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The Journal of Neuroscience, March 17, 2004, 24(11):2813-2824; doi:10.1523/JNEUROSCI.3779-03.2004

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Behavioral/Systems/Cognitive
Nitric Oxide Inhibits the Rate and Strength of Cardiac Contractions in the Lobster Homarus americanus by Acting on the Cardiac Ganglion

Anand Mahadevan,¹ Jason Lappé,¹ Randall T. Rhyne,² Nelson D. Cruz-Bermúdez,¹ Eve Marder,¹ and Michael F. Goy²

¹Department of Biology and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454, and ²Department of Cell and Molecular Physiology, University of North Carolina, Chapel Hill, North Carolina 27599

The lobster heart is synaptically driven by the cardiac ganglion, a spontaneously bursting neural network residing within the cardiac lumen. Here, we present evidence that nitric oxide (NO) plays an inhibitory role in lobster cardiac physiology. (1) NO decreases heartbeat frequency and amplitude. Decreased frequency is a direct consequence of a decreased ganglionic burst rate. Decreased amplitude is an indirect consequence of decreased burst frequency, attributable to the highly facilitating nature of the synapses between cardiac ganglion neurons and muscle fibers (although, during prolonged exposure to NO, amplitude recovers to the original level by a frequency-independent adaptation mechanism). NO does not alter burst duration, spikes per burst, heart muscle contractility, or amplitudes of synaptic potentials evoked by stimulating postganglionic motor nerves. Thus, NO acts on the ganglion, but not on heart muscle. (2) Two observations suggest that NO is produced within the lobster heart. First, immunoblot analysis shows that nitric oxide synthase (NOS) is strongly expressed in heart muscle relative to other muscles. Second, L-nitroarginine (L-NA), an NOS inhibitor, increases the rate of the heartbeat (opposite to the effects of NO). In contrast, the isolated ganglion is insensitive to L-NA, suggesting that heart muscle (but not the ganglion) produces endogenous NO. Basal heart rate varies from animal to animal, and L-NA has the greatest effect on the slowest hearts, presumably because these hearts are producing the most NO. Thus, because the musculature is a site of NOS expression, whereas the ganglion is the only intracardiac target of NO, we hypothesize that NO serves as an inhibitory retrograde transmitter.

Key words: crustacean; heart; neuromodulation; central pattern generator; negative inotropy; negative chronotropy; nitric oxide

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Received Aug 13, 2003; revised January 29, 2004; accepted January 29, 2004.

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