Fluorescence imaging of active respiratory networks

Respiratory Physiology and Neurobiology

Volumn 168, Issue 1-2, 2009, Pages 26-38

  Ruangkittisakul, Araya ^a   Okada, Yasumasa ^b   Oku, Yoshitaka ^c   Koshiya, Naohiro ^d   Ballanyi, Klaus ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b KEIO UNIVERSITY   (Japan)

^c HYOGO COLLEGE OF MEDICINE   (Japan)

^d Blanchette Rockefeller Neurosciences Institute   (United States)

Author keywords

2 Photon microscopy; Breathing; Calcium imaging; Chemosensitivity; Fictive eupnea; Fictive sighs; Fluorescence; Para facial respiratory group; Pre Botzinger complex; Respiratory centre; Respiratory control; Respiratory rhythm; Voltage sensitive dye imaging

Indexed keywords

CALCIUM CHANNEL; FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN; NEUROKININ 1 RECEPTOR; TETRAMETHYLRHODAMINE;

ARTICLE; BREATHING; BREATHING PATTERN; FLUORESCENCE IMAGING; NERVE CELL NETWORK; NONHUMAN; PATCH CLAMP; PONS ANGLE; PRIORITY JOURNAL; RESPIRATION CENTER; RESPIRATION CONTROL; RESPIRATORY NERVE CELL; SIGNAL TRANSDUCTION; VOLTAGE CLAMP;

ANIMALS; CALCIUM; DIAGNOSTIC IMAGING; MEDULLA OBLONGATA; NERVE NET; NEURAL PATHWAYS; NEURONS; RESPIRATION; RESPIRATORY CENTER;

EID: 68949189049     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2009.02.012     Document Type: Article

References (84)

