Arousal response to hypoxia in newborns: Insights from animal models

Biological Psychology

Volumn 84, Issue 1, 2010, Pages 39-45

  Gallego, Jorge ^a,b   Matrot, Boris ^a,b  

^a HÔPITAL ROBERT DEBRÉ   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Breathing; Conditioning; Habituation; Ultrasonic vocalizations

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PHOX2B; UNCLASSIFIED DRUG;

AROUSAL; ARTERIAL PRESSURE; BLOOD OXYGEN TENSION; CHEMORECEPTOR; CONDITIONING; DISEASE ASSOCIATION; ELECTROENCEPHALOGRAPHY; FATTY ACID DESATURATION; GENE MUTATION; HABITUATION; HEART RATE; HEREDITY; HUMAN; HYPOXIA; MECHANORECEPTOR; METABOLIC RATE; NONHUMAN; PATHOGENESIS; PRADER WILLI SYNDROME; PRIORITY JOURNAL; RESPIRATION CONTROL; REVIEW; SLEEP PATTERN; SOLITARY TRACT NUCLEUS; TEMPERATURE;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; AROUSAL; ASSOCIATION LEARNING; MICE; MODELS, ANIMAL; RESPIRATION;

EID: 77952291052     PISSN: 03010511     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsycho.2009.12.001     Document Type: Review

References (96)

