Hypoglossal motoneurons in newborn mice receive respiratory drive from both sides of the medulla

Neuroscience

Volumn 161, Issue 1, 2009, Pages 259-268

  Tarras Wahlberg, S ^a   Rekling, J C ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

brainstem; dendrites; respiration; rhythm generation

Indexed keywords

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; HYPOGLOSSAL NERVE; IN VITRO STUDY; MOTONEURON; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RESPIRATION CENTER; RESPIRATORY DRIVE;

ANIMALS; ANIMALS, NEWBORN; AXONS; DENDRITES; HYPOGLOSSAL NERVE; MEDULLA OBLONGATA; MICE; MOTOR NEURONS; RESPIRATORY MECHANICS;

EID: 67349194947     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.02.064     Document Type: Article

References (60)

1. Altschuler S.M., Bao X., and Miselis R.R. Dendritic architecture of hypoglossal motoneurons projecting to extrinsic tongue musculature in the rat. J Comp Neurol 342 (1994) 538-550
2. Borke R.C., Nau M.E., and Ringler Jr. R.L. Brain stem afferents of hypoglossal neurons in the rat. Brain Res 269 (1983) 47-55
3. Boulenguez P., Gauthier P., and Kastner A. Respiratory neuron subpopulations and pathways potentially involved in the reactivation of phrenic motoneurons after C2 hemisection. Brain Res 1148 (2007) 96-104
4. Cameron W.E., Averill D.B., and Berger A.J. Morphology of cat phrenic motoneurons as revealed by intracellular injection of horseradish peroxidase. J Comp Neurol 219 (1983) 70-80
5. Chen Z., Travers S.P., and Travers J.B. Muscimol infusions in the brain stem reticular formation reversibly block ingestion in the awake rat. Am J Physiol Regul Integr Comp Physiol 280 (2001) R1085-R1094
6. Dobbins E.G., and Feldman J.L. Brainstem network controlling descending drive to phrenic motoneurons in rat. J Comp Neurol 347 (1994) 64-86
7. Dobbins E.G., and Feldman J.L. Differential innervation of protruder and retractor muscles of the tongue in rat. J Comp Neurol 357 (1995) 376-394
8. Duffin J., and Li Y.M. Transmission of respiratory rhythm: midline-crossing connections at the level of the phrenic motor nucleus?. Respir Physiol Neurobiol 153 (2006) 139-147
9. Ellenberger H.H., and Feldman J.L. Monosynaptic transmission of respiratory drive to phrenic motoneurons from brainstem bulbospinal neurons in rats. J Comp Neurol 269 (1988) 47-57
10. Ellenberger H.H., and Feldman J.L. Brainstem connections of the rostral ventral respiratory group of the rat. Brain Res 513 (1990) 35-42
11. Ellenberger H.H., Feldman J.L., and Goshgarian H.G. Ventral respiratory group projections to phrenic motoneurons: electron microscopic evidence for monosynaptic connections. J Comp Neurol 302 (1990) 707-714
12. Ezure K. Synaptic connections between medullary respiratory neurons and considerations on the genesis of respiratory rhythm. Prog Neurobiol 35 (1990) 429-450
13. Ezure K., and Tanaka I. Distribution and medullary projection of respiratory neurons in the dorsolateral pons of the rat. Neuroscience 141 (2006) 1011-1023
14. Feldman J. Neurophysiology of breathing in mammals. In: Bloom F.E. (Ed). Handbook of physiology. The nervous system. Intrinsic regulatory system in the brain (1986), Am Physiol Soc, Washington, DC 463-524
15. Feldman J.L., Loewy A.D., and Speck D.F. Projections from the ventral respiratory group to phrenic and intercostal motoneurons in cat: an autoradiographic study. J Neurosci 5 (1985) 1993-2000
16. Furrer M.P., Kim S., Wolf B., and Chiba A. Robo and frazzled/DCC mediate dendritic guidance at the CNS midline. Nat Neurosci 6 (2003) 223-230
17. Gaytan S.P., Calero F., Nunez-Abades P.A., Morillo A.M., and Pasaro R. Pontomedullary efferent projections of the ventral respiratory neuronal subsets of the rat. Brain Res Bull 42 (1997) 323-334
