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Canadian Association of Neuroscience Review: Respiratory Control and Behavior in Humans: Lessons from Imaging and Experiments of Nature

Published online by Cambridge University Press:  02 December 2014

Immanuela Ravé Moss
Immanuela Ravé Moss*
Affiliation:
Departments of Pediatrics and Physiology, McGill University and McGill University Health Centre Research Institute, Montreal Children's Hospital and Montreal Children's Hospital Research Institute, Montreal, Quebec, Canada
*
Departments of Pediatrics and Physiology, McGill University. The Montreal Children’s Hospital, Room A-707, 2300 Tupper Street. Montreal, QC H3H 1P3 Canada.
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Abstract:

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The purpose of this review is to demonstrate that respiration is a complex behavior comprising both brainstem autonomic control and supramedullary influences, including volition. Whereas some fundamental mechanisms had to be established using animal models, this review focuses on clinical cases and physiological studies in humans to illustrate normal and abnormal respiratory behavior. To summarize, central respiratory drive is generated in the rostroventrolateral medulla, and transmitted to both the upper airway and to the main and accessory respiratory muscles. Afferent feedback is provided from lung and muscle mechnoreceptors, peripheral carotid and aortic chemoreceptors, and multiple central chemoreceptors. Supramedullary regions, including cortex and subcortex, modulate or initiate breathing with volition, emotion and at the onset of exercise. Autonomic breathing control can be perturbed by brainstem pathology including space occupying lesions, compression, congenital central hypoventilation syndrome and sudden infant death syndrome. Sleep-wake states are important in regulating breathing. Thus, respiratory control abnormalities are most often evident during sleep, or during transition from sleep to wakefulness. Previously undiagnosed structural brainstem pathology may be revealed by abnormal breathing during sleep. Ondine's curse and 'the locked-in syndrome' serve to distinguish brainstem from supramedullary regulatory mechanisms in humans: The former comprises loss of autonomic respiratory control and requires volitional breathing for survival, and the latter entails loss of corticospinal or corticobulbar tracts required for volitional breathing, but preserves autonomic respiratory control.

Résumé:

RÉSUMÉ:

Le but de cette revue est de démontrer que la respiration est un acte complexe impliquant un contrôle neuro-végétatif provenant du tronc cérébral et des influences supramédullaires, entre autres la volonté. Alors que les mécanismes fondamentaux ont dû être établis grâce à des modèles animaux, cette revue est axée sur des cas cliniques et des études physiologiques chez l’humain afin d’illustrer le comportement respiratoire normal et anormal. En résumé, la stimulation respiratoire centrale origine de la moelle rostro-ventro-latérale et elle est transmise aux voies aériennes supérieures et aux muscles respiratoires principaux et accessoires. La rétroaction afférente provient de mécanorécepteurs pulmonaires et musculaires, de chémorécepteurs périphériques à la carotide et à l’aorte et de multiples chémorécepteurs centraux. Des régions supramédullaires corticales et sous-corticales jouent un rôle dans la modulation ou le déclenchement de la respiration par la volonté, l’émotion et en début d’exercice. Le contrôle neuro-végétatif de la respiration peut être perturbé par une pathologie du tronc cérébral, soit par une lésion expansive, une compression, le syndrome congénital d’hypoventilation alvéolaire central et le syndrome de la mort subite du nourrisson. Les états de sommeil et d’éveil sont importants dans la régelation de la respiration. Des anomalies du contrôle respiratoire sont plus souvent évidentes pendant le sommeil ou pendant la période de transition du sommeil à l’éveil. Une respiration anormale pendant le sommeil peut révéler une pathologie structurale du tronc cérébral encore non détectée. Le syndrome d’Ondine et le syndrome de déefférentation motrice (locked-in syndrome) distinguent les mécanismes régulateurs du tronc cérébral des mécanismes supramédullaires chez l’humain: les premiers comportent une perte du contrôle respiratoire neuro-végétatif et la survie dépend alors de la respiration volontaire et les derniers impliquent la perte des voies corticospinales ou corticobulbaires nécessaires à la respiration volontaire, mais préservent le contrôle respiratoire neurovégétatif.

Type
Review Article
Information
Canadian Journal of Neurological Sciences , Volume 32 , Issue 3 , August 2005 , pp. 287 - 297
Copyright
Copyright © The Canadian Journal of Neurological 2005