1. Arata A., Onimaru H., and Homma I. Respiration-related neurons in the ventral medulla of newborn rats in vitro. Brain Res. Bull. 24 (1990) 599-604
2. Ballanyi K., and Onimaru H. Respiratory network analysis, isolated respiratory center functions. In: Binder M., Hirsch M., Hirokawa N., and Windhorst U. (Eds). Encyclopedic Reference of Neuroscience (2009), Springer Verlag, Heidelberg, New York, Tokyo part 18 3453-3458
3. Ballanyi K., Onimaru H., and Homma I. Respiratory network function in the isolated brainstem-spinal cord of newborn rats. Prog. Neurobiol. 59 (1999) 583-634
4. Ballanyi K., Onimaru H., and Keller B. Respiratory network analysis, functional imaging. In: Binder M., Hirsch M., Hirokawa N., and Windhorst U. (Eds). Encyclopedic Reference of Neuroscience (2009), Springer Verlag, Heidelberg, New York, Tokyo part 18 3447-3453
5. Ballanyi, K., Ruangkittisakul, A., this issue. Structure-function analysis of inspiratory pre-Bötzinger complex networks in "calibrated" newborn rat brainstem slices. Resp. Physiol. Neurobiol.
6. Ballanyi, K., Ruangkittisakul, A., Onimaru, H., in press. Opiates prolongs and anoxia shortens the delay between onset of pre-inspiratory (pFRG) and inspiratory (preBötC) network bursting in newborn rat brainstems. Eur. J. Physiol., (Pflüger's Arch), doi:10.1007/s00424-009-0645-3.
7. Ballanyi K., Mückenhoff K., Bellingham M.C., Okada Y., Scheid P., and Richter D.W. Activity related pH changes in respiratory neurons and glial cells of cats. Neuroreport 6 (1994) 33-36
8. Barnes B.J., Tuong C.M., and Mellen N.M. Functional imaging reveals respiratory network activity during hypoxic and opioid challenge in the neonate rat tilted sagittal slab preparation. J. Neurophysiol. 97 (2007) 2283-2292
9. 2+ levels in brainstem motoneurones from mouse. J. Physiol. 555 (2004) 45-59
10. Bouvier J., Autran S., Dehorter N., Katz D.M., Champagnat J., Fortin G., and Thoby-Brisson M. Brain-derived neurotrophic factor enhances fetal respiratory rhythm frequency in the mouse preBötzinger complex in vitro. Eur. J. Neurosci. 28 (2008) 510-520
11. Bradley P.M., Murphy D., Kasparov S., Croker J., and Paton J.F. A micro-optrode for simultaneous extracellular electrical and intracellular optical recording from neurons in an intact oscillatory neuronal network. J. Neurosci. Methods 168 (2008) 383-395
12. Brockhaus J., Ballanyi K., Smith J.C., and Richter D.W. Microenvironment of respiratory neurons in the in vitro brainstem-spinal cord of neonatal rats. J. Physiol. 462 (1993) 421-445
13. Büsselberg D., Bischoff A.M., and Richter D.W. A combined blockade of glycine and calcium-dependent potassium channels abolishes the respiratory rhythm. Neuroscience 122 (2003) 831-541
14. Ebner T.J., and Chen G. Use of voltage-sensitive dyes and optical recordings in the central nervous system. Prog. Neurobiol. 46 (1995) 463-506
15. Eugenin J., Nicholls J.G., Cohen L.B., and Muller K.J. Optical recording from respiratory pattern generator of fetal mouse brainstem reveals a distributed network. Neuroscience 137 (2006) 1221-1227
16. Feldman J.L., and Del Negro C.A. Looking for inspiration: new perspectives on respiratory rhythm. Nat. Rev. Neurosci. 7 (2006) 232-242
17. Fisher J.A., Marchenko V.A., Yodh A.G., and Rogers R.F. Spatiotemporal activity patterns during respiratory rhythmogenesis in the rat ventrolateral medulla. J. Neurophysiol. 95 (2006) 1982-1991
18. Frermann D., Keller B.U., and Richter D.W. Calcium oscillations in rhythmically active respiratory neurones in the brainstem of the mouse. J. Physiol. 515 (1999) 119-131
19. Funke F., Dutschmann M., and Müller M. Imaging of respiratory-related population activity with single-cell resolution. Am. J. Physiol. Cell. Physiol. 292 (2007) C508-C516
20. Funke F., Müller M., and Dutschmann M. Reconfiguration of respiratory-related population activity in a rostrally tilted transversal slice preparation following blockade of inhibitory neurotransmission in neonatal rats. Eur. J. Physiol. 457 (2008) 185-195
