Defined medium organotypic cultures of spinal cord put 'pain in a dish'

Neuromethods

Volumn 73, Issue , 2012, Pages 405-436

  Biggs, James E ^a   Van B Lu, ^a   Kim, Helena J ^a   Lai, Aaron ^a   Todd, Kathryn G ^a   Ballanyi, Klaus ^a   Colmers, William F ^a   Smith, Peter A ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Calcium imaging; Chronic pain; Dorsal horn; Electrophysiology; Immunohistochemistry; Neurons; Nociception; Organotypic; Spinal cord

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM; POTASSIUM;

ADENOVIRUS INFECTION; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM SIGNALING; CELL ACTIVATION; CHRONIC PAIN; CLINICAL PROTOCOL; CULTURE MEDIUM; ELECTROSTIMULATION; EMBRYO; FETUS; MICROGLIA; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL NETWORK; NERVE EXCITABILITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROANATOMY; NEUROIMAGING; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN EXPRESSION; RAT; SPINAL CORD; SPINAL CORD DORSAL HORN;

EID: 84867558622     PISSN: 08932336     EISSN: 19406045     Source Type: Book Series    
DOI: 10.1007/978-1-62703-020-5_14     Document Type: Article

References (64)

1. Woolf CJ (1983) Evidence for a central component of post-injury pain hypersensitivity. Nature 306:686-688
2. Sandkühler J (2009) Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 89:707-758
3. Millan MJ (1999) The induction of pain: an integrative review. Prog Neurobiol 57:1-164
4. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y (2005) BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438: 1017-1021
5. Lu VB, Biggs JE, Stebbing MJ, Balasubramanyan S, Todd KG, Lai AY, Colmers WF, Dawbarn D, Ballanyi K, Smith PA (2009) BDNF Drives the changes in excitatory synaptic transmission in the rat super fi cial dorsal horn that follow sciatic nerve injury. J Physiol 587:1013-1032
6. Ballerini L, Galante M (1998) Network bursting by organotypic spinal slice cultures in the presence of bicuculline and/or strychnine is developmentally regulated. Eur J Neurosci 10:2871-2879
7. Avossa D, Rosato-Siri MD, Mazzarol F, Ballerini L (2003) Spinal circuits formation: a study of developmentally regulated markers in organotypic cultures of embryonic mouse spinal cord. Neuroscience 122:391-405
8. Gähwiler BH (1981) Organotypic monolayer cultures of nervous tissue. J Neurosci Methods 4:329-342
9. De Simoni A, Griesinger CB, Edwards FA (2003) Development of rat CA 1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J Physiol 550:135-147
10. Gähwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci 20:471-477
11. Lu VB, Moran TD, Balasubramanyan S, Alier KA, Dryden WF, Colmers WF, Smith PA (2006) Substantia Gelatinosa neurons in de fi ned-medium organotypic slice culture are similar to those in acute slices from young adult rats. Pain 121:261-275
12. Lu VB, Colmers WF, Smith PA (2009) Longterm effects of brain-derived neurotrophic factor on the frequency of inhibitory synaptic events in the rat super fi cial dorsal horn. Neuroscience 161:1135-1143
13. Lu VB, Ballanyi K, Colmers WF, Smith PA (2007) Neuron type-speci fi c effects of brainderived neurotrophic factor in rat super fi cial dorsal horn and their relevance to central sensitization. J Physiol 584:543-563
14. Trapp S, Ballanyi K (2012) Autonomic nervous system in vitro: studying tonically active neurons controlling vagal out fl ow in rodent brainstem slices. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 1-59
15. Ruangkittisakul A, Panaitescu B, Secchia L, Bobocea N, Kantor C, Kuribayashi J, Iizuka M, Ballanyi K (2012) Isolated brainstem respiratory centers from perinatal rodents. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 61-124
16. Kantor C, Panaitescu B, Kuribayashi J, Ruangkittisakul A, Jovanovic I, Leung V, Lee TF, MacTavish D, Jhamandas JH, Cheung PY, Ballanyi K (2012) Spontaneous neural network oscillations in hippocampus, cortex and locus coeruleus of newborn rat and piglet brain slices. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 315-356
17. De Curtis M, Lilbrizzi L, Uva L, Gnatkovsky V (2012) Neuronal networks in the in vitro isolated guinea pig brain. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 357-383
18. Mandadi S, Nakanishi ST, Han P, Humphreys J, Whelan PJ (2012) The use of rodent isolated spinal cord preparations to examine motor output. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 437-464