References

1. Feldman, JL, Smith, JC. Neural control of respiratory pattern inmammals: an overview. In: Dempsey, JA, Pack, AI, (Eds). Regulation of Breathing, Lung Biology in Health and Disease, Vol 79. New York: Marcel Dekker, 1995: 39–69.Google Scholar
2. Feldman, JL, Mitchell, GS, Nattie, EE. Breathing: rhythmicity,plasticity, chemosensitivity. Annu Rev Neurosci 2003; 26: 239–266.Google Scholar
3. Allen, AM, Chai, SY, Sexton, SY, et al. Angiotensin II receptors andangiotensin converting enzyme in the medulla oblongata. Hypertension 1987; 9 (Suppl II): 198–205.CrossRefGoogle ScholarPubMed
4. Allen, AM, Chai, SY, Clevers, J, et al. Localization andcharacterization of angiotensin II receptor binding and angiotensin converting enzyme in the human medulla oblongata. J Comp Neurol 1988; 269: 249–264.Google Scholar
5. Feldman, JL, McCrimmon, DR. Neural control of breathing. In: Squire, LR, Bloom, FE, McConnell, SK, Roberts, JL, Spitzer, NC, Zigmond, MJ, (Eds). Fundamental Neuroscience. Amsterdam: Academic Press, 2003: 967–990.Google Scholar
6. Gottesmann, C. Brain inhibitory mechanisms involved in basic andhigher integrated sleep processes. Brain Res. Brain Res Rev 2004; 45: 230–249.Google Scholar
7. Davenport, PW, Reep, RL. Cerebral cortex and respiration. In: Dempsey, JA, Pack, AI, Regulation of Respiration. Lung Biology in Health and Disease, Vol 79. New York: Marcel Dekker, 1995: 365–388.Google Scholar
8. Plum, F, Leigh, RJ. Abnormalities of central mechanisms. In: Hornbein, TF, (Ed). Regulation of Breathing. New York: Marcel Dekker, 1981: 989–1067.Google Scholar
9. Morrell, MJ, Heywood, P, Moosavi, SH, et al. Unilateral focal lesionsin the rostrolateral medulla influence chemosensitivity and breathing measured during wakefulness, sleep, and exercise. J Neurol Neurosurg Psychiat 1999; 67: 637–645.Google Scholar
10. Morrell, MJ, Heywood, P, Moosavi, SH, et al. Centralchemosensitivity and breathing asleep in unilateral medullary lesions patients: comparisons to animal data. Respir Physiol 2001; 129: 269–277.Google Scholar
11. Straus, C, Locher, C, Zelter, M, et al. Facilitation of the diaphragmresponse to transcranial magnetic stimulation by increases in human respiratory drive. J Appl Physiol 2004; 97: 902–912.Google Scholar
12. Macey, PM, Henderson, LA, Macey, KE, et al. Brain morphologyassociated with obstructive sleep apnea. Am J Respir Crit Care Med 2002; 166: 1382–1387.Google Scholar
13. Morrell, MJ, McRobbie, DW, Quest, RA, et al. Changes in brainmorphology associated with obstructive sleep apnea. Sleep Med 2003; 4: 451–454.Google Scholar
14. Rosen, GM, Bendel, AE, Neglia, JP, et al. Sleep in children withneoplasms of the central nervous system: case review of 14 children. Pediatrics 2003; 112: e46-e54.CrossRefGoogle ScholarPubMed
15. Rhodes, RH, Wightman, HR. Nucleus of the tractus solitariusmetastasis: relationship to respiratory arrest? Can J Neurol Sci 2000; 27: 328–332.Google Scholar
16. Corne, S, Webster, K, McGinn, G, et al. Medullary metastasis causingimpairment of respiratory pressure output with intact respiratory rhythm. Am J Respir Crit Care Med 1999; 159: 315–320.Google Scholar
17. Aryanpur, J, Hurko, O, Francomano, C, et al. Craniocervicaldecompression for cervicomedullary compression in pediatric patients with achondroplasia. J Neurosurg 1990; 73: 375–382.Google Scholar
18. Waters, KA, Forbes, P, Morielli, A, et al. Sleep-disordered breathingin children with myelomeningocele. J Pediatr 1998; 132: 672–681.Google Scholar
19. Gozal, D. New concepts in abnormalities of respiratory control inchildren. Curr Opin Pediatr 2004; 16: 305–308.Google Scholar
20. Vanderlaan, M, Holbrook, CR, Wang, M, et al. Epidemiologic survey of 196 patients with congenital central hypoventilation syndrome. Pediatr Pulmonol 2004; 37: 217–229.Google Scholar
21. Weese-Mayer, DE, Berry-Kravis, EM, Zhu, L, et al. Idiopathiccongenital central hypoventilation syndrome: analysis of genes pertinent to early autonomic nervous system embryologic development and identification of mutations in PHOX2b. Am J Med Gen 2003; 123A: 267–278.CrossRefGoogle Scholar
22. Sritippayawan, S, Hamutcu, R, Kun, SS, et al. Mother-daughtertransmission of congenital central hypoventilation syndrome. Am J Respir Crit Care Med 2002; 166: 367–369.CrossRefGoogle ScholarPubMed
23. Siegel, J. Brain mechanisms that control sleep and waking. Naturwissenschaften 2004; 91: 355–365.CrossRefGoogle ScholarPubMed
