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Volume 17, Number 20, Issue of October 15, 1997 pp. 7703-7713
Copyright ©1997 Society for Neuroscience

Removal of Spike Frequency Adaptation via Neuromodulation Intrinsic to the Tritonia Escape Swim Central Pattern Generator

Received May 27, 1997; revised Aug. 5, 1997; accepted Aug. 6, 1997.

Paul S. Katz1 and William N. Frost2

1 Department of Biology, Georgia State University, Atlanta, Georgia 30303, and 2 Department of Neurobiology and Anatomy, University of Texas Medical School, Houston, Texas 77030

For the mollusc Tritonia diomedea to generate its escape swim motor pattern, interneuron C2, a crucial member of the central pattern generator (CPG) for this rhythmic behavior, must fire repetitive bursts of action potentials. Yet, before swimming, repeated depolarizing current pulses injected into C2 at periods similar those in the swim motor program are incapable of mimicking the firing rate attained by C2 on each cycle of a swim motor program. This resting level of C2 inexcitability is attributable to its own inherent spike frequency adaptation (SFA). Clearly, this property must be altered for the swim behavior to occur. The pathway for initiation of the swimming behavior involves activation of the serotonergic dorsal swim interneurons (DSIs), which are also intrinsic members of the swim CPG. Physiologically appropriate DSI stimulation transiently decreases C2 SFA, allowing C2 to fire at higher rates even when repeatedly depolarized at short intervals. The increased C2 excitability caused by DSI stimulation is mimicked and occluded by serotonin application. Furthermore, the change in excitability is not caused by the depolarization associated with DSI stimulation or serotonin application but is correlated with a decrease in C2 spike afterhyperpolarization. This suggests that the DSIs use serotonin to evoke a neuromodulatory action on a conductance in C2 that regulates its firing rate. This modulatory action of one CPG neuron on another is likely to play a role in configuring the swim circuit into its rhythmic pattern-generating mode and maintaining it in that state.

Key words: intrinsic neuromodulation; serotonin; nudibranch mollusc; repetitive firing; central pattern generator; after- hyperpolarization




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