19. Gustafson-Vickers SL, Lu VB, Lai AY, Todd KG, Ballanyi K, Smith PA (2008) Long-term actions of interleukin-1beta on delay and tonic fi ring neurons in rat super fi cial dorsal horn and their relevance to central sensitization. Mol Pain 4:63
20. Balasubramanyan S, Stemkowski PL, Stebbing MJ, Smith PA (2006) Sciatic chronic constriction injury produces cell-type speci fi c changes in the electrophysiological properties of rat Substantia Gelatinosa neurons. J Neurophysiol 96:579-590
21. Biggs JE, Lu VB, Stebbing MJ, Balasubramanyan S, Smith PA (2010) Is BDNF suf fi cient for information transfer between microglia and dorsal horn neurons during the onset of central sensitization? Mol Pain 6:44
22. Tsuda M, Inoue K, Salter MW (2005) Neuropathic pain and spinal microglia: a big problem from molecules in small glia. Trends Neurosci 28:101-107
23. Echeverry S, Shi XQ, Zhang J (2007) Characterization of cell proliferation in rat spinal cord following peripheral nerve injury and the relationship with neuropathic pain. Pain 135:37-47
24. Hendrich J, Van Minh AT, Heblich F, Nieto- Rostro M, Watschinger K, Striessnig J, Wratten J, Davies A, Dolphin AC (2008) Pharmacological disruption of calcium channel traf fi cking by the alpha/2delta ligand gabapentin. Proc Natl Acad Sci USA 105: 3628-3633
25. Bauer CS, Nieto-Rostro M, Rahman W, Tran- Van-Minh A, Ferron L, Douglas L, Kadurin I, Sri Ranjan Y, Fernandez-Alacid L, Millar NS, Dickenson AH, Lujan R, Dolphin AC (2009) The increased traf fi cking of the calcium channel subunit alpha2/delta-1 to presynaptic terminals in neuropathic pain is inhibited by the alpha2/delta ligand pregabalin. J Neurosci 29:4076-4088
26. Biggs JE, Balasubramanyan S, Ballanyi K, Smith PA (2008) Chronic Gabapentin acts intracellularly to reduce dorsal horn excitability. Soc Neurosci Abs Abstract # 569.6/LL6
27. Luhmann HJ, Kilb W (2012) Intact in vitro preparation of the neonatal rodent cerebral cortex- analysis of cellular properties and network activity. In Isolated Central Nervous System Circuits (Ed K Ballanyi), Neuromethods Series Vol. 73 (Ed W Walz). Springer Science+Business Media, LLC, New York, NY, pp 301-314
28. Chen Y, Balasubramanyan S, Lai AY, Todd KG, Smith PA (2009) Effects of sciatic nerve axotomy on excitatory synaptic transmission in rat substantia gelatinosa. J Neurophysiol 102:3203-3215
29. Watkins LR, Maier SF (2002) Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiol Rev 82:981-1011
30. Milligan ED, Twining C, Chacur M, Biedenkapp J, OConnor K, Poole S, Tracey K, Martin D, Maier SF, Watkins LR (2003) Spinal glia and proin fl ammatory cytokines mediate mirror-image neuropathic pain in rats. J Neurosci 23:1026-1040
31. Milligan ED, Zapata V, Chacur M, Schoeniger D, Biedenkapp J, OConnor KA, Verge GM, Chapman G, Green P, Foster AC, Naeve GS, Maier SF, Watkins LR (2004) Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats. Eur J Neurosci 20:2294-2302
32. Siao CJ, Tsirka SE (2002) Tissue plasminogen activator mediates microglial activation via its fi nger domain through annexin II. J Neurosci 22:3352-3358
33. Eckert WA III, Willcockson HH, Light AR (2001) Interference of biocytin with opioidevoked hyperpolarization and membrane properties of rat spinal substantia gelatinosa neurons. Neurosci Lett 297:117-120
34. Todd AJ, Lewis SG (1986) The morphology of Golgi-stained neurons in lamina II of the rat spinal cord. J Anat 149:113-119
35. Grudt TJ, Perl ER (2002) Correlations between neuronal morphology and electrophysiological features in the rodent super fi cial dorsal horn. J Physiol 540:189-207
36. Todd AJ, McKenzie J (1989) GABAimmunoreactive neurons in the dorsal horn of the rat spinal cord. Neuroscience 31:799-806
37. Scholz J, Woolf CJ (2007) The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 10:1361-1368
38. Lai AY, Todd KG (2008) Differential regulation of trophic and proin fl ammatory microglial effectors is dependent on severity of neuronal injury. Glia 56:259-270
39. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S (1998) Microglia-speci fi c localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57:1-9
40. Ruangkittisakul A, Schwarzacher SW, Secchia L, Poon BY, Ma Y, Funk GD, Ballanyi K (2006) High sensitivity to neuromodulator- activated signaling pathways at physiological [K + ] of confocally imaged respiratory center neurons in on-line-calibrated newborn rat brainstem slices. J Neurosci 26: 11870-11880
