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First published online November 30, 2007
Journal of Experimental Biology 210, 4448-4456 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.010009

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Nitrergic modulation of an oviposition digging rhythm in locusts

Philip L. Newland^* and Paul Yates

School of Biological Sciences, Biomedical Science Building, University of Southampton, Bassett Crescent East, Southampton, SO16 7PX, UK

View larger version (53K): [in this window] [in a new window]   Fig. 1. The oviposition digging rhythm. (A) Photographs showing the cyclical movements of the locust ovipositor valves. (i) The dorsal valves (D.V.) and ventral valves (V.V.) in their closed positions. (ii) The protractive movements of the ovipositor push the valves out of the abdomen. (iii,iv) The opening movements of the ovipositor valves can be seen (iv=fully open). (v,vi) The simultaneous closing and retraction movements of the valves, returning the valves back to their original closed position. Small arrows indicate the direction of movement of the valves. (B) A recording from the left and right dorsal and ventral opener muscles. All four muscles were active and in phase during the opening (O) movement of the digging rhythm. `C' represents the closed phase of the digging rhythm. (C) A recording from a ventral opener and ventral closer muscle. The ventral closer muscle bursts (C) directly after the ventral opener muscle (O) in order to pull the valves shut. (D) A recording from the ventral opener and ventral retractor muscle. The ventral retractor muscle bursts (R) directly after the ventral opener muscle.

View larger version (25K): [in this window] [in a new window]   Fig. 2. The effect of NO on the cycle frequency of the digging rhythm. (Ai) The bath application of 20 mmol l–1 L-arginine caused a statistically significant increase in the oviposition cycle frequency (t=2.44, *P<0.05, mean ± s.e.m. from eight animals). (Aii) An example showing the effect of a 10 min bath application of 20 mmol l–1 L-arginine on the ovipositor valve opener muscles. The number of cycles of muscle activity increased from a control value of 5 to 6 after L-arginine application within the same time period. After a 30 min wash with locust saline, the number of cycles of opener muscle activity returned to the control value. (Bi) The effect of the NO donor PAPANONOate (PNONO) on the cycle frequency. A 10 min bath application of 0.2 mmol l–1 PAPANONOate caused a statistically significant increase in the cycle frequency (t=–2.82, P<0.01) (*=P<0.05). Mean ± s.e.m. of five animals. (Bii) An example showing a 10 min bath application of 0.2 mmol l–1 PAPANONOate resulted in a significant increase in the number of cycles of muscle activity within the same time period. A 30 min wash with locust saline resulted in the digging rhythm partially returning to its original cycle frequency.

View larger version (25K): [in this window] [in a new window]   Fig. 3. The effects of the NO donor SNAP on oviposition digging. (Ai) A 10 min bath application of SNAP resulted in a statistically significant increase in the cycle frequency of the digging rhythm (t=2.5, *P<0.05, mean ± s.e.m. of five animals). (Aii) An example showing the effect of increased exogenous levels of NO on the digging rhythm. A 10 min bath application of 0.2 mmol l–1 SNAP resulted in an increase in the number of cycles of muscle activity while a 30 min wash with locust saline resulted in the number of cycles of muscle activity returning to control. (B) The effect of bath application of the inactive isomer of SNAP, NAP, on the cycle frequency. A 10 min bath application of 0.2 mmol l–1 NAP had no effect on the cycle frequency (t=0.14, P>0.05, N=4). (C) A 10 min bath application of 0.2 mmol l–1 degassed SNAP (DG SNAP) had no significant effect on cycle frequency (t=0.17, P>0.05, mean ± s.e.m. from four animals). (D) Bath application of normal locust saline similarly resulted in no significant effect on cycle frequency (t=–1.81, P>0.05, mean ± s.e.m. from four animals).

View larger version (23K): [in this window] [in a new window]   Fig. 4. The effect of inhibiting NO synthesis by bath application of the NOS inhibitor L-NAME. (Ai) A 10 min bath application of 20 mmol l–1 L-NAME caused a statistically significant decrease in the cycle frequency of the digging rhythm (t=2.08, *P<0.05, mean ± s.e.m. from eight animals). (Aii) The effects of L-NAME were reversed by a 30 min wash with locust saline. (Bi) A 10 min bath application of the inactive isomer 20 mmol l–1 D-NAME caused no statistically significant change in cycle frequency (t=0.12, P>0.05, mean ± s.e.m. from four animals). (Bii) An example showing that a 10 min bath application of 20 mmol l–1 D-NAME resulted in no significant decrease in the number of cycles between test and control values.

View larger version (12K): [in this window] [in a new window]   Fig. 5. The effect of removing endogenous NO by bath application of the NO scavenger PTIO. (Ai) A 10 min bath application of 0.5 mmol l–1 PTIO caused a statistically significant decrease in cycle frequency (t=2.04, *P<0.05, N=11). A 30 min wash with locust saline resulted in the digging rhythm returning to its original cycle frequency. (Aii) An example showing that a 10 min bath application of 0.5 mmol l–1 PTIO resulted in a decrease in the number of cycles within the same time period.

View larger version (31K): [in this window] [in a new window]   Fig. 6. The effects of the sGC inhibitor, ODQ, and the cGMP analogue, 8-Br-cGMP, on the digging rhythm. (Ai) A 10 min bath application of 0.1 mmol l–1 ODQ resulted in a significant decrease in cycle frequency (t=2.85, *P<0.05, mean ± s.e.m. from five animals). (Aii) An example showing that a 10 min bath application of ODQ resulted in a decrease in the cycle number that was reversed by a 30 min wash with locust saline. (B) The simultaneous bath application of L-arginine and ODQ resulted in no statistically significant difference between control and test values (t=–1.34, P>0.05, mean ± s.e.m. from five animals). (Ci) A 10 min bath application of 0.1 mmol l–1 8-Br-cGMP resulted in a significant increase in cycle frequency of the digging rhythm (t=2.22, *P<0.05, mean ± s.e.m. from six animals). A 30 min wash with locust saline did not result in the cycle frequency returning back to its original value. (Cii) An example showing that bath application of 8-Br-cGMP resulted in an increase in the number of cycles of muscle activity of the digging rhythm, from a control value of four cycles to a test value of five within the same time period.

View larger version (26K): [in this window] [in a new window]   Fig. 7. The effect of the generic protein kinase inhibitor H-7 and the PKG inhibitor KT-5823 on the digging rhythm. (Ai) A 10 min bath application of 0.1 mmol l–1 H-7 resulted in a significant decrease in cycle frequency (t=4.93, *P<0.05, mean ± s.e.m. from five animals). A 30 min wash with locust saline resulted in a partial recovery of the digging rhythm to control levels. (Aii) A 10 min bath application of H-7 resulted in a decrease in the number of cycles (three cycles) compared with control (five cycles). A 30 min wash with locust saline resulted in a partial recovery of the digging rhythm to control levels. (Bi) A 10 min bath application of 10 µmol l–1 KT-5823 resulted in a significant decrease in the cycle frequency (t=2.8, *P<0.05, mean ± s.e.m. from five animals). (Bii) A 10 min bath application of KT-5823 resulted in a decrease in the number of cycles (five cycles) from a control value of six. This particular recording shows that a 30 min wash with locust saline did not result in the number of cycles returning to its control value.