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The Journal of Neuroscience, March 1, 2002, 22(5):1985-1993
Highly Dissimilar Behaviors Mediated by a Multifunctional Network
in the Marine Mollusk Tritonia diomedea
Ion R.
Popescu and
William N.
Frost
Department of Cell Biology and Anatomy, Finch University of Health
Sciences, The Chicago Medical School, North Chicago, Illinois 60064
Several motor networks have now been found to be multifunctional,
in which one group of neurons participates in the generation of
multiple behavioral motor programs. Not surprisingly, the behaviors involved are frequently closely related, often using the same or
similar muscle groups. Here we describe an interneuronal network in the
marine mollusk Tritonia diomedea that is involved in
producing two highly dissimilar behaviors, rhythmic, muscle-based
escape swimming and nonrhythmic, cilia-mediated crawling. Several
observations support this conclusion. First, the dorsal swim
interneurons (DSIs) of the swim central pattern generator (CPG)
directly excite Pedal neuron 21 (Pd21) and Pd5, the only identified
cilia-activating efferent neurons in Tritonia. Second,
stimulation of a single DSI elicits beating of the foot cilia in
semi-intact preparations and crawling in intact animal treadmill
preparations. Third, the DSIs fire at an elevated rate for nearly 1 hr
after a swim motor program, which correlates reasonably well with the
period freely behaving animals were found to crawl after they swam.
Fourth, silencing the tonically active DSIs after a swim motor program substantially reduces or eliminates ongoing cilia neuron firing, indicating that the DSIs are major contributors to the synaptic input
driving these cells. Finally, all of the other swim CPG neurons also
connect to the cilia neurons, most monosynaptically. Taken together,
these observations indicate that the Tritonia swim CPG
network participates in producing both escape swimming and crawling.
Given the extreme differences between these behaviors -rhythmic versus
tonic, muscular versus ciliary, and brief versus prolongedthese findings reveal a striking versatility for a small multifunctional network.
Key words:
Tritonia; multifunctional network; central
pattern generator; cilia; locomotion; mollusk; CPG; evolution; multifunctional neuron
Copyright © 2002 Society for Neuroscience 0270-6474/02/2251985-09$05.00/0
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