41. Paredes RM, Etzler JC, Watts LT, Zheng W, Lechleiter JD (2008) Chemical calcium indicators. Methods 46:143-151
42. Gee KR, Brown KA, Chen WN, Bishop- Stewart J, Gray D, Johnson I (2000) Chemical and physiological characterization of fl uo-4 Ca 2+ -indicator dyes. Cell Calcium 27:97-106
43. Perrier JF, Noraberg J, Simon M, Hounsgaard J (2000) Dedifferentiation of intrinsic response properties of motoneurons in organotypic cultures of the spinal cord of the adult turtle. Eur J Neurosci 12:2397-2404
44. Safronov BV, Wolff M, Vogel W (1997) Functional distribution of three types of Na + channel on soma and processes of dorsal horn neurones of rat spinal cord. J Physiol 503: 371-385
45. Todd AJ (2010) Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci 11:823-836
46. Hashizume H, De Leo JA, Colburn RW, Weinstein JN (2000) Spinal glial activation and cytokine expression after lumbar root injury in the rat. Spine 25:1206-1217
47. Lee J, Kim M, Back S, Uhm C, Hong S, Na H (2004) Activation of spinal microglia following peripheral nerve injury is related to the generation of mechanical allodynia in a rat model of neuropathic pain. Abstract Viewer/ Itinerary Planner Washington, DC: Society for Neuroscience, Online 2004; Program No. 518.8
48. Clark AK, Gentry C, Bradbury EJ, McMahon SB, Malcangio M (2006) Role of spinal microglia in rat models of peripheral nerve injury and in fl ammation. Eur J Pain 11:223-230
49. Ban fi eld MJ, Naylor RL, Robertson AG, Allen SJ, Dawbarn D, Brady RL (2001) Speci fi city in Trk receptor:neurotrophin interactions: the crystal structure of TrkB-d5 in complex with neurotrophin-4/5. Structure 9:1191-1199
50. Cho HJ, Kim JK, Zhou XF, Rush RA (1997) Increased brain-derived neurotrophic factor immunoreactivity in rat dorsal root ganglia and spinal cord following peripheral in fl ammation. Brain Res 764:269-272
51. Fukuoka T, Kondo E, Dai Y, Hashimoto N, Noguchi K (2001) Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. J Neurosci 21: 4891-4900
52. Pezet S, Cunningham J, Patel J, Grist J, Gavazzi I, Lever IJ, Malcangio M (2002) BDNF modulates sensory neuron synaptic activity by a facilitation of GABA transmission in the dorsal horn. Mol Cell Neurosci 21:51-62
53. Wilkemeyer MF, Smith KL, Zarei MM, Benke TA, Swann JW, Angelides KJ, Eisensmith RC (1996) Adenovirus-mediated gene transfer into dissociated and explant cultures of rat hippocampal neurons. J Neurosci Res 43: 161-174
54. Cho ES, Lee SY, Park JY, Hong SG, Ryu PD (2007) Organotypic slice culture of the hypothalamic paraventricular nucleus of rat. J Vet Sci 8:15-20
55. Wilkemeyer MF, Angelides KJ (1995) Adenovirus-mediated expression of a reporter gene in thalamocortical cocultures. Brain Res 703:129-138
56. Ruscheweyh R, Sandkühler J (2005) Longrange oscillatory Ca 2+ waves in rat spinal dorsal horn. Eur J Neurosci 22:1967-1976
57. Asghar AU, Cilia La Corte PF, LeBeau FE, Al Dawoud M, Reilly SC, Bühl EH (2005) Whittington MA, King AE Oscillatory activity within rat substantia gelatinosa in vitro: a role for chemical and electrical neurotransmission. J Physiol 562:183-198
58. Labrakakis C, Lorenzo LE, Bories C, Ribeiroda- Silva A, De Koninck Y (2009) Inhibitory coupling between inhibitory interneurons in the spinal cord dorsal horn. Mol Pain 5:24
59. Bardoni R, Ghirri A, Zonta M, Betelli C, Vitale G, Ruggieri V, Sandrini M, Carmignoto G (2010) Glutamate-mediated astrocyte-to-neuron signalling in the rat dorsal horn. J Physiol 588:831-846
60. Ballanyi K, Panaitescu B, Ruangkittisakul A (2010) Control of breathing by "nerve glue". Sci Signal 3:e41
61. Huxtable AG, Zwicker JD, Alvares TS, Ruangkittisakul A, Fang X, Hahn LB, Posse de Chaves E, Baker GB, Ballanyi K, Funk GD (2010) Glia contribute to the purinergic modulation of inspiratory rhythm-generating networks. J Neurosci 30:3947-3958
62. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, fl ies and mice with improved GCaMP calcium indicators. Nat Methods 6:875-881
63. Akerboom J, Rivera JD, Guilbe MM, Malavé EC, Hernandez HH, Tian L, Hires SA, Marvin JS, Looger LL, Schreiter ER (2009) Crystal structures of the GCaMP calcium sensor reveal the mechanism of fl uorescence signal change and aid rational design. J Biol Chem 284: 6455-6464
64. Mao T, OConnor DH, Scheuss V, Nakai J, Svoboda K (2008) Characterization and subcellular targeting of GCaMP-type genetically- encoded calcium indicators. PLoS One 3:e1796