Modulation of swimming in the gastropod Melibe leonina by nitric oxide
James M. Newcomb1,2,* and
Winsor H. Watson, III1,2
1 Zoology Department and Center for Marine Biology, University of New Hampshire, Durham, NH 03824, USA and
2 Friday Harbor Laboratories, University of Washington, Friday Harbor, WA 98250, USA
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Fig. 1. (A) Drawing of the brain of Melibe leonina. The two fused ganglia that constitute most of the brain are the cerebral (C) and pleural (P) ganglia (also referred to jointly as the cerebropleural ganglia). Near the large commissure that connects the two halves of the brain are the paired tentacular lobes (T). The left and right pedal ganglia (PD) are lateral to the cerebropleural ganglia. Interneurons of the swim central pattern generator (CPG) are indicated on the right half of this drawing (although the CPG is actually bilateral). Swim interneuron I (SiI) is located in the cerebropleural ganglion. It projects to the ipsilateral pedal ganglion, where it synapses on swim interneuron II (SiII) and swim motoneurons (indicated as filled circles in the left pedal ganglion). SiII synapses with motoneurons in the ipsilateral pedal ganglion and with SiII and motoneurons in the contralateral pedal ganglion via the pedal connective (PC), which encircles the esophagus in vivo. S, statocyst. (B) Typical recording from swim motoneurons in an isolated brain. Contralateral motoneurons fire in anti-phase, producing the alternating rhythmic bursting pattern characteristic of fictive swimming. lSMN, left swim motoneuron; rSMN, right swim motoneuron.
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Fig. 2. Effects of sodium nitroprusside (SNP) on the swim motor program. (A) Control recording showing typical fictive swimming. Fifteen minutes after the addition of 1 mmol l–1 SNP, the period of the swim rhythm increased and became more erratic. This effect was reversible, as indicated by a return to a normal swimming pattern after a 23-min wash in seawater. (B) Reduced oxyhemoglobin blocked the effects of 1 mmol l–1 SNP. This confirms that the effects from SNP were in fact due to NO and not to some other chemical property of the NO donor. All recordings were from the same cell.
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Fig. 3. Effects of S-nitroso-N-acetylpenicillamine (SNAP) on the swim motor program. (A) Control recording showing typical fictive swimming. Seven minutes after the addition of 1 mmol l–1 SNAP, the period of the swim rhythm increased and became more erratic. This effect was not completely reversible, as indicated by a gradual return to a shorter swim cycle and a more consistent bursting pattern after a 20 min wash in seawater. (B) Reduced oxyhemoglobin blocked the effects of 1 mmol l–1 SNAP. All recordings were from the same cell.
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Fig. 4. Effects of 8-bromoguanosine 3',5'-cyclic monophosphate (8-Br-cGMP) on the swim motor program. The control recording showing typical fictive swimming. Six minutes after the addition of 1 mmol l–1 8-Br-cGMP, the pattern changed to one with a longer swim cycle and less consistency in the pattern. These effects were totally reversible after only a 2-min wash in seawater. This pattern was similar to the results with the NO donors and is thus suggestive of the involvement of a cGMP-dependent pathway in modulation of the swim central pattern generator by NO. All recordings were from the same cell.
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Fig. 5. Effects of sodium nitroprusside (SNP) on semi-intact preparations (N=3). Video analysis of swimming in semi-intact preparations was correlated with motoneuron bursting recorded from the brain of the same animal. After the addition of SNP, the period of motoneuron bursting and actual swimming increased significantly from control levels (t-test, P<0.05). In the single preparation that remained viable long enough, a 5-min wash in seawater resulted in a return to a normal swim period. Values are means ± S.E.M. Asterisks indicate a significant difference from control values.
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© The Company of Biologists Ltd 2002
