Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2016, Article ID 3905257, 10 pages
http://dx.doi.org/10.1155/2016/3905257
Research Article

Mechanisms Underlying Adaptation of Respiratory Network Activity to Modulatory Stimuli in the Mouse Embryo

Institut de Neurosciences Cognitives et Intégratives d’Aquitaine, CNRS UMR 5287, Université de Bordeaux, 33076 Bordeaux, France

Received 26 February 2016; Accepted 11 April 2016

Academic Editor: Mathias Dutschmann

Copyright © 2016 Marc Chevalier et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. A. Gray, W. A. Janczewski, N. Mellen, D. R. McCrimmon, and J. L. Feldman, “Normal breathing requires preBötzinger complex neurokinin-1 receptor-expressing neurons,” Nature Neuroscience, vol. 4, no. 9, pp. 927–930, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. L. C. McKay, W. A. Janczewski, and J. L. Feldman, “Sleep-disordered breathing after targeted ablation of preBötzinger complex neurons,” Nature Neuroscience, vol. 8, no. 9, pp. 1142–1144, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. J. M. Ramirez, S. W. Schwarzacher, O. Pierrefiche, B. M. Olivera, and D. W. Richter, “Selective lesioning of the cat pre-Botzinger complex in vivo eliminates breathing but not gasping,” Journal of Physiology, vol. 507, no. 3, pp. 895–907, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. J. C. Smith, H. H. Ellenberger, K. Ballanyi, D. W. Richter, and J. L. Feldman, “Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals,” Science, vol. 254, no. 5032, pp. 726–729, 1991. View at Publisher · View at Google Scholar · View at Scopus
  5. W. Tan, W. A. Janczewski, P. Yang, X. M. Shao, E. M. Callaway, and J. L. Feldman, “Silencing preBotzinger complex somatostatin-expressing neurons induces persistent apnea in awake rat,” Nature Neuroscience, vol. 11, no. 5, pp. 538–540, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. N. Koshiya and J. C. Smith, “Neuronal pacemaker for breathing visualized in vitro,” Nature, vol. 400, no. 6742, pp. 360–363, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. J. F. R. Paton, A. P. L. Abdala, H. Koizumi, J. C. Smith, and W. M. St-John, “Respiratory rhythm generation during gasping depends on persistent sodium current,” Nature Neuroscience, vol. 9, no. 3, pp. 311–313, 2006. View at Publisher · View at Google Scholar · View at Scopus
  8. F. Peña, M. A. Parkis, A. K. Tryba, and J.-M. Ramirez, “Differential contribution of pacemaker properties to the generation of respiratory rhythms during normoxia and hypoxia,” Neuron, vol. 43, no. 1, pp. 105–117, 2004. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Thoby-Brisson and J.-M. Ramirez, “Identification of two types of inspiratory pacemaker neurons in the isolated respiratory neural network of mice,” Journal of Neurophysiology, vol. 86, no. 1, pp. 104–112, 2001. View at Google Scholar · View at Scopus
  10. A. Doi and J.-M. Ramirez, “Neuromodulation and the orchestration of the respiratory rhythm,” Respiratory Physiology and Neurobiology, vol. 164, no. 1-2, pp. 96–104, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. P. A. Gray, J. C. Rekling, C. M. Bocchiaro, and J. L. Feldman, “Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBotzinger complex,” Science, vol. 286, no. 5444, pp. 1566–1568, 1999. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Peña and J.-M. Ramirez, “Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro,” Journal of Neuroscience, vol. 22, no. 24, pp. 11055–11064, 2002. View at Google Scholar · View at Scopus
  13. F. Peña and J.-M. Ramirez, “Substance P-mediated modulation of pacemaker properties in the mammalian respiratory network,” The Journal of Neuroscience, vol. 24, no. 34, pp. 7549–7556, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. X. M. Shao and J. L. Feldman, “Acetylcholine modulates respiratory pattern: effects mediated by M3-like receptors in preBotzinger complex inspiratory neurons,” Journal of Neurophysiology, vol. 83, no. 3, pp. 1243–1252, 2000. View at Google Scholar · View at Scopus
