Learning to breathe: Habituation of Hering-Breuer inflation reflex emerges with postnatal brainstem maturation

Respiratory Physiology and Neurobiology

Volumn 195, Issue 1, 2014, Pages 44-49

  Dutschmann, Mathias ^a,b   Bautista, Tara G ^a   Mörschel, Michael ^b   Dick, Thomas E ^c  

^a FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^b Bernstein Center for Computational Neuroscience   (Germany)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brainstem; Hebbian plasticity; Postnatal development; Sensory processing

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN STEM; BRAINSTEM MATURATION; BREATHING MECHANICS; BREATHING PATTERN; BREATHING RATE; CONTROLLED STUDY; EXHALATION; FEEDBACK SYSTEM; FUNCTIONAL ASSESSMENT; HABITUATION; HERING BREUER REFLEX; JUVENILE ANIMAL; LUNG FUNCTION; LUNG FUNCTION TEST; LUNG INFLATION; LUNG INFLATION TEST; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; REPETITIVE TONIC VAGAL STIMULATION; STEREOTYPY; STIMULUS RESPONSE; VAGUS NERVE STIMULATION; ANIMAL; BREATHING; ELECTROSTIMULATION; GROWTH, DEVELOPMENT AND AGING; IN VITRO STUDY; LUNG; PHRENIC NERVE; PHYSIOLOGY; REFLEX; VAGUS NERVE;

ANIMALS; BRAIN STEM; ELECTRIC STIMULATION; EXHALATION; IN VITRO TECHNIQUES; LUNG; NEURONAL PLASTICITY; PHRENIC NERVE; RATS; REFLEX; RESPIRATION; VAGUS NERVE;

EID: 84896047659     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2014.02.009     Document Type: Article

References (44)