21. Grass D., Pawlowski P.G., Hirrlinger J., Papadopoulos N., Richter D.W., Kirchhoff F., and Hülsmann S. Diversity of functional astroglial properties in the respiratory network. J. Neurosci. 24 (2004) 1358-1365
22. Gray P.A. Transcription factors and the genetic organization of brain stem respiratory neurons. J. Appl. Physiol. 104 (2008) 1513-1521
23. Gray P.A., Rekling J.C., Bocchiaro C.M., and Feldman J.L. Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBötzinger complex. Science 286 (1999) 1566-1568
24. Haller M., Mironov S.L., and Richter D.W. Intrinsic optical signals in respiratory brain stem regions of mice: neurotransmitters, neuromodulators, and metabolic stress. J. Neurophysiol. 86 (2001) 412-421
25. Härtel, K., Schnell, C., Hülsmann, S., in press. Astrocytic calcium signals induced by neuromodulators via functional metabotropic receptors in the ventral respiratory group of neonatal mice. Glia, doi:10.1002/glia.20808.
26. Hartelt N., Skorova E., Manzke T., Suhr M., Mironova L., Kügler S., and Mironov S.L. Imaging of respiratory network topology in living brainstem slices. Mol. Cell. Neurosci. 37 (2008) 425-431
27. Hayes J.A., and Del Negro C.A. Neurokinin receptor-expressing pre-Bötzinger complex neurons in neonatal mice studied in vitro. J. Neurophysiol. 97 (2007) 4215-4224
28. Homma R., Baker B.J., Jin L., Garaschuk O., Konnerth A., Cohen L.B., Bleau C.X., Canepari M., Djurisic M., and Zecevic D. Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes. Methods Mol. Biol. 489 (2009) 43-79
29. Hülsmann S., Straub H., Richter D.W., and Speckmann E.J. Blockade of astrocyte metabolism causes delayed excitation as revealed by voltage-sensitive dyes in mouse brainstem slices. Exp. Brain Res. 150 (2003) 117-121
30. Kawai S., Oku Y., Okada Y., Miwakeichi F., Tamura Y., and Ishiguro M. A novel statistical analysis of voltage-imaging data by structural time series modeling and its application to the respiratory neuronal network. Neurosci. Res. 63 (2009) 165-171
31. Knisley S.B., Justice R.K., Kong W., and Johnson P.L. Ratiometry of transmembrane voltage-sensitive fluorescent dye emission in hearts. Am. J. Physiol. Heart Circ. Physiol. 279 (2000) H1421-H1433
32. Kobayashi S., Onimaru H., Inoue M., Inoue T., and Sasa R. Localization and properties of respiratory neurons in the rostral pons of the newborn rat. Neuroscience 134 (2005) 317-325
33. Koizumi H., Wilson C.G., Wong S., Yamanishi T., Koshiya N., and Smith J.C. Functional imaging, spatial reconstruction, and biophysical analysis of a respiratory motor circuit isolated in vitro. J. Neurosci. 28 (2008) 2353-2365
34. Koshiya N., and Okada Y. Apparent slow propagation of membrane potential from the pre-Botzinger complex to the ventral surface of the medulla. FASEB J. 19 5 Suppl. (2005) A1640
35. Koshiya N., and Smith J.C. Neuronal pacemaker for breathing visualized in vitro. Nature 400 (1999) 360-363
36. 2-sensitivity of GABAergic neurons in the ventral medullary surface of GAD67-GFP knock-in neonatal mice. Adv. Exp. Med. Biol. 605 (2008) 338-342
37. Kuwana S., Tsunekawa N., Yanagawa Y., Okada Y., Kuribayashi J., and Obata K. Electrophysiological and morphological characteristics of GABAergic respiratory neurons in the mouse pre-Bötzinger complex. Eur. J. Neurosci. 23 (2006) 667-674
38. Ladewig T., and Keller B.U. Simultaneous patch-clamp recording and calcium imaging in a rhythmically active neuronal network in the brainstem slice preparation from mouse. Eur. J. Physiol. 440 (2000) 322-332
39. Ladewig T., Lalley P.M., and Keller B.U. Serotonergic modulation of intracellular calcium dynamics in neonatal hypoglossal motoneurons from mouse. Brain Res. 1001 (2004) 1-12
