Developmental nicotine exposure alters neurotransmission and excitability in hypoglossal motoneurons

Journal of Neurophysiology

Volumn 105, Issue 1, 2011, Pages 423-433

  Pilarski, Jason Q ^a   Wakefield, Hilary E ^a   Fuglevand, Andrew J ^a,b   Levine, Richard B ^a,b   Fregosi, Ralph F ^a,b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINE; NICOTINIC RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APNEA; ARTICLE; BRAIN SLICE; BRAIN STEM; BREATHING; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HYPOGLOSSAL NERVE; INCIDENCE; LONG TERM EXPOSURE; MALE; MOTONEURON; NERVE CELL EXCITABILITY; NEUROTRANSMISSION; NEWBORN; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; RAT; RESPIRATORY NERVE CELL; VOLTAGE CLAMP;

ANIMALS; ANIMALS, NEWBORN; BIOPHYSICAL PHENOMENA; FEMALE; GLUTAMIC ACID; HYPOGLOSSAL NERVE; MALE; MODELS, ANIMAL; MOTOR NEURONS; NICOTINE; PATCH-CLAMP TECHNIQUES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NICOTINIC; SYNAPTIC TRANSMISSION;

EID: 78651414863     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00876.2010     Document Type: Article

References (70)

1. Abdel-Rahman A, Dechkovskaia AM, Sutton JM, Chen WC, Guan X, Khan WA, Abou-Donia MB. Maternal exposure of rats to nicotine via infusion during gestation produces neurobehavioral deficits and elevated expression of glial fibrillary acidic protein in the cerebellum and CA1 subfield in the offspring at puberty. Toxicology 209: 245-261, 2005.
2. Bailey EF, Huang YH, Fregosi RF. Anatomic consequences of intrinsic tongue muscle activation. J Appl Physiol 101: 1377-1385, 2006.
3. Barik J, Wonnacott S. Molecular and cellular mechanisms of action of nicotine in the CNS. In: Nicotine Psychopharmacology, edited by Henning-field JE, London ED, Pogun S. Berlin: Springer, 2009, p. 173-207.
4. Bellingham MC, Berger AJ. Presynaptic depression of excitatory synaptic inputs to rat hypoglossal motoneurons by muscarinic M2 receptors. J Neurophysiol 76: 3758-3770, 1996.
5. Benowitz NL, Jacob P 3rd. Daily intake of nicotine during cigarette smoking. Clin Pharmacol Ther 35: 499-504, 1984.
6. Benwell ME, Balfour DJ. Regional variation in the effects of nicotine on catecholamine overflow in rat brain. Eur J Pharmacol 325: 13-20, 1997.
7. Bissonnette JM, Knopp SJ. Hypercapnic ventilatory response in mice lacking the 65 kDa isoform of glutamic acid decarboxylase (GAD65) (Abstract). Respir Res 5: 3, 2004.
8. Bordia T, Campos C, McIntosh JM, Quik M. Nicotinic receptor-mediated reduction in L-DOPA-induced dyskinesias may occur via desensitization. J Pharmacol Exp Ther 333: 929-938, 2010.
9. Carroll JL. Developmental plasticity in respiratory control. J Appl Physiol 94: 375-389, 2003.
10. Chamberlin NL, Bocchiaro CM, Greene RW, Feldman JL. Nicotinic excitation of rat hypoglossal motoneurons. Neuroscience 115: 861-870, 2002.
11. Chen H, Parker SL, Matta SG, Sharp BM. Gestational nicotine exposure reduces nicotinic cholinergic receptor (nAChR) expression in dopaminergic brain regions of adolescent rats. Eur J Neurosci 22: 380-388, 2005.
12. Chen WJ, King KA, Lee RE, Sedtal CS, Smith AM. Effects of nicotine exposure during prenatal or perinatal period on cell numbers in adult rat hippocampus and cerebellum: a stereology study. Life Sci 79: 2221-2227, 2006.
13. Dehkordi O, Millis RM, Dennis GC, Coleman BR, Johnson SM, Changizi L, Ovid Trouth C. Alpha-7 and alpha-4 nicotinic receptor subunit immunoreactivity in genioglossus muscle motoneurons. Respir Physiol Neurobiol 145: 153-161, 2005.
