Descending control of the respiratory neuronal network by the midbrain periaqueductal grey in the rat in vivo

Journal of Physiology

Volumn 591, Issue 1, 2013, Pages 109-122

  Subramanian, Hari H ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN NERVE CELL; BREATHING PATTERN; CELL ACTIVATION; CELL ACTIVITY; CONTROLLED STUDY; FEEDBACK SYSTEM; FEMALE; IN VIVO STUDY; MALE; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; RESPIRATION CONTROL; RESPIRATORY DRIVE;

ANIMALS; FEMALE; HOMOCYSTEINE; MALE; NEURONS; PERIAQUEDUCTAL GRAY; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATION;

EID: 84872047243     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.245217     Document Type: Article

References (58)

1. Baker JP Jr & Remmers JE (1980). Temporal correlation of graded reversible inspiratory inhibition with discharge patterns of late inspiratory neurons located in the dorsal respiratory group in cats. Brain Res 200, 331-340.
2. Ballantyne D & Richter DW (1984). Post-synaptic inhibition of bulbar inspiratory neurones in the cat. J Physiol 348, 67-87.
3. Bandler R & Carrive P (1988). Integrated defence reaction elicited by excitatory amino acid microinjection in the midbrain periaqueductal grey region of the unrestrained cat. Brain Res 439, 95-106.
4. Basnayake SD, Hyam JA, Pereira EA, Schweder PM, Brittain JS, Aziz TZ, Green AL & Paterson DJ (2011). Identifying cardiovascular neurocircuitry involved in the exercise pressor reflex in humans using functional neurosurgery. J Appl Physiol 110, 881-891.
5. Bianchi AL, Denavit-Saubie M & Champagnat J (1995). Central control of breathing in mammals: neuroneal circuitry, membrane properties and neurotransmitters. Physiol Rev 75, 1-44.
6. Bianchi AL, Grélot L, Iscoe S & Remmers JE (1988). Electrophysiological properties of rostral medullary respiratory neurones in the cat: an intracellular study. J Physiol 407, 293-310.
7. Cohen MI (1979). Neurogenesis of respiratory rhythm in the mammal. Physiol Rev 59, 1105-1173.
8. Cohen MI & Feldman JL (1984). Discharge properties of dorsal medullary inspiratory neurons: relation to pulmonary afferent and phrenic efferent discharge. J Neurophysiol 51, 753-776.
9. Cohen MI, Huang WX, Barnhardt R & See WR (1993). Timing of medullary late-inspiratory neuron discharges: vagal afferent effects indicate possible off-switch function. J Neurophysiol 69, 1784-1787.
10. Duffin J (2004). Functional organization of respiratory neurones: a brief review of current questions and speculations. Exp Physiol 89, 517-529.
11. Dutschmann M & Herbert H (2006). The Kölliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. Eur J Neurosci 24, 1071-1084.
12. Dutschmann M, Mörschel M, Rybak IA & Dick TE (2009a). Learning to breathe: control of the inspiratory-expiratory phase transition shifts from sensory- to central-dominated during postnatal development in rats. J Physiol 587, 4931-4948.
13. Dutschmann M & Paton JF (2002). Glycinergic inhibition is essential for co-ordinating cranial and spinal respiratory motor outputs in the neonatal rat. J Physiol 543, 643-653.
14. Dutschmann M, Waki H, Manzke T, Simms AE, Pickering AE, Richter DW & Paton JF (2009b). The potency of different serotonergic agonists in counteracting opioid evoked cardiorespiratory disturbances. Philos Trans R Soc Lond B Biol Sci 364, 2611-2623.
15. Ezure K (1990). Synaptic connections between medullary respiratory neurones and considerations on the genesis of respiratory rhythm. Prog Neurobiol 35, 429-450.
16. Ezure K, Tanaka I & Oku Y (1993). Location and axonal projection of early-onset decrementing expiratory neurons in the cat. Neurosci Lett 163, 105-108.
