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The Journal of Neuroscience, January 4, 2006, 26(1):21-29; doi:10.1523/JNEUROSCI.4221-05.2006

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Behavioral/Systems/Cognitive
Differential Control of Central Cardiorespiratory Interactions by Hypercapnia and the Effect of Prenatal Nicotine

Zheng-Gui Huang, Kathleen J. S. Griffioen, Xin Wang, Olga Dergacheva, Harriet Kamendi, Christopher Gorini, Euguenia Bouairi, and David Mendelowitz

Department of Pharmacology and Physiology, The George Washington University, Washington, DC 20037

Hypercapnia evokes a strong cardiorespiratory response including gasping and a pronounced bradycardia; however, the mechanism responsible for these survival responses initiated in the brainstem is unknown. To examine the effects of hypercapnia on the central cardiorespiratory network, we used an in vitro medullary slice that allows simultaneous examination of rhythmic respiratory-related activity and inhibitory synaptic neurotransmission to cardioinhibitory vagal neurons (CVNs). Hypercapnia differentially modulated inhibitory neurotransmission to CVNs; whereas hypercapnia selectively depressed spontaneous glycinergic IPSCs in CVNs without altering respiratory-related increases in glycinergic neurotransmission, it decreased both spontaneous and inspiratory-associated GABAergic IPSCs. Because maternal smoking is the highest risk factor for sudden infant death syndrome (SIDS) and prenatal nicotine exposure is proposed to be the link between maternal smoking and SIDS, we examined the cardiorespiratory responses to hypercapnia in animals exposed to nicotine in the prenatal and perinatal period. In animals exposed to prenatal nicotine, hypercapnia evoked an exaggerated depression of GABAergic IPSCs in CVNs with no significant change in glycinergic neurotransmission. Hypercapnia altered inhibitory neurotransmission to CVNs at both presynaptic and postsynaptic sites. Although the results obtained in this study in vitro cannot be extrapolated with certainty to in vivo responses, the results of this study provide a likely neurochemical mechanism for hypercapnia-evoked bradycardia and the dysregulation of this response with exposure to prenatal nicotine, creating a higher risk for SIDS.

Key words: ambiguus; SIDS; GABA; glycine; prenatal nicotine; hypercapnia

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Received Oct 4, 2005; revised November 1, 2005; accepted November 2, 2005.

This article has been cited by other articles:

				J. Eugenin, M. Otarola, E. Bravo, C. Coddou, V. Cerpa, M. Reyes-Parada, I. Llona, and R. von Bernhardi Prenatal to Early Postnatal Nicotine Exposure Impairs Central Chemoreception and Modifies Breathing Pattern in Mouse Neonates: A Probable Link to Sudden Infant Death Syndrome J. Neurosci., December 17, 2008; 28(51): 13907 - 13917. [Abstract] [Full Text] [PDF]

				H. W. Kamendi, Q. Cheng, O. Dergacheva, J. G. Frank, C. Gorini, H. S. Jameson, R. A. Pinol, X. Wang, and D. Mendelowitz Recruitment of Excitatory Serotonergic Neurotransmission to Cardiac Vagal Neurons in the Nucleus Ambiguus Post Hypoxia and Hypercapnia J Neurophysiol, March 1, 2008; 99(3): 1163 - 1168. [Abstract] [Full Text] [PDF]

				Z. G. Huang, K. J. S. Griffioen, X. Wang, O. Dergacheva, H. Kamendi, C. Gorini, and D. Mendelowitz Nicotinic Receptor Activation Occludes Purinergic Control of Central Cardiorespiratory Network Responses to Hypoxia/Hypercapnia J Neurophysiol, October 1, 2007; 98(4): 2429 - 2438. [Abstract] [Full Text] [PDF]

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