40. Ladewig T., Kloppenburg P., Lalley P.M., Zipfel W.R., Webb W.W., and Keller B.U. Spatial profiles of store-dependent calcium release in motoneurones of the nucleus hypoglossus from newborn mouse. J. Physiol. 547 (2003) 775-787
41. Lückermann M., Trapp S., and Ballanyi K. GABA- and glycine-mediated fall of intracellular pH in neurons of brainstem slices from rats. J. Neurophysiol. 77 (1997) 1844-1852
42. Mironov S.L. Metabotropic glutamate receptors activate dendritic calcium waves and TRPM channels which drive rhythmic respiratory patterns in mice. J. Physiol. 586 (2008) 2277-2291
43. 2+ influx into respiratory neurons during hypoxia. Neuropharmacology 48 (2005) 1056-1065
44. Mironov S.L., and Richter D.W. Oscillations and hypoxic changes of mitochondrial variables in neurons of the brainstem respiratory centre of mice. J. Physiol. 533 (2001) 227-236
45. 2+ transients do not contribute to inspiratory drive in preBötzinger Complex neurons. J. Physiol. 586 (2008) 4531-4540
46. + regulation. J. Neurophysiol. 95 (2006) 1843-1852
47. Okada Y., Kuwana S., Kawai A., Mückenhoff K., and Scheid P. Significance of extracellular potassium in central respiratory control studied in the isolated brainstem-spinal cord preparation of the neonatal rat. Respir. Physiol. Neurobiol. 146 (2005) 21-32
48. Okada Y., Masumiya H., Tamura Y., and Oku Y. Respiratory and metabolic acidosis differentially affect the respiratory neuronal network in the ventral medulla of neonatal rats. Eur. J. Neurosci. 26 (2007) 2834-2843
49. 2 in the isolated brain stem-spinal cord of the neonatal rat. Respir. Physiol. 93 (1993) 315-326
50. Oku Y., Masumiya H., and Okada Y. Postnatal developmental changes in activation profiles of the respiratory neuronal network in the rat ventral medulla. J. Physiol. 585 (2007) 175-186
51. Oku Y., Okabe A., Hayakawa T., and Okada Y. Respiratory neuron group in the high cervical spinal cord discovered by optical imaging. Neuroreport 19 (2008) 1739-1743
52. Onimaru H., Arata A., Arata S., Shirasawa S., and Cleary M.L. In vitro visualization of respiratory neuron activity in the newborn mouse ventral medulla. Brain Res. Dev. Brain Res. 153 (2004) 275-279
53. 2+-dependent conductances to membrane potential fluctuations of medullary respiratory neurons of newborn rats in vitro. J. Physiol. 552 (2003) 727-741
54. Onimaru H., and Homma I. A novel functional neuron group for respiratory rhythm generation in the ventral medulla. J. Neurosci. 23 (2003) 1478-1486
55. Onimaru H., and Homma I. Optical imaging of respiratory neuron activity from the dorsal view of the lower brainstem. Clin. Exp. Pharmacol. Physiol. 32 (2005) 297-301
56. Onimaru H., and Homma I. Developmental changes in the spatio-temporal pattern of respiratory neuron activity in the medulla of late fetal rat. Neuroscience 131 (2005) 969-977
57. Onimaru H., and Homma I. Spontaneous oscillatory burst activity in the piriform-amygdala region and its relation to in vitro respiratory activity in newborn rats. Neuroscience 144 (2007) 387-394
58. 2-sensitive preinspiratory neurons of the parafacial respiratory group express Phox2b in the neonatal rat. J. Neurosci. 28 (2008) 12845-12850
59. Onimaru H., Kumagawa Y., and Homma I. Respiration-related rhythmic activity in the rostral medulla of newborn rats. J. Neurophysiol. 96 (2006) 55-61
60. Onimaru H., Kanamaru A., and Homma I. Optical imaging of respiratory burst activity in newborn rat medullary block preparations. Neurosci. Res. 25 (1996) 183-190
61. Pagliardini S., Adachi T., Ren J., Funk G.D., and Greer J.J. Fluorescent tagging of rhythmically active respiratory neurons within the pre-Bötzinger complex of rat medullary slice preparations. J. Neurosci. 25 (2005) 2591-2596
62. Pierani A., Moran-Rivard L., Sunshine M.J., Littman D.R., Goulding M., and Jessell T.M. Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29 (2001) 367-384
63. Potts J.T., and Paton J.F. Optical imaging of medullary ventral respiratory network during eupnea and gasping in situ. Eur. J. Neurosci. 23 (2006) 3025-3033