1. Bechbache R.R., Chow H.H., Duffin J., Orsini E.C. The effects of hypercapnia, hypoxia, exercise and anxiety on the pattern of breathing in man. J. Physiol. 1979, 293:285-300.
2. Berger A.J., Dick T.E. Connectivity of slowly adapting pulmonary stretch receptors with dorsal medullary respiratory neurons. J. Neurophysiol. 1987, 58:1259-1274.
3. Bianchi A.L., Denavit-Saubie M., Champagnat J. Central control of breathing in mammals: neuronal circuitry, membrane properties, and neurotransmitters. Physiol. Rev. 1995, 75:1-45.
4. Bonham A.C., Coles S.K., McCrimmon D.R. Pulmonary stretch receptor afferents activate excitatory amino receptors in the nucleus tractus solitarii in rat. J. Physiol. 1993, 464:725-745.
5. Bonham A.C., McCrimmon D.R. Neurones in a discrete region of the nucleus tractus solitarius are required for the Breuer-Hering reflex in rat. J. Physiol. 1990, 427:261-280.
6. Bradley G.W., von Euler C., Marttila I., Roos B. A model of the central and reflex inhibition of inspiration in the cat. Biol. Cybern. 1975, 19:105-116.
7. Breuer J. Die Selbststeurung der Athmung durch Nervus Vagus. Akad. Wiss. Wien (II) 1868, 58:909-937.
8. BuSha B.F., Stella M.H., Manning H.L., Leiter J.C. Termination of inspiration by phase-dependent respiratory vagal feedback in awake normal humans. J. Appl. Physiol. 2002, 93:903-910.
9. Clark F.J., von Euler C. On the regulation of depth and rate of breathing. J. Physiol. 1972, 222:267-295.
10. 2 inhalation in man, with special emphasis on expiration. J. Physiol. 1977, 272:613-632.
11. Duffin J., Mohan R.M., Vasiliou P., Stephenson R., Mahamed S. A model of the chemoreflex control of breathing in humans: model parameters measurement. Respir. Physiol. 2000, 120:13-26.
12. Dutschmann M., Dick T.E. Pontine mechanisms of respiratory control. Compr. Physiol. 2012, 2:2443-2469.
13. Dutschmann M., Morschel M., Rybak I.A., Dick T.E. Learning to breathe: control of the inspiratory-expiratory phase transition shifts from sensory- to central-dominated during postnatal development in rats. J. Physiol. 2009, 587:4931-4948.
14. Dutschmann M., Morschel M., Reuter J., Zhang W., Gestreau C., Stettner G.M., Kron M. Postnatal emergence of synaptic plasticity associated with dynamic adaptation of the respiratory motor pattern. Respir. Physiol. Neurobiol. 2008, 164:72-79.
15. Dutschmann M., Morschel M., Kron M., Herbert H. Development of adaptive behaviour of the respiratory network: implications for the pontine Kolliker-Fuse nucleus. Respir. Physiol. Neurobiol. 2004, 143:155-165.
16. von Euler C. The contribution of sensory inputs to the pattern generation of breathing. Can. J. Physiol. Pharmacol. 1981, 59:700-706.
17. von Euler C. On the central pattern generator for the basic breathing rhythmicity. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 1983, 55:1647-1659.
18. Ezure K., Tanaka I. GABA, in some cases together with glycine, is used as the inhibitory transmitter by pump cells in the Hering-Breuer reflex pathway of the rat. Neuroscience 2004, 127:409-417.
19. Fedorko L., Kelly E.N., England S.J. Importance of vagal afferents in determining ventilation in newborn rats. J. Appl. Physiol. 1988, 65:1033-1039.
20. Gerhardt T., Bancalari E. Maturational changes of reflexes influencing inspiratory timing in newborns. J. Appl. Physiol. 1981, 50:1282-1285.
21. Hering E. Die Selbststeurung der Athmung durch den Nervus Vagus. Akad. Wiss. Wien (II) 1868, 58:672-677.
22. Katz D.M., Dutschmann M., Ramirez J.M., Hilaire G. Breathing disorders in Rett syndrome: progressive neurochemical dysfunction in the respiratory network after birth. Respir. Physiol. Neurobiol. 2009, 168:101-108.
23. Kron M., Reuter J., Gerhardt E., Manzke T., Zhang W., Dutschmann M. Emergence of brain-derived neurotrophic factor-induced postsynaptic potentiation of NMDA currents during the postnatal maturation of the Kolliker-Fuse nucleus of rat. J. Physiol. 2008, 586:2331-2343.
24. Kubin L., Alheid G.F., Zuperku E.J., McCrimmon D.R. Central pathways of pulmonary and lower airway vagal afferents. J. Appl. Physiol. 2006, 101:618-627.
25. Liu Q., Wong-Riley M.T.T. Postnatal development of N-methyl-d-aspartate receptor subunits 2A, 2B, 2C, 2D and 3B immunoreactivity in brain stem respiratory nuclei of rat. Neuroscience 2010, 171:637-654.
26. MacDonald S.M., Tin C., Song G., Poon C.S. Use-dependent learning and memory of the Hering-Breuer inflation reflex in rats. Exp. Physiol. 2009, 94:269-278.
27. MacDonald S.M., Song G., Poon C.S. Nonassociative learning promotes respiratory entrainment to mechanical ventilation. PLoS ONE 2007, 2:e865.
28. Marckwald M. Die Athembewegungen und deren Innervation beim Kaninchen. Z. Biol. 1887, 23:149-283.
29. Miyazaki M., Arata A., Tanaka I., Ezure K. Activity of rat pump neurons is modulated with central respiratory rhythm. Neurosci. Lett. 1998, 249:61-64.
30. Miyazaki M., Tanaka I., Ezure K. Excitatory and inhibitory synaptic inputs shape the discharge pattern of pump neurons of the nucleus tractus solitarii in the rat. Exp. Brain Res. 1999, 129:191-200.
31. Phillipson E.A., Hickey R.F., Graf P.D., Nadel J.A. Hering-Breuer inflation reflex and regulation of breathing in conscious dogs. J. Appl. Physiol. 1971, 31:746-750.
32. Poon C.S. Organization of central pathways mediating the Hering-Breuer reflex and carotid chemoreflex. Adv. Exp. Med. Biol. 2004, 551:95-100.
33. Poon C.S., Zhou Z., Champagnat J. NMDA receptor activity in utero averts respiratory depression and anomalous long-term depression in newborn mice. J. Neurosci. 2000, 20:RC73.
34. Rabbette P.S., Costeloe K.L., Stocks J. Persistence of the Hering-Breuer reflex beyond the neonatal period. J. Appl. Physiol. 1991, 71:474-480.
35. Rabbette P.S., Stocks J. Influence of volume dependency and timing of airway occlusions on the Hering-Breuer reflex in infants. J. Appl. Physiol. 1998, 85:2033-2039.
36. Siniaia M.S., Young D.L., Poon C.S. Habituation and desensitization of the Hering-Breuer reflex in rat. J. Physiol. 2000, 523:479-491.
37. Song G., Poon C.S. Functional and structural models of pontine modulation of mechanoreceptor and chemoreceptor reflexes. Respir. Physiol. Neurobiol. 2004, 143:281-292.
38. Song G., Tin C., Giacometti E., Poon C.S. Habituation without NMDA receptor-dependent desensitization of Hering-Breuer apnea reflex in a Mecp2 mutant mouse model of Rett syndrome. Front. Integr. Neurosci. 2011, 5:6.
39. Stella G. On the mechanism of production and the physiological significance of apneusis. J. Physiol. 1938, 93:10-23.
40. St John W.M., Glasser R.L., King R.A. Rhythmic respiration in awake vagotomized cats with chronic pneumotaxic area lesions. Respir. Physiol. 1972, 15:233-244.
41. Stanley N.N., Altose M.D., Cherniack N.S., Fishman A.P. Changes in strength of lung inflation reflex during prolonged inflation. J. Appl. Physiol. 1975, 38:474-480.
42. -/y knockout mice. J. Physiol. 2007, 579:863-876.
43. Tadjalli A., Duffin J., Peever J. Identification of a novel form of noradrenergic-dependent respiratory motor plasticity triggered by vagal feedback. J. Neurosci. 2010, 30:16886-16895.
44. Trippenbach T. Pulmonary reflexes and control of breathing during development. Biol. Neonate 1994, 65:205-210.