  15. A. K. Tryba, F. Peña, S. P. Lieske, J.-C. Viemari, M. Thoby-Brisson, and J.-M. Ramirez, “Differential modulation of neural network and pacemaker activity underlying eupnea and sigh-breathing activities,” The Journal of Neurophysiology, vol. 99, no. 5, pp. 2114–2125, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. J.-C. Viemari and J.-M. Ramirez, “Norepinephrine differentially modulates different types of respiratory pacemaker and nonpacemaker neurons,” Journal of Neurophysiology, vol. 95, no. 4, pp. 2070–2082, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Thoby-Brisson, B. Cauli, J. Champagnat, G. Fortin, and D. M. Katz, “Expression of functional Tyrosine kinase B receptors by rhythmically active respiratory neurons in the pre-Bötzinger complex of neonatal mice,” The Journal of Neuroscience, vol. 23, no. 20, pp. 7685–7689, 2003. View at Google Scholar · View at Scopus
  18. P. Li, W. A. Janczewski, K. Yackle et al., “The peptidergic control circuit for sighing,” Nature, vol. 530, no. 7590, pp. 293–297, 2016. View at Publisher · View at Google Scholar
  19. M. Thoby-Brisson, J.-B. Trinh, J. Champagnat, and G. Fortin, “Emergence of the pre-Bötzinger respiratory rhythm generator in the mouse embryo,” The Journal of Neuroscience, vol. 25, no. 17, pp. 4307–4318, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. J. Bouvier, M. Thoby-Brisson, N. Renier et al., “Hindbrain interneurons and axon guidance signaling critical for breathing,” Nature Neuroscience, vol. 13, no. 9, pp. 1066–1074, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Pagliardini, J. Ren, and J. J. Greer, “Ontogeny of the pre-Botzinger complex in perinatal rats,” Journal of Neuroscience, vol. 23, no. 29, pp. 9575–9584, 2003. View at Google Scholar · View at Scopus
  22. J. Bouvier, S. Autran, N. Dehorter et al., “Brain-derived neurotrophic factor enhances fetal respiratory rhythm frequency in the mouse preBötzinger complex in vitro,” European Journal of Neuroscience, vol. 28, no. 3, pp. 510–520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. N. M. Mellen and C.-M. Tuong, “Semi-automated region of interest generation for the analysis of optically recorded neuronal activity,” NeuroImage, vol. 47, no. 4, pp. 1331–1340, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. A. K. Tryba and J.-M. Ramirez, “Hyperthermia modulates respiratory pacemaker bursting properties,” Journal of Neurophysiology, vol. 92, no. 5, pp. 2844–2852, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Ptak, T. Yamanishi, J. Aungst et al., “Raphe neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P,” The Journal of Neuroscience, vol. 29, no. 12, pp. 3720–3737, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. W. Tan, S. Pagliardini, P. Yang, W. A. Janczewski, and J. L. Feldman, “Projections of preBotzinger complex neurons in adult rats,” The Journal of Comparative Neurology, vol. 518, no. 10, pp. 1862–1878, 2010. View at Publisher · View at Google Scholar
  27. N. M. Mellen, W. A. Janczewski, C. M. Bocchiaro, and J. L. Feldman, “Opioid-induced quantal slowing reveals dual networks for respiratory rhythm generation,” Neuron, vol. 37, no. 5, pp. 821–826, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Thoby-Brisson, M. Karlén, N. Wu, P. Charnay, J. Champagnat, and G. Fortin, “Genetic identification of an embryonic parafacial oscillator coupling to the preBötzinger complex,” Nature Neuroscience, vol. 12, no. 8, pp. 1028–1035, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. W. A. Janczewski, H. Onimura, I. Homma, and J. L. Feldman, “Opioid-resistant respiratory pathway from the preinspiratory neurones to abdominal muscles: in vivo and in vitro study in the newborn rat,” The Journal of Physiology, vol. 545, part 3, pp. 1017–1026, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Takeda, L. I. Eriksson, Y. Yamamoto, H. Joensen, H. Onimaru, and S. G. Lindahl, “Opioid action on respiratory neuron activity of the isolated respiratory network in newborn rats,” Anesthesiology, vol. 95, no. 3, pp. 740–749, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. A. H. Jansen and V. Chernick, “Development of respiratory control,” Physiological Reviews, vol. 63, no. 2, pp. 437–483, 1983. View at Google Scholar · View at Scopus