1. Al-Matary A., Kutbi I., Qurashi M., Khalil M., Alvaro R., Kwiatkowski K., et al. Increased peripheral chemoreceptor activity may be critical in destabilizing breathing in neonates. Seminars in Perinatology 2004, 28:264-272.
2. Amiel J., Laudier B., Attie-Bitach T., Trang H., de Pontual L., Gener B., et al. Polyalanine expansion and frameshift mutations of the paired-like homeobox gene PHOX2B in congenital central hypoventilation syndrome. Nature Genetics 2003, 33:459-461.
3. Antic N.A., Malow B.A., Lange N., McEvoy R.D., Olson A.L., Turkington P., et al. PHOX2B mutation-confirmed congenital central hypoventilation syndrome: presentation in adulthood. American Journal of Respiratory and Critical Care Medicine 2006, 174:923-927.
4. Arens R., Gozal D., Burrell B.C., Bailey S.L., Bautista D.B., Keens T.G., et al. Arousal and cardiorespiratory responses to hypoxia in Prader-Willi syndrome. American Journal of Respiratory and Critical Care Medicine 1996, 153:283-287.
5. Audero E., Coppi E., Mlinar B., Rossetti T., Caprioli A., Banchaabouchi M.A., et al. Sporadic autonomic dysregulation and death associated with excessive serotonin autoinhibition. Science 2008, 321:130-133.
6. Ayas N.T., Brown R., Shea S.A. Hypercapnia can induce arousal from sleep in the absence of altered respiratory mechanoreception. American Journal of Respiratory and Critical Care Medicine 2000, 162:1004-1008.
7. Balbir A., Lande B., Fitzgerald R.S., Polotsky V., Mitzner W., Shirahata M. Behavioral and respiratory characteristics during sleep in neonatal DBA/2J and A/J mice. Brain Research 2008, 1241:84-91.
8. Barratt S., Kendrick A.H., Buchanan F., Whittle A.T. Central hypoventilation with PHOX2B expansion mutation presenting in adulthood. Thorax 2007, 62:919-920.
9. Bass J.L., Corwin M., Gozal D., Moore C., Nishida H., Parker S., et al. The effect of chronic or intermittent hypoxia on cognition in childhood: a review of the evidence. Pediatrics 2004, 114:805-816.
10. Berry R.B., Gleeson K. Respiratory arousal from sleep: mechanisms and significance. Sleep 1997, 20:654-675.
11. Bissonnette J.M. Mechanisms regulating hypoxic respiratory depression during fetal and postnatal life. American Journal of Physiology: Regulatory Integrative and Comparative Physiology 2000, 278:R1391-1400.
12. Blumberg M.S., Karlsson K.A., Seelke A.M., Mohns E.J. The ontogeny of mammalian sleep: a response to Frank and Heller (2003). Journal of Sleep Research 2005, 14:91-98.
13. Bollen B., Bouslama M., Matrot B., D'Hooge R., Van den Bergh O., Gallego J. Learned defense response to hypoxia in newborn mice. Neuroscience Letters 2007, 420:268-272.
14. Bollen B., Bouslama M., Matrot B., Rotrou Y., Vardon G., Lofaso F., et al. Cold stimulates the behavioral response to hypoxia in newborn mice. American Journal of Physiology: Regulatory Integrative and Comparative Physiology 2009, 296:R1503-1511.
15. Brunet J.F., Pattyn A. Phox2 genes-from patterning to connectivity. Current Opinion in Genetics and Development 2002, 12:435-440.
16. Camfferman D., Lushington K., O'Donoghue F., Doug McEvoy R. Obstructive sleep apnea syndrome in Prader-Willi Syndrome: an unrecognized and untreated cause of cognitive and behavioral deficits?. Neuropsychology Review 2006, 16:123-129.
17. 2 sensitivity. Respiration Physiology and Neurobiology 2005, 149:201-215.
18. Chen M.L., Keens T.G. Congenital central hypoventilation syndrome: not just another rare disorder. Paediatric Respiratory Reviews 2004, 5:182-189.
19. Cohen G., Roux J.C., Grailhe R., Malcolm G., Changeux J.P., Lagercrantz H. Perinatal exposure to nicotine causes deficits associated with a loss of nicotinic receptor function. PNAS 2005, 102:3817-3821.
20. Cummings K.J., Klotz C., Liu W.Q., Weese-Mayer D.E., Marazita M.L., Cooper M.E., et al. Sudden infant death syndrome (SIDS) in African Americans: polymorphisms in the gene encoding the stress peptide pituitary adenylate cyclase-activating polypeptide (PACAP). Acta Paediatrica 2009, 98:482-489.
21. Dauger S., Aizenfisz S., Renolleau S., Durand E., Vardon G., Gaultier C., et al. Arousal response to hypoxia in newborn mice. Respiration Physiology 2001, 128:235-240.
22. Dauger S., Pattyn A., Lofaso F., Gaultier C., Goridis C., Gallego J., et al. Phox2b controls the development of peripheral chemoreceptors and afferent visceral pathways. Development 2003, 130:6635-6642.
23. Diedrich A., Malow B.A., Antic N.A., Sato K., McEvoy R.D., Mathias C.J., et al. Vagal and sympathetic heart rate and blood pressure control in adult onset PHOX2B mutation-confirmed congenital central hypoventilation syndrome. Clinical Autonomic Research 2007, 17:177-185.
