivacaine in a peripheral nerve block in rats, Anesth Analg IARS Meeting Abstr, 203

10.1016/0197-0186(82)90027-4

10.1006/dbio.1998.8861

10.1152/jn.1999.81.5.2398

10.1038/aps.2009.129

10.1016/S0304-3959(99)00042-1

10.1016/0959-4388(92)90183-L

Soto R, 2007, The in vitro effect of dexmedetomidine on rat sciatic nerve transmission, Anesthesiol ASA Meeting Abstr, 976

10.1523/JNEUROSCI.19-15-06497.1999

10.1113/jphysiol.2002.027656

10.1016/0304-3959(96)03116-8

10.1002/cne.10669

Tansey KE, 2007, Plasticity in an intersegmental pain reflex following spinal cord lateral hemisection in the rat, 606

10.1152/jn.1988.60.2.463

10.1152/jn.1988.60.2.446

10.1073/pnas.96.14.7714

10.1017/S1740925X12000087

10.1016/j.brainres.2005.01.019

10.1016/j.jpain.2005.07.005

10.1007/BF01187079

Verge VM, 1992, Colocalization of NGF binding sites, trk mRNA, and low‐affinity NGF receptor mRNA in primary sensory neurons: responses to injury and infusion of NGF, J Neurosci, 12, 4011, 10.1523/JNEUROSCI.12-10-04011.1992

10.1016/S0028-3908(97)00126-3

10.1213/ane.0b013e318182401b

10.1126/science.2530630

Wilson PO, 1988, The immunolocalization of protein gene product 9.5 using rabbit polyclonal and mouse monoclonal antibodies, Br J Exp Pathol, 69, 91

10.1002/cne.903510302

10.1034/j.1399-6576.2000.440604.x

10.1016/0304-3959(94)90051-5

10.1016/S0304-3959(96)03177-6

10.1016/S0304-3959(96)03176-4

10.1213/ane.0b013e318176be73

10.1016/S0006-8993(96)01466-7

10.1152/jn.2000.84.2.798

10.1016/j.neuron.2004.12.015