14. Dobbins EG, Feldman JL. Brainstem network controlling descending drive to phrenic motoneurons in rat. J Comp Neurol 347: 64-86, 1994.
15. Feldman JL, Del Negro CA. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7: 232-242, 2006.
16. Fregosi RF, Luo Z, Iizuka M. GABAA receptors mediate postnatal depression of respiratory frequency by barbiturates. Respir Physiol Neurobiol 140: 219-230, 2004.
17. Fregosi RF, Pilarski JQ. Prenatal nicotine exposure and development of nicotinic and fast amino acid-mediated neurotransmission in the control of breathing. Respir Physiol Neurobiol 164: 80-86, 2008.
18. Fuller DD, Williams JS, Janssen PL, Fregosi RF. Effect of co-activation of tongue protrudor and retractor muscles on tongue movements and pharyngeal airflow mechanics in the rat. J Physiol 519: 601-613, 1999.
19. Funk GD, Parkis MA, Selvaratnam SR, Robinson DM, Miles GB, Peebles KC. Synaptic control of motoneuron excitability in rodents: from months to milliseconds. Clin Exp Pharmacol Physiol 27: 120-125, 2000.
20. Funk GD, Smith JC, Feldman JL. Generation and transmission of respiratory oscillations in medullary slices: role of excitatory amino acids. J Neurophysiol 70: 1497-1515, 1993.
21. Gastaut H, Duron B, Tassinari CA, Lyagoubi S, Saier J. Mechanism of the respiratory pauses accompanying slumber in the Pickwickian syndrome (Abstract). Act Nerv Super (Praha) 11: 2095, 1969.
22. Gaultier C. Development of the control of breathing: implications for sleep-related breathing disorders in infants. Sleep 23, Suppl. 4: S136-S139, 2000.
23. Gentry CL, Lukas RJ. Regulation of nicotinic acetylcholine receptor numbers and function by chronic nicotine exposure. Curr Drug Targets CNS Neurol Disord 1: 359-385, 2002.
24. Giniatullin R, Nistri A, Yakel JL. Desensitization of nicotinic ACh receptors: shaping cholinergic signaling. Trends Neurosci 28: 371-378, 2005.
25. Gothe B, Strohl KP, Levin S, Cherniack NS. Nicotine: a different approach to treatment of obstructive sleep apnea. Chest 87: 11-17, 1985.
26. Gottesmann C. Brain inhibitory mechanisms involved in basic and higher integrated sleep processes. Brain Res Brain Res Rev 45: 230-249, 2004.
27. Gray PA, Rekling JC, Bocchiaro CM, Feldman JL. Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the pre-Bötzinger complex. Science 286: 1566-1568, 1999.
28. Greer JJ, Smith JC, Feldman JL. Role of excitatory amino acids in the generation and transmission of respiratory drive in neonatal rat. J Physiol 437: 727-749, 1991.
29. Griguoli M, Maul A, Nguyen C, Giorgetti A, Carloni P, Cherubini E. Nicotine blocks the hyperpolarization-activated current Ih and severely impairs the oscillatory behavior of oriens-lacunosum moleculare interneurons. J Neurosci 30: 10773-10783, 2010.
30. Hafstrom O, Milerad J, Sandberg KL, Sundell HW. Cardiorespiratory effects of nicotine exposure during development. Respir Physiol Neurobiol 149: 325-341, 2005.
31. Hayashida S, Katsura M, Torigoe F, Tsujimura A, Ohkuma S. Increased expression of L-type high voltage-gated calcium channel alpha1 and alpha2/delta subunits in mouse brain after chronic nicotine administration. Brain Res Mol Brain Res 135: 280-284, 2005. (Pubitemid 40602419)
32. Hehre DA, Devia CJ, Bancalari E, Suguihara C. Brainstem amino acid neurotransmitters and ventilatory response to hypoxia in piglets. Pediatr Res 63: 46-50, 2008.