24. Doherty L.S., Kiely J.L., Deegan P.C., Nolan G., McCabe S., Green A.J., et al. Late-onset central hypoventilation syndrome: a family genetic study. European Respiratory Journal 2007, 29:312-316.
25. 2 chemosensitivity, fatal central apnea, and specific loss of parafacial neurons. PNAS 2008, 105:1067-1072.
26. Dunne K.P., Fox G.P., O'Regan M., Matthews T.G. Arousal responses in babies at risk of sudden infant death syndrome at different postnatal ages. Irish Medical Journal 1992, 85:19-22.
27. Durand E., Dauger S., Pattyn A., Gaultier C., Goridis C., Gallego J. Sleep-disordered breathing in newborn mice heterozygous for the transcription factor Phox2b. American Journal of Respiratory and Critical Care Medicine 2005, 172:238-243.
28. Eichenwald E.C., Aina A., Stark A.R. Apnea frequently persists beyond term gestation in infants delivered at 24 to 28 weeks. Pediatrics 1997, 100:354-359.
29. Enhorning G., van Schaik S., Lundgren C., Vargas I. Whole-body plethysmography, does it measure tidal volume of small animals?. Canadian Journal of Physiology and Pharmacology 1998, 76:945-951.
30. Erickson J.T., Shafer G., Rossetti M.D., Wilson C.G., Deneris E.S. Arrest of 5HT neuron differentiation delays respiratory maturation and impairs neonatal homeostatic responses to environmental challenges. Respiration Physiology and Neurobiology 2007, 159:85-101.
31. Festen D.A., Wevers M., de Weerd A.W., van den Bossche R.A., Duivenvoorden H.J., Hokken-Koelega A.C. Cognition and behavior in pre-pubertal children with Prader-Willi syndrome and associations with sleep-related breathing disorders. American Journal of Medical Genetics A 2008, 146A:3018-3025.
32. Fewell J.E. Protective responses of the newborn to hypoxia. Respiration Physiology and Neurobiology 2005, 149:243-255.
33. Fewell J.E., Konduri G.G. Influence of repeated exposure to rapidly developing hypoxaemia on the arousal and cardiopulmonary response to rapidly developing hypoxaemia in lambs. Journal of Developmental Physiology 1989, 11:77-82.
34. Galland B.C., Taylor B.J., Bolton D.P., Sayers R.M. Respiratory responses to hypoxia/hypercapnia in small for gestational age infants influenced by maternal smoking. Archives of Disease in Childhood Fetal Neonatal Edition 2003, 88:F217-F222.
35. Gallego J., Dauger S. PHOX2B mutations and ventilatory control. Respiration Physiology and Neurobiology 2008, 164:49-54.
36. Gauda E.B., Cristofalo E., Nunez J. Peripheral arterial chemoreceptors and sudden infant death syndrome. Respiration Physiology and Neurobiology 2007, 157:162-170.
37. Gaultier C., Amiel J., Dauger S., Trang H., Lyonnet S., Gallego J., et al. Genetics and early disturbances of breathing control. Pediatric Research 2004, 55:729-733.
38. Greer J.J., Wevrick R. Respiratory control abnormalities in necdin-null mice: implications for the pathogenesis of Prader-Willi Syndrome. Genetic Basis for Respiratory Control Disorders 2008, 259-269. Springer, New York. C. Gaultier (Ed.).
39. Hafstrom O., Milerad J., Sandberg K.L., Sundell H.W. Cardiorespiratory effects of nicotine exposure during development. Respiration Physiology and Neurobiology 2005, 149:325-341.
40. Hafstrom O., Milerad J., Sundell H.W. Prenatal nicotine exposure blunts the cardiorespiratory response to hypoxia in lambs. American Journal of Respiratory and Critical Care Medicine 2002, 166:1544-1549.
41. Harrington C., Kirjavainen T., Teng A., Sullivan C.E. Altered autonomic function and reduced arousability in apparent life-threatening event infants with obstructive sleep apnea. American Journal of Respiratory and Critical Care Medicine 2002, 165:1048-1054.
42. Hodges M.R., Tattersall G.J., Harris M.B., McEvoy S.D., Richerson D.N., Deneris E.S., et al. Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. Journal of Neurosciences 2008, 28:2495-2505.
43. Hodges M.R., Wehner M., Aungst J., Smith J.C., Richerson G.B. Transgenic mice lacking serotonin neurons have severe apnea and high mortality during development. Journal of Neurosciences 2009, 29:10341-10349.
44. Hoppenbrouwers T., Hodgman J.E., Rybine D., Fabrikant G., Corwin M., Crowell D., et al. Sleep architecture in term and preterm infants beyond the neonatal period: the influence of gestational age, steroids, and ventilatory support. Sleep 2005, 28:1428-1436.
45. Horne R.S., Parslow P.M., Harding R. Respiratory control and arousal in sleeping infants. Paediatric Respiratory Reviews 2004, 5:190-198.
46. Horne R.S., Parslow P.M., Harding R. Postnatal development of ventilatory and arousal responses to hypoxia in human infants. Respiration Physiology and Neurobiology 2005, 149:257-271.
47. Huffman A.D., Smok-Pearsall S.M., Silvestri J.M., Weese-Mayer D.E. SIDS risk factor awareness: assessment among nursing students. Journal of Obstetric, Gynecology and Neonatal Nursing 1999, 28:68-73.