18. Gierke H. Die Theile der Medulla oblongata, deren Verlezung die Athembewegungen hemmt, und das Athemzentrum. Pflugers Arch 7 (1873) 583-600
19. Goshgarian H.G. The crossed phrenic phenomenon: a model for plasticity in the respiratory pathways following spinal cord injury. J Appl Physiol 94 (2003) 795-810
20. Goshgarian H.G., Ellenberger H.H., and Feldman J.L. Decussation of bulbospinal respiratory axons at the level of the phrenic nuclei in adult rats: a possible substrate for the crossed phrenic phenomenon. Exp Neurol 111 (1991) 135-139
21. Gromysz H., and Karczewski W.A. Respiratory activity generated by a split brainstem preparation of the rabbit. Acta Neurobiol Exp Wars 41 (1981) 237-242
22. Gromysz H., and Karczewski W.A. Phrenic motoneurone activity in split-brainstem cats and monkeys. Respir Physiol 50 (1982) 51-61
23. Hamam B.N., and Kennedy T.E. Visualization of the dendritic arbor of neurons in intact 500 microm thick brain slices. J Neurosci Methods 123 (2003) 61-67
24. Janczewski W.A., and Karczewski W.A. The role of neural connections crossed at the cervical level in determining rhythm and amplitude of respiration in cats and rabbits. Respir Physiol 79 (1990) 163-175
25. Johnson S.M., Koshiya N., and Smith J.C. Isolation of the kernel for respiratory rhythm generation in a novel preparation: the pre-Botzinger complex "island.". J Neurophysiol 85 (2001) 1772-1776
26. Kashiwagi M., Onimaru H., and Homma I. Correlation analysis of respiratory neuron activity in ventrolateral medulla of brainstem-spinal cord preparation isolated from newborn rat. Exp Brain Res 95 (1993) 277-290
27. Kim S., and Chiba A. Dendritic guidance. Trends Neurosci 27 (2004) 194-202
28. 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
29. Koshiya N., and Smith J.C. Neuronal pacemaker for breathing visualized in vitro. Nature 400 (1999) 360-363
30. Kubin L., Lipski J., and Trzebski A. Respiratory rhythmicity in a split medulla preparation of the cat. Exp Neurol 96 (1987) 720-726
31. Langendoff F.O., Nitschmann R., and Witzack H. Studien über die Innervation der Athembewegungen. Über Ungleichzeitige Thätigkeit beider Zwerchfellshälften. Arch Anat Physiol (Leipzig) Physiol Abt (1881) 78-89
32. Li Y.M., Shen L., Peever J.H., and Duffin J. Connections between respiratory neurones in the neonatal rat transverse medullary slice studied with cross-correlation. J Physiol 549 (2003) 327-332
33. Li Y.Q., Takada M., and Mizuno N. Identification of premotor interneurons which project bilaterally to the trigeminal motor, facial or hypoglossal nuclei: a fluorescent retrograde double-labeling study in the rat. Brain Res 611 (1993) 160-164
34. Li Y.Q., Takada M., and Mizuno N. Premotor neurons projecting simultaneously to two orofacial motor nuclei by sending their branched axons. A study with a fluorescent retrograde double-labeling technique in the rat. Neurosci Lett 152 (1993) 29-32
35. Lindsay A.D., Greer J.J., and Feldman J.L. Phrenic motoneuron morphology in the neonatal rat. J Comp Neurol 308 (1991) 169-179
36. Lipski J., Zhang X., Kruszewska B., and Kanjhan R. Morphological study of long axonal projections of ventral medullary inspiratory neurons in the rat. Brain Res 640 (1994) 171-184
37. Loeschcke H.H. Central chemosensitivity and the reaction theory. J Physiol 332 (1982) 1-24
38. Nunez-Abades P.A., He F., Barrionuevo G., and Cameron W.E. Morphology of developing rat genioglossal motoneurons studied in vitro: changes in length, branching pattern, and spatial distribution of dendrites. J Comp Neurol 339 (1994) 401-420
39. Onimaru H., Kashiwagi M., Arata A., and Homma I. Possible mutual excitatory couplings between inspiratory neurons in caudal ventrolateral medulla of brainstem-spinal cord preparation isolated from newborn rat. Neurosci Lett 150 (1993) 203-206