17. Feldman JL & Cohen MI (1978). Relation between expiratory duration and rostral medullary expiratory neuronal discharge. Brain Res 141, 172-178.
18. Feldman JL & Del Negro CA (2006). Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7, 232-242.
19. Fries W & Zieglgansberger W (1974). A method to discriminate axonal from cell body activity and to analyse 'silent' cells. Exp Brain Res 21, 441-445.
20. Goodchild AK, Dampney RAL & Bandler R (1982). A method for evoking physiological responses by stimulation of cell bodies, but not axons of passage, within localized regions of the central nervous system. J Neurosci Meth 6, 351-363.
21. Haji A, Okazaki M, Yamazaki H & Takeda R (2002). Physiological properties of late inspiratory neurons and their possible involvement in inspiratory off-switching in cats. J Neurophysiol 87, 1057-1067.
22. Hayashi F, Coles SK & McCrimmon DR (1996). Respiratory neurons mediating the Breuer-Hering reflex prolongation of expiration in rat. J Neurosci 16, 6526-6536.
23. Hayward LF, Castellanos M & Davenport P (2004). Parabrachial neurons mediate dorsal periaqueductal grey evoked respiratory responses in the rat. J Appl Physiol 96, 1146-1154.
24. Holstege G (1991). Descending pathways from the periaqueductal grey and adjacent areas. In The Midbrain Periaqueductal Gray Matter: Functional Anatomical and Immunohistochemical Organization, ed. Depaulis A & Bandler R, pp. 239-265. Plenum Press, New York.
25. Kubin L, Alheid GF, Zuperku EJ & McCrimmon DR (2006). Central pathways of pulmonary and lower airway vagal afferents. J Appl Physiol 101, 618-627.
26. Lindsey BG, Segers LS & Shannon R (1989). Discharge patterns of rostrolateral medullary expiratory neurons in the cat: regulation by concurrent network processes. J Neurophysiol 61, 1185-1196.
27. Lipski J, Bellingham MC, West MJ & Pilowsky P (1988). Limitations of the technique of pressure microinjection of excitatory amino acids for evoking responses from localized regions of the CNS. J Neurosci Methods 26, 169-179.
28. Long S & Duffin J (1986). Neuronal determinants of respiratory rhythm. Prog Neurobiol 27, 101-182.
29. Lovick TA. 2000. Panic disorder: a malfunction of multiple transmitter control systems with the midbrain periaqueductal grey matter. Neuroscientist 6, 48-59.
30. Manabe M & Ezure K (1988). Decrementing expiratory neurons of the Bötzinger complex. I. Response to lung inflation and axonal projection. Exp Brain Res 72, 150-158.
31. Manzke T, Dutschmann M, Schlaf G, Mörschel M, Koch UR, Ponimaskin E, Bidon O, Lalley PM & Richter DW (2009). Serotonin targets inhibitory synapses to induce modulation of network functions. Philos Trans R Soc Lond B Biol Sci 364, 2589-2602.
32. Manzke T, Niebert M, Koch UR, Caley A, Vogelgesang S, Hülsmann S, Ponimaskin E, Müller U, Smart TG, Harvey RJ & Richter DW (2010). Serotonin receptor 1A-modulated phosphorylation of glycine receptor α3 controls breathing in mice. J Clin Invest 120, 4118-4128.
33. Merrill EG (1970). The lateral respiratory neurons of the medulla: their associations with NA, NRA and the spinal accessory nucleus and the spinal cord. Brain Res 24, 11-28.
34. Merrill EG (1974). Finding a respiratory function for the medullary respiratory neurons. In Essays on the Nervous System, ed. Bellairs R & Gray EG, 451-486. Clarendon Press, Oxford.
35. Morris KF, Nuding SC, Segers LS, Baekey DM, Shannon R, Lindsey BG & Dick TE (2010). Respiratory and Mayer wave-related discharge patterns of raphé and pontine neurons change with vagotomy. J Appl Physiol 109, 189-202.
36. Mörschel M & Dutschmann M (2009). Pontine respiratory activity involved in inspiratory/expiratory phase transition. Philos Trans R Soc Lond B Biol Sci 364, 2517-2526.