48. Hunt C.E. Gene-environment interactions: implications for sudden unexpected deaths in infancy. Archives Disease Childhood 2005, 90:48-53.
49. Janvier A., Khairy M., Kokkotis A., Cormier C., Messmer D., Barrington K.J. Apnea is associated with neurodevelopmental impairment in very low birth weight infants. Journal of Perinatology 2004, 24:763-768.
50. Johnston R.V., Grant D.A., Wilkinson M.H., Walker A.M. Repetitive hypoxia rapidly depresses cardio-respiratory responses during active sleep but not quiet sleep in the newborn lamb. Journal of Physiology 1999, 519(Pt 2):571-579.
51. Johnston R.V., Grant D.A., Wilkinson M.H., Walker A.M. The effects of repeated exposure to hypercapnia on arousal and cardiorespiratory responses during sleep in lambs. Journal of Physiology 2007, 582:369-378.
52. Kahn A., Groswasser J., Franco P., Scaillet S., Sawaguchi A., Kelmenson I., et al. Sudden infant deaths: arousal as a survival mechanism. Sleep Medicine 2002, 3:S11-S14.
53. Karlsson K.A., Blumberg M.S. The union of the state: myoclonic twitching is coupled with nuchal muscle atonia in infant rats. Behavioral Neurosciences 2002, 116:912-917.
54. Kinney H.C. Brainstem mechanisms underlying the sudden infant death syndrome: evidence from human pathologic studies. Developmental Psychobiology 2009, 51:223-233.
55. Lehtonen L., Martin R.J. Ontogeny of sleep and awake states in relation to breathing in preterm infants. Seminars in Neonatology 2004, 9:229-238.
56. Leiter J.C. Serotonin, gasping, autoresuscitation and SIDS-a contrarian view. Journal of Applied Physiology 2009.
57. Leiter J.C., Bohm I. Mechanisms of pathogenesis in the sudden infant death syndrome. Respiration Physiology and Neurobiology 2007, 159:127-138.
58. Li A., Nattie E. Serotonin transporter knockout mice have a reduced ventilatory response to hypercapnia (predominantly in males) but not to hypoxia. Journal of Physiology 2008, 586:2321-2329.
59. Lijowska A.S., Reed N.W., Chiodini B.A., Thach B.T. Sequential arousal and airway-defensive behavior of infants in asphyxial sleep environments. Journal of Applied Physiology 1997, 83:219-228.
60. Marazita M.L., Maher B.S., Cooper M.E., Silvestri J.M., Huffman A.D., Smok-Pearsall S.M., et al. Genetic segregation analysis of autonomic nervous system dysfunction in families of probands with idiopathic congenital central hypoventilation syndrome. American Journal of Medical Genetics 2001, 100:229-236.
61. Martin R.J., Abu-Shaweesh J.M. Control of breathing and neonatal apnea. Biology of the Neonate 2005, 87:288-295.
62. Martin R.J., DiFiore J.M., Jana L., Davis R.L., Miller M.J., Coles S.K., et al. Persistence of the biphasic ventilatory response to hypoxia in preterm infants. Journal of Pediatrics 1998, 132:960-964.
63. Masa J.F., Corral J., Martin M.J., Riesco J.A., Sojo A., Hernandez M., et al. Assessment of thoracoabdominal bands to detect respiratory effort-related arousal. European Respiratory Journal 2003, 22:661-667.
64. Matera I., Bachetti T., Puppo F., Di Duca M., Morandi F., Casiraghi G., et al. PHOX2B mutations and polyalanine expansions correlate with the severity of the respiratory phenotype and associated symptoms in both congenital and late onset Central Hypoventilation syndrome. Journal of Medical Genetics 2004, 41:373-380.
65. Matrot B., Durand E., Dauger S., Vardon G., Gaultier C., Gallego J. Automatic classification of activity and apneas using whole body plethysmography in newborn mice. Journal of Applied Physiology 2005, 98:365-370.
66. McCulloch K., Brouillette R.T., Guzzetta A.J., Hunt C.E. Arousal responses in near-miss sudden infant death syndrome and in normal infants. Journal of Pediatrics 1982, 101:911-917.
67. McNamara F., Wulbrand H., Thach B.T. Characteristics of the infant arousal response. Journal of Applied Physiology 1998, 85:2314-2321.
68. Mortola J.P., Frappell P.B. On the barometric method for measurements of ventilation, and its use in small animals. Canadian Journal of Physiology and Pharmacology 1998, 76:937-944.
69. Nakada Y., Taniura H., Uetsuki T., Inazawa J., Yoshikawa K. The human chromosomal gene for necdin, a neuronal growth suppressor, in the Prader-Willi syndrome deletion region. Gene 1998, 213:65-72.
70. Nixon G.M., Brouillette R.T. Sleep and breathing in Prader-Willi syndrome. Pediatric Pulmonology 2002, 34:209-217.
71. Nsegbe E., Vardon G., Dauger S., Perruchet P., Gaultier C., Gallego J. Classical conditioning to hypoxia using odors as conditioned stimuli in rats. Behavioral Neurosciences 1998, 112:1393-1401.
72. Nsegbe E., Villaret E., Renolleau S., Vardon G., Gaultier C., Gallego J. Behavioural correlates of conditioned ventilatory responses to hypoxia in rats. Behavioral Brain Research 1999, 106:29-37.