  32. M. M. Grunstein, T. A. Hazinski, and M. A. Schlueter, “Respiratory control during hypoxia in newborn rabbits: implied action of endorphins,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 51, no. 1, pp. 122–130, 1981. View at Google Scholar · View at Scopus
  33. T. A. Hazinski, M. M. Grunstein, M. A. Schlueter, and W. H. Tooley, “Effect of naloxone on ventilation in newborn rabbits,” Journal of Applied Physiology: Respiratory, Environmental and Exercise Physiology, vol. 50, no. 4, pp. 713–717, 1981. View at Google Scholar
  34. J. D. Kelty, P. A. Noseworthy, M. E. Feder, R. M. Robertson, and J.-M. Ramirez, “Thermal preconditioning and heat-shock protein 72 preserve synaptic transmission during thermal stress,” The Journal of Neuroscience, vol. 22, no. 1, Article ID RC193, 2002. View at Google Scholar · View at Scopus
  35. A. K. Tryba and J.-M. Ramirez, “Response of the respiratory network of mice to hyperthermia,” Journal of Neurophysiology, vol. 89, no. 6, pp. 2975–2983, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. S. F. Morrison and K. Nakamura, “Central neural pathways for thermoregulation,” Frontiers in Bioscience, vol. 16, no. 1, pp. 74–104, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. A. G. Boden, M. C. Harris, and M. J. Parkes, “The preoptic area in the hypothalamus is the source of the additional respiratory drive at raised body temperature in anaesthetised rats,” Experimental Physiology, vol. 85, no. 5, pp. 527–537, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. J. C. Clapham, “Central control of thermogenesis,” Neuropharmacology, vol. 63, no. 1, pp. 111–123, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Matsuishi, S. Nagamitsu, Y. Yamashita et al., “Decreased cerebrospinal fluid levels of substance P in patients with Rett syndrome,” Annals of Neurology, vol. 42, no. 6, pp. 978–981, 1997. View at Publisher · View at Google Scholar · View at Scopus
  40. D. S. Paterson, F. L. Trachtenberg, E. G. Thompson et al., “Multiple serotonergic brainstem abnormalities in sudden infant death syndrome,” The Journal of the American Medical Association, vol. 296, no. 17, pp. 2124–2132, 2006. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Matsuishi, Y. Yamashita, T. Takahashi, and S. Nagamitsu, “Rett syndrome: the state of clinical and basic research, and future perspectives,” Brain and Development, vol. 33, no. 8, pp. 627–631, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. K. Waters, “Serotonin in the sudden infant death syndrome,” Drug News and Perspectives, vol. 23, no. 9, pp. 537–548, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Åkefeldt, R. Ekman, C. Gillberg, and J.-E. Månsson, “Cerebrospinal fluid monoamines in Prader-Willi syndrome,” Biological Psychiatry, vol. 44, no. 12, pp. 1321–1328, 1998. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Zanella, F. Watrin, S. Mebarek et al., “Necdin plays a role in the serotonergic modulation of the mouse respiratory network: implication for Prader-Willi syndrome,” The Journal of Neuroscience, vol. 28, no. 7, pp. 1745–1755, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Zanella, M. Barthelemy, F. Muscatelli, and G. Hilaire, “Necdin gene, respiratory disturbances and prader-willi syndrome,” Advances in Experimental Medicine and Biology, vol. 605, pp. 159–164, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. M. J. Russell and R. Vink, “Increased facial temperature as an early warning in Sudden Infant Death Syndrome,” Medical Hypotheses, vol. 57, no. 1, pp. 61–63, 2001. View at Publisher · View at Google Scholar · View at Scopus