37. Nuding SC, Segers LS, Shannon R, O'Connor R, Morris KF & Lindsey BG (2009). Central and peripheral chemoreceptors evoke distinct responses in simultaneously recorded neurons of the raphé-pontomedullary respiratory network. Philos Trans R Soc Lond B Biol Sci 364, 2501-2516.
38. Paton JFR (1996). The ventral medullary respiratory network of the mature mouse studied in a working heart-brainstem preparation. J Physiol 493, 819-831.
39. Paxinos G & Watson C (1997). The Rat Brain in Stereotaxic Co-Ordinates. Academic Press, San Diego, CA.
40. Pierrefiche O, Haji A, Foutz AS, Takeda R, Champagnat J & Denavit-Saubie M (1998). Synaptic potentials in respiratory neurones during evoked phase switching after NMDA receptor blockade in the cat. J Physiol 508, 549-559.
41. Richter DW (1982). Generation and maintenance of respiratory rhythm. J Exp Biol 100, 93-107.
42. Richter DW, Ballantyne D & Remmers JE (1987). The differential organization of medullary post-inspiratory activities. Pflugers Arch 410, 420-427.
43. Rybak IA, Paton JF & Schwaber JS (1997). Modeling neural mechanisms for genesis of respiratory rhythm and pattern. II. Network models of the central respiratory pattern generator. J Neurophysiol 77, 2007-2026.
44. Rybak IA, Shevtsova NA, Paton JF, Dick TE, St-John WM, Mörschel M & Dutschmann M (2004). Modeling the ponto-medullary respiratory network. Respir Physiol Neurobiol 143, 307-319.
45. Shannon R, Baekey DM, Morris KF, Li Z & Lindsey BG (2000). Functional connectivity among ventrolateral medullary respiratory neurones and responses during fictive cough in the cat. J Physiol 525, 207-224.
46. Shen L, Li YM & Duffin J (2003). Inhibitory connections among rostral medullary expiratory neurones detected with cross-correlation in the decerebrate rat. Pflugers Arch 446, 365-372.
47. Shevtsova NA, Manzke T, Molkov YI, Bischoff A, Smith JC, Rybak IA & Richter DW. (2011). Computational modelling of 5-HT receptor-mediated reorganization of the brainstem respiratory network. Eur J Neurosci 34, 1276-1291.
48. Siniaia MS, Young DL & Poon CS (2000). Habituation and desensitization of the Hering-Breuer reflex in rat. J Physiol 523, 479-491.
49. Smith JC, Abdala AP, Koizumi H, Rybak IA & Paton JF (2007). Spatial and functional architecture of the mammalian brain stem respiratory network: a hierarchy of three oscillatory mechanisms. J Neurophysiol 98, 3370-3387.
50. Subramanian HH, Balnave RJ & Holstege G (2008). The midbrain periaqueductal grey control of respiration. J Neurosci 28, 12274-12283.
51. Subramanian HH & Holstege G (2009). The nucleus retroambiguus control of respiration. J Neurosci 29, 3824-3832.
52. Subramanian HH & Holstege G (2010). Periaqueductal grey control of breathing. Adv Exp Med Biol 669, 353-358.
53. Subramanian HH & Holstege G (2011). Midbrain and medullary control of postinspiratory activity of the crural and costal diaphragm in vivo. J Neurophysiol 105, 2852-2862.
54. von Euler C (1983). On the central pattern generator for the basic breathing rhythmicity. J Appl Physiol 55, 1647-1659.
55. Zhang SP, Bandler R & Carrive P (1990). Flight and immobility evoked by excitatory amino acid microinjection within distinct parts of the subtentorial midbrain periaqueductal grey of the cat. Brain Res 520, 73-82.
56. Zhang SP, Davis PJ, Bandler R & Carrive P (1994). Brain stem integration of vocalization: role of the midbrain periaqueductal grey. J Neurophysiol 72, 1337-1356.
57. Zheng Y, Barillot JC & Bianchi AL (1991a). Patterns of membrane potentials and distributions of the medullary respiratory neurons in the decerebrate rat. Brain Res 546, 261-270.
58. Zheng Y, Barillot JC & Bianchi AL (1991b). Are the post-inspiratory neurons in the decerebrate rat cranial motoneurons or interneurons Brain Res 551, 256-266.