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J Appl Physiol 92: 1899-1910, 2002. First published December 21, 2001; doi:10.1152/japplphysiol.00475.2001
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Vol. 92, Issue 5, 1899-1910, May 2002

Modulation of phrenic motoneuron excitability by ATP: consequences for respiratory-related output in vitro

Gareth B. Miles, Marjorie A. Parkis, Janusz Lipski, and Gregory D. Funk

Department of Physiology, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand

On the basis of the high level of P2X receptor expression found in phrenic motoneurons (MN) in rats (Kanjhan et al., J Comp Neurol 407: 11-32, 1999) and potentiation of hypoglossal MN inspiratory activity by ATP (Funk et al., J Neurosci 17: 6325-6337, 1997), we tested the hypothesis that ATP receptor activation also modulates phrenic MN activity. This question was examined in rhythmically active brain stem-spinal cord preparations from neonatal rats by monitoring effects of ATP on the activity of spinal C4 nerve roots and phrenic MNs. ATP produced a rapid-onset, dose-dependent, suramin- and pyridoxal-phosphate-6-azophenyl-2',4'-disulphonic acid 4-sodium-sensitive increase in C4 root tonic discharge and a 22 ± 7% potentiation of inspiratory burst amplitude. This was followed by a slower, 10 ± 5% reduction in burst amplitude. ATPgamma S, the hydrolysis-resistant analog, evoked only the excitatory response. ATP induced inward currents (57 ± 39 pA) and increased repetitive firing of phrenic MNs. These data, combined with persistence of ATP currents in TTX and immunolabeling for P2X2 receptors in Fluoro-Gold-labeled C4 MNs, implicate postsynaptic P2 receptors in the excitation. Inspiratory synaptic currents, however, were inhibited by ATP. This inhibition differed from that seen in root recordings; it did not follow an excitation, had a faster onset, and was induced by ATPgamma S. Thus ATP inhibited activity through at least two mechanisms: 1) a rapid P2 receptor-mediated inhibition and 2) a delayed P1 receptor-mediated inhibition associated with hydrolysis of ATP to adenosine. The complex effects of ATP on phrenic MNs highlight the importance of ATP as a modulator of central motor outflows.

P2 receptors; adenosine; immunohistochemistry; rat; neonate


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