73. Parslow P.M., Cranage S.M., Adamson T.M., Harding R., Horne R.S. Arousal and ventilatory responses to hypoxia in sleeping infants: effects of maternal smoking. Respiration Physiology and Neurobiology 2004, 140:77-87.
74. Parslow P.M., Harding R., Cranage S.M., Adamson T.M., Horne R.S. Ventilatory responses preceding hypoxia-induced arousal in infants: effects of sleep-state. Respiration Physiology and Neurobiology 2003, 136:235-247.
75. Pattyn A., Morin X., Cremer H., Goridis C., Brunet J.F. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 1997, 124:4065-4075.
76. Phillipson E.A., Sullivan C.E. Arousal: the forgotten response to respiratory stimuli. American Review of Respiratory Disease 1978, 118:807-809.
77. Prabhakar N.R., Fields R.D., Baker T., Fletcher E.C. Intermittent hypoxia: cell to system. American Journal of Physiology: Lung Cellular and Molecular Physiology 2001, 281:L524-528.
78. Ramanantsoa N., Vaubourg V., Matrot B., Vardon G., Dauger S., Gallego J. Effects of temperature on ventilatory response to hypercapnia in newborn mice heterozygous for transcription factor Phox2b. American Journal of Physiology: Regulatory Integrative and Comparative Physiology 2007, 293:R2027-2035.
79. Richardson H.L., Parslow P.M., Walker A.M., Harding R., Horne R.S. Variability of the initial phase of the ventilatory response to hypoxia in sleeping infants. Pediatric Research 2006, 59:700-704.
80. Richardson H.L., Parslow P.M., Walker A.M., Harding R., Horne R.S. Maturation of the initial ventilatory response to hypoxia in sleeping infants. Journal of Sleep Research 2007, 16:117-127.
81. Rigatto H., Brady J.P. Periodic breathing and apnea in preterm infants. I. Evidence for hypoventilation possibly due to central respiratory depression. Pediatrics 1972, 50:202-218.
82. Rigatto H., Brady J.P. Periodic breathing and apnea in preterm infants. II. Hypoxia as a primary event. Pediatrics 1972, 50:219-228.
83. Sasaki A., Kanai M., Kijima K., Akaba K., Hashimoto M., Hasegawa H., et al. Molecular analysis of congenital central hypoventilation syndrome. Human Genetics 2003, 114:22-26.
84. Sawaguchi T., Kato I., Franco P., Sottiaux M., Kadhim H., Shimizu S., et al. Apnea, glial apoptosis and neuronal plasticity in the arousal pathway of victims of SIDS. Forensic Science International 2005, 149:205-217.
85. Stornetta R.L., Moreira T.S., Takakura A.C., Kang B.J., Chang D.A., West G.H., et al. Expression of Phox2b by brainstem neurons involved in chemosensory integration in the adult rat. Journal of Neurosciences 2006, 26:10305-10314.
86. Task Force on Sudden Infant Death Syndrome The changing concept of sudden infant death syndrome: diagnostic coding shifts, controversies regarding the sleeping environment, and new variables to consider in reducing risk. Pediatrics 2005, 116:1245-1255.
87. Thach B.T. Graded arousal responses in infants: advantages and disadvantages of a low threshold for arousal. Sleep Medicine 2002, 3(Suppl (2)):S37-40.
88. Thach B.T. The role of respiratory control disorders in SIDS. Respiration Physiology and Neurobiology 2005, 149:343-353.
89. Thoppil C.K., Belan M.A., Cowen C.P., Mathew O.P. Behavioral arousal in newborn infants and its association with termination of apnea. Journal of Applied Physiology 1991, 70:2479-2484.
90. Tiveron M.C., Hirsch M.R., Brunet J.F. The expression pattern of the transcription factor Phox2b delineates synaptic pathways of the autonomic nervous system. Journal of Neurosciences 1996, 16:7649-7660.
91. Trochet D., Hong S.J., Lim J.K., Brunet J.F., Munnich A., Kim K.S., et al. Molecular consequences of PHOX2B missense, frameshift and alanine expansion mutations leading to autonomic dysfunction. Human Molecular Genetics 2005, 14:3697-3708.
92. Vanderlaan M., Holbrook C.R., Wang M., Tuell A., Gozal D. Epidemiologic survey of 196 patients with congenital central hypoventilation syndrome. Pediatric Pulmonology 2004, 37:217-229.
93. Vennemann M., Fischer D., Jorch G., Bajanowski T. Prevention of sudden infant death syndrome (SIDS) due to an active health monitoring system 20 years prior to the public " Back to Sleep" campaigns. Archives of Disease in Childhood 2006, 91:324-326.
94. Ward S.L., Bautista D.B., Keens T.G. Hypoxic arousal responses in normal infants. Pediatrics 1992, 89:860-864.
95. Waters K.A., Tinworth K.D. Habituation of arousal responses after intermittent hypercapnic hypoxia in piglets. American Journal of Respiratory and Critical Care Medicine 2005, 171:1305-1311.
96. Wen S.W., Smith G., Yang Q., Walker M. Epidemiology of preterm birth and neonatal outcome. Seminars in Fetal and Neonatal Medicine 2004, 9:429-435.