33. Horner RL. Motor control of the pharyngeal musculature and implications for the pathogenesis of obstructive sleep apnea. Sleep 19: 827-853, 1996.
34. Horner RL. Neuromodulation of hypoglossal motoneurons during sleep. Respir Physiol Neurobiol 164: 179-196, 2008.
35. Horner RL. Emerging principles and neural substrates underlying tonic sleep-state-dependent influences on respiratory motor activity. Philos Trans R Soc Lond B Biol Sci 364: 2553-2564, 2009.
36. Huang YH, Brown AR, Costy-Bennett S, Luo Z, Fregosi RF. Influence of prenatal nicotine exposure on postnatal development of breathing pattern. Respir Physiol Neurobiol 143: 1-8, 2004.
37. Ishibashi H, Eto K, Kajiwara M, Noda M. Facilitation of spontaneous glutamate release by antidepressant drugs in rat locus coeruleus. Neurosci Lett 374: 152-156, 2005.
38. Kuribayashi J, Sakuraba S, Hosokawa Y, Hatori E, Tsujita M, Takeda J, Yanagawa Y, Obata K, Kuwana S. CO2-sensitivity of GABAergic neurons in the ventral medullary surface of GAD67-GFP knock-in neonatal mice. Adv Exp Med Biol 605: 338-342, 2008.
39. Luck W, Nau H. Nicotine and cotinine concentrations in serum and urine of infants exposed via passive smoking or milk from smoking mothers. J Pediatr 107: 816-820, 1985.
40. Luo Z, Costy-Bennett S, Fregosi RF. Prenatal nicotine exposure increases the strength of GABA(A) receptor-mediated inhibition of respiratory rhythm in neonatal rats. J Physiol 561: 387-393, 2004.
41. Luo Z, McMullen NT, Costy-Bennett S, Fregosi RF. Prenatal nicotine exposure alters glycinergic and GABAergic control of respiratory frequency in the neonatal rat brainstem-spinal cord preparation. Respir Physiol Neurobiol 157: 226-234, 2007.
42. Martin-Caraballo M, Greer JJ. Electrophysiological properties of rat phrenic motoneurons during perinatal development. J Neurophysiol 81: 1365-1378, 1999. (Pubitemid 29272453)
43. Melton JE, Neubauer JA, Edelman NH. GABA antagonism reverses hypoxic respiratory depression in the cat. J Appl Physiol 69: 1296-1301, 1990.
44. Mennella JA, Yourshaw LM, Morgan LK. Breastfeeding and smoking: short-term effects on infant feeding and sleep. Pediatrics 120: 497-502, 2007.
45. Okada Y, Kuwana S, Kawai A, Muckenhoff K, Scheid P. Significance of extracellular potassium in central respiratory control studied in the isolated brainstem-spinal cord preparation of the neonatal rat. Respir Physiol Neurobiol 146: 21-32, 2005.
46. Pilarski JQ, Fregosi RF. Prenatal nicotine exposure alters medullary nicotinic and AMPA-mediated control of respiratory frequency in vitro. Respir Physiol Neurobiol 169: 1-10, 2009.
47. Ptak K, Yamanishi T, Aungst J, Milescu LS, Zhang R, Richerson GB, Smith JC. Raphe neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J Neurosci 29: 3720-3737, 2009.
48. Quitadamo C, Fabbretti E, Lamanauskas N, Nistri A. Activation and desensitization of neuronal nicotinic receptors modulate glutamatergic transmission on neonatal rat hypoglossal motoneurons. Eur J Neurosci 22: 2723-2734, 2005.
49. Rekling JC, Feldman JL. Pre-Bötzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu Rev Physiol 60: 385-405, 1998.
50. Remmers JE, deGroot WJ, Sauerland EK, Anch AM. Pathogenesis of upper airway occlusion during sleep. J Appl Physiol 44: 931-938, 1978.