24. Villablanca, JR. Counterpointing the functional role of the forebrainand of the brainstem in the control of the sleep-waking system. J Sleep Res 2004; 13: 179–208.CrossRefGoogle Scholar
25. Collop, NA, Shepard, JW, Strollo, PJ. Executive summary on thesystematic review and practice parameters for portable monitoring in the investigation of suspected sleep apnea in adults. Am J Respir Crit Care Med 2004; 169: 1160–1163.Google Scholar
26. Nixon, GM, Kermack, AS, Davis, GM, et al. Planningadenotonsillectomy in children with obstructive sleep apnea: the role of overnight oximetry. Pediatrics 2004; 113: e19-e25.Google Scholar
27. O’Brien, LM, Mervis, CB, Holbrook, CR, et al. Neurobehavioralcorrelates of sleep-disordered breathing in children. J Sleep Res 2004; 13: 165–172.CrossRefGoogle ScholarPubMed
28. Parish, JM, Somers, VK. Obstructive sleep apnea and cardiovasculardisease. Mayo Clinic Proc 2004; 79: 1036–1046.Google Scholar
29. Arens, R, Marcus, CL. Pathophysiology of upper airway obstruction: a developmental perspective. Sleep 2004; 27: 997–1019.CrossRefGoogle ScholarPubMed
30. Lipton, AJ, Gozal, D. Treatment of obstructive sleep apnea inchildren: do we really know how? Sleep Med Rev 2003; 7: 61–80.Google Scholar
31. Hamilton, GS, Solin, P, Naughton, MT. Obstructive sleep apnoea andcardiovascular disease. Intern Med J 2004; 34: 420–426.Google Scholar
32. Schechter, MS. Technical report: diagnosis and management ofchildhood obstructive sleep apnea syndrome. Pediatrics 2002; 109: e69(1-20).CrossRefGoogle Scholar
33. Hunt, CE. Genes and sudden Infant death syndrome. Pediatr Res 2004; 56: 321–322.Google Scholar
34. Sparks, DL, Hunsaker, JC III. Neuropathology of sudden infant death(syndrome): literature review and evidence of a probable apoptotic degenerative disease. Childs Nerv Syst 2002; 18: 568–592.Google Scholar
35. Ramsay, SC, Adams, L, Murphy, K, et al. Regional cerebral bloodflow during volitional expiration in man: a comparison with volitional inspiration. J Physiol 1993; 461: 85–101.Google Scholar
36. Evans, KC, Shea, SA, Saykin, AJ. Functional MRI localisation ofcentral nervous system regions associated with volitional inspiration in humans. J Physiol 1999; 520: 383–392.CrossRefGoogle Scholar
37. Haouzi, P, Chenuel, B, Huszczuk, A. Sensing vascular distension inskeletal muscle by slow conducting afferent fibers: neurophysiological basis and implication for respiratory control. J Appl Physiol 2004; 96: 407–418.Google Scholar
38. Eldridge, FL, Millhorn, DE, Kiley, JP, et al. Stimulation by centralcommand of locomotion, respiration and circulation during exercise. Respir Physiol 1985; 59: 313–337.Google Scholar
39. Thornton, JM, Guz, A, Murphy, K, et al. Identification of higher braincentres that may encode the cardiorespiratory response to exercise in humans. J Physiol 2001; 533: 3–36.Google Scholar
40. Evans, KC, Banzett, RB, Adams, L, et al. BOLD fMRI identifieslimbic, paralimbic, and cerebellar activation during air hunger. J Neurophysiol 2002; 88: 1500–1511.Google Scholar
41. Brannan, S, Liotti, M, Egan, G, et al. Neuroimaging of cerebralactivations and deactivations associated with hypercapnia and hunger for air. Proc Natl Acad Sci USA 2001; 98: 2029–2034.Google Scholar
42. Banzett, RB, Mulnier, HE, Murphy, K, et al. Breathlessness inhumans activates insular cortex. Neuro Report 2000; 11: 2117–2120.Google Scholar
43. Moosavi, SH, Golestanian, E, Binks, AP, et al. Hypoxic andhypercapnic drives to breathe generate equivalent levels of air hunger in humans. J Appl Physiol 2003; 94: 141–154.Google Scholar
44. King, AB, Menon, RS, Hachinski, V, et al. Human forebrainactivation by visceral stimuli. J Comp Neurol 1999; 413: 572–582.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
45. D’Esposito, M, Deouell, LY, Gazzaley, A. Alterations in the BOLDfMRI signal with ageing and disease: a challenge for neuroimaging. Nat Rev Neurosci 2003; 4: 863–872.Google Scholar
46. Bolton, CF, Chen, R, Wijdicks, EFM, Zifko, UA. Neurology of Breathing. Philadelphia: Butterworth Heinemann, 2004: 1–304 Google Scholar
47. Heywood, P, Murphy, K, Corfield, DR, et al. Control of breathing inman; insights from the ‘locked-in’ syndrome. Respir Physiol 1996; 106: 13–20.Google Scholar
48. Boiten, FA, Frijda, NH, Wientjes, CJE. Emotions and respiratorypatterns – review and critical analysis. Intl J Psychophysiol 1994; 17: 103–128.Google Scholar
49. Harrer, G. SomatischeAspekte des Musikerlebens. Med Monatsspiegel 1970; 6: 124–127.Google Scholar