64. Putnam R.W. Intracellular pH regulation of neurons in chemosensitive and nonchemosensitive areas of brain slices. Respir. Physiol. 129 (2001) 37-56
65. Ritucci N.A., Erlichman J.S., Dean J.B., and Putnam R.W. A fluorescence technique to measure intracellular pH of single neurons in brainstem slices. J. Neurosci. Methods 68 (1996) 149-163
66. Ritucci N.A., Dean J.B., and Putnam R.W. Intracellular pH response to hypercapnia in neurons from chemosensitive areas of the medulla. Am. J. Physiol. Regul. Integr. Comp. Physiol. 273 (1997) R433-R441
67. Ruangkittisakul A., and Ballanyi K. Neuron-glia-imaging. In: Windhorst U., Binder M., and Hirokawa N. (Eds). Encyclopedic Reference of Neuroscience (2009), Springer Verlag, Heidelberg, New York, Tokyo part 18 2756-2764
68. +] of confocally-imaged respiratory centre neurons in online-calibrated newborn rat brainstem slices. J. Neurosci. 26 (2006) 11870-11880
69. Ruangkittisakul A., Schwarzacher S.W., Secchia L., Ma Y., Bobocea N., Poon B.Y., Funk G.D., and Ballanyi K. Generation of eupnea and sighs by a spatiochemically organized inspiratory network. J. Neurosci. 28 (2008) 2447-2458
70. Salama G., Choi B.R., Azour G., Lavasani M., Tumbev V., Salzberg B.M., Patrick M.J., Ernst L.A., and Waggoner A.S. Properties of new, long-wavelength, voltage-sensitive dyes in the heart. J. Membr. Biol. 208 (2005) 125-140
71. Smith J.C., Ellenberger H.H., Ballanyi K., Richter D.W., and Feldman J.L. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254 (1991) 726-729
72. Smith J.C., Greer J.J., Liu G.S., and Feldman J.L. Neural mechanisms generating respiratory pattern in mammalian brain stem-spinal cord in vitro. I. Spatiotemporal patterns of motor and medullary neuron activity. J. Neurophysiol. 64 (1990) 1149-1169
73. Sugama S., Shimokawa N., Okada J., and Miura M. In vitro study of H+-sensitive neurons in the ventral medullary surface of neonate rats. Brain Res. 777 (1997) 95-102
74. Szoke K., Härtel K., Grass D., Hirrlinger P.G., Hirrlinger J., and Hülsmann S. Glycine transporter 1 expression in the ventral respiratory group is restricted to protoplasmic astrocytes. Brain Res. 1119 (2006) 182-189
75. Thoby-Brisson M., Trinh J.B., Champagnat J., and Fortin G. Emergence of the pre-Bötzinger respiratory rhythm generator in the mouse embryo. J. Neurosci. 25 (2005) 4307-4318
76. Tokumasu M., Nakazono Y., Ide H., Akagawa K., and Onimaru H. Optical recording of spontaneous respiratory neuron activity in the rat brain stem. Jpn. J. Physiol. 51 (2001) 613-619
77. Tong C.K., Chen K., and Chesler M. Kinetics of activity-evoked pH transients and extracellular pH buffering in rat hippocampal slices. J. Neurophysiol. 95 (2006) 3686-3697
78. CO2 and pH and their role as chemo-stimulants in the isolated respiratory network of neonatal rats. J. Physiol. 499 (1997) 527-542
79. Völker A., Ballanyi K., and Richter D.W. Anoxic disturbance of the isolated respiratory network of neonatal rats. Exp. Brain Res. 103 (1995) 9-19
80. 2+, mitochondria and selective motoneuron vulnerability: implications for ALS. Trends Neurosci. 28 (2005) 494-500
81. Wiemann M., and Bingmann D. Ventrolateral neurons of medullary organotypic cultures: intracellular pH regulation and bioelectric activity. Respir. Physiol. 129 (2001) 57-70
82. Winter S.M., Hirrlinger J., Kirchhoff F., and Hülsmann S. Transgenic expression of fluorescent proteins in respiratory neurons. Respir. Physiol. Neurobiol. 159 (2007) 108-114
83. Winter, S.M., Fresemann, J., Schnell, C., Oku, Y., Hirrlinger, J., Hülsmann, S., 2009. Glycinergic interneurons are functionally integrated into the inspiratory network of mouse medullary slices. Eur. J. Physiol., (Pflüger's Arch), doi:10.1007/s00424-009-0647-1.
84. Yuste R., Konnerth A., and Masters B.R. Imaging in neuroscience and development, a laboratory manual. J. Biomed. Opt. 11 (2006) 19902