51. Robinson DM, Peebles KC, Kwok H, Adams BM, Clarke LL, Woollard GA, Funk GD. Prenatal nicotine exposure increases apnoea and reduces nicotinic potentiation of hypoglossal inspiratory output in mice. J Physiol 538: 957-973, 2002.
52. Roy TS, Sabherwal U. Effects of prenatal nicotine exposure on the morphogenesis of somatosensory cortex. Neurotoxicol Teratol 16: 411-421, 1994.
53. Roy TS, Seidler FJ, Slotkin TA. Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex. J Pharmacol Exp Ther 300: 124-133, 2002.
54. Sawnani H, Jackson T, Murphy T, Beckerman R, Simakajornboon N. The effect of maternal smoking on respiratory and arousal patterns in preterm infants during sleep. Am J Respir Crit Care Med 169: 733-738, 2004.
55. Shao XM, Feldman JL. Mechanisms underlying regulation of respiratory pattern by nicotine in pre-Bötzinger complex. J Neurophysiol 85: 2461-2467, 2001.
56. Shao XM, Feldman JL. Pharmacology of nicotinic receptors in pre-Bötzinger complex that mediate modulation of respiratory pattern. J Neurophysiol 88: 1851-1858, 2002.
57. Shao XM, Feldman JL. Cholinergic neurotransmission in the pre-Bötzinger complex modulates excitability of inspiratory neurons and regulates respiratory rhythm. Neuroscience 130: 1069-1081, 2005.
58. Slotkin TA, Greer N, Faust J, Cho H, Seidler FJ. Effects of maternal nicotine injections on brain development in the rat: ornithine decarboxylase activity, nucleic acids and proteins in discrete brain regions. Brain Res Bull 17: 41-50, 1986.
59. Slotkin TA, Ryde IT, Mackillop EA, Bodwell BE, Seidler FJ. Adolescent nicotine administration changes the responses to nicotine given subsequently in adulthood: adenylyl cyclase cell signaling in brain regions during nicotine administration and withdrawal, and lasting effects. Brain Res Bull 76: 522-530, 2008.
60. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
61. Smith JC, Morrison DE, Ellenberger HH, Otto MR, Feldman JL. Brainstem projections to the major respiratory neuron populations in the medulla of the cat. J Comp Neurol 281: 69-96, 1989.
62. Steiner RC, Heath CJ, Picciotto MR. Nicotine-induced phosphorylation of ERK in mouse primary cortical neurons: evidence for involvement of glutamatergic signaling and CaMKII. J Neurochem 103: 666-678, 2007.
63. Stuart GJ, Dodt HU, Sakmann B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflügers Arch 423: 511-518, 1993.
64. Suzue T. Respiratory rhythm generation in the in vitro brain stem-spinal cord preparation of the neonatal rat. J Physiol 354: 173-183, 1984.
65. Toubas PL, Duke JC, McCaffree MA, Mattice CD, Bendell D, Orr WC. Effects of maternal smoking and caffeine habits on infantile apnea: a retrospective study. Pediatrics 78: 159-163, 1986.
66. Underner M, Paquereau J, Meurice JC. Cigarette smoking and sleep disturbance. Rev Mal Respir 23: 6S67-6S77, 2006.
67. Wang J, Irnaten M, Venkatesan P, Evans C, Baxi S, Mendelowitz D. Synaptic activation of hypoglossal respiratory motorneurons during inspiration in rats. Neurosci Lett 332: 195-199, 2002.
68. Weese-Mayer DE, Ackerman MJ, Marazita ML, Berry-Kravis EM. Sudden infant death syndrome: review of implicated genetic factors. Am J Med Genet A 143A: 771-788, 2007.
69. Wonnacott S. Presynaptic nicotinic ACh receptors. Trends Neurosci 20: 92-98, 1997.
70. Zaninetti M, Tribollet E, Bertrand D, Raggenbass M. Presence of functional neuronal nicotinic acetylcholine receptors in brainstem motoneurons of the rat. Eur J Neurosci 11: 2737-2748, 1999.