40. Ono T., Ishiwata Y., Inaba N., Kuroda T., and Nakamura Y. Hypoglossal premotor neurons with rhythmical inspiratory-related activity in the cat: localization and projection to the phrenic nucleus. Exp Brain Res 98 (1994) 1-12
41. Peever J.H., and Duffin J. Bilateral synchronisation of respiratory motor output in rats: adult versus neonatal in vitro preparations. Pflugers Arch 442 (2001) 943-951
42. Peever J.H., Shen L., and Duffin J. Respiratory pre-motor control of hypoglossal motoneurons in the rat. Neuroscience 110 (2002) 711-722
43. Peever J.H., Tian G.F., and Duffin J. Bilaterally independent respiratory rhythms in the decerebrate rat. Neurosci Lett 247 (1998) 41-44
44. Pena F., and Ramirez J.M. Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22 (2002) 11055-11064
45. Prakash Y.S., Mantilla C.B., Zhan W.Z., Smithson K.G., and Sieck G.C. Phrenic motoneuron morphology during rapid diaphragm muscle growth. J Appl Physiol 89 (2000) 563-572
46. Rekling J.C., and Feldman J.L. PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu Rev Physiol 60 (1998) 385-405
47. +] of confocally imaged respiratory center neurons in on-line-calibrated newborn rat brainstem slices. J Neurosci 26 (2006) 11870-11880
48. Schwarzacher S.W., Pestean A., Gunther S., and Ballanyi K. Serotonergic modulation of respiratory motoneurons and interneurons in brainstem slices of perinatal rats. Neuroscience 115 (2002) 1247-1259
49. Sebe J.Y., and Berger A.J. Inspiratory-phase short time scale synchrony in the brainstem slice is generated downstream of the pre-Botzinger complex. Neuroscience 153 4 (2008) 1390-1401
50. Segers L.S., Nuding S.C., Dick T.E., Shannon R., Baekey D.M., Solomon I.C., Morris K.F., and Lindsey B.G. Functional connectivity in the Pontomedullary Respiratory Network. J Neurophysiol 100 4 (2008) 1749-1769
51. Shen L., Peever J.H., and Duffin J. Bilateral coordination of inspiratory neurones in the rat. Pflugers Arch 443 (2002) 829-835
52. Song A., Ashwell K.W., and Tracey D.J. Development of the rat phrenic nucleus and its connections with brainstem respiratory nuclei. Anat Embryol 202 (2000) 159-177
53. Stornetta R.L., Rosin D.L., Wang H., Sevigny C.P., Weston M.C., and Guyenet P.G. A group of glutamatergic interneurons expressing high levels of both neurokinin-1 receptors and somatostatin identifies the region of the pre-Botzinger complex. J Comp Neurol 455 (2003) 499-512
54. Suli A., Mortimer N., Shepherd I., and Chien C.B. Netrin/DCC signaling controls contralateral dendrites of octavolateralis efferent neurons. J Neurosci 26 (2006) 13328-13337
55. Tan W., Janczewski W.A., Yang P., Shao X.M., Callaway E.M., and Feldman J.L. Silencing preBotzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat. Nat Neurosci 11 5 (2008) 538-540
56. Thoby-Brisson M., Trinh J.B., Champagnat J., and Fortin G. Emergence of the pre-Botzinger respiratory rhythm generator in the mouse embryo. J Neurosci 25 (2005) 4307-4318
57. Tian G.F., and Duffin J. Spinal connections of ventral-group bulbospinal inspiratory neurons studied with cross-correlation in the decerebrate rat. Exp Brain Res 111 (1996) 178-186
58. Travers J.B., and Norgren R. Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220 (1983) 280-298
59. Travers J.B., and Rinaman L. Identification of lingual motor control circuits using two strains of pseudorabies virus. Neuroscience 115 (2002) 1139-1151
60. Ye J.H., Zhang J., Xiao C., and Kong J.Q. Patch-clamp studies in the CNS illustrate a simple new method for obtaining viable neurons in rat brain slices: glycerol replacement of NaCl protects CNS neurons. J Neurosci Methods 158 (2006) 251-259