Characterization of a radula opener neuromuscular system in Aplysia.
Evans, C. G., S. Rosen, I. Kupfermann, K. R. Weiss, and E. C. Cropper.
Department of Physiology and Biophysics, and 2the Fishberg Center for
Research in Neurobiology, The Mt. Sinai Medical Center, One Gustave L. Levy
Place, New York, NY 10029; 3Center for Neurobiology & Behavior, The New York
State Psychiatric Institute, 722 W 168 Street, New York, NY 10032; Departments
of 4Physiology, and 5Psychiatry, Columbia University, College of Physicians &
Surgeons, New York, NY 10032.
APStracts 3:0066N, 1996.
SUMMARY AND CONCLUSIONS
1) Several lines of evidence suggest that the I7-I10 muscle group contributes
to the radula opening phase of behavior in Aplysia ; (a) extracellular
stimulation of these muscles in reduced preparations causes the halves of the
radula to separate, (b) synaptic activity can be recorded from muscles I7-I10
in intact animals when the radula is opening, and (c) motor neurons
innervating I7-I10 are activated out of phase with retractor/closer motor
neurons during cycles of buccal activity driven by the cerebral-to-buccal
interneuron 2 (CBI-2). 2) All of the opener muscles are innervated by the B48
neurons, a bilaterally symmetrical pair of cholinergic motor neurons. B48
neurons produce EJPs in opener muscle fibers that summate to produce muscle
contractions. Contraction size is determined by the size of depolarization in
muscle fibers and/or by action potentials that are triggered by summation of
B48-evoked EJPs. 3) In addition to input from B48 neurons opener muscles also
receive excitatory input from the cholinergic multi-action neurons B4/B5. EJPs
evoked by stimulation of neurons B4/B5 are one tenth the size of B48-evoked
EJPs. Consequently, changes in muscle tension produced by B4/B5 activity are
relatively small. In contrast to B48 neurons B4/B5 are likely to be active
during the closing/retraction phase of behavior. During cycles of buccal
activity driven by neuron CBI-2, neurons B4/B5 fire in phase with
closer/retractor motor neurons. Thus, opener muscles may develop a modest
amount of tension during the closing/retraction phase of behavior as a result
of synaptic input from neurons B4/B5. 4) Opener muscles may also develop
tension during closing/retraction simply by virtue of the fact that they have
been stretched. When isolated opener muscles are lengthened, depolarizations
are recorded from individual muscle fibers, and muscle tension increases. With
sufficient changes in fiber length action potentials are elicited. These
action potentials produce twitch-like muscle contractions that become rhythmic
with maintained stretch. Stretch-activated depolarizations are generally first
apparent when fiber length is increased by one mm. Four to five mm length
changes are generally necessary to elicit twitch-like muscle contractions. One
to two mm changes in muscle length are observed when the opener muscle's
antagonist, the accessory radula closer (ARC) is activated in reduced
preparations. 5) Stretch may also modulate B48-induced contractions of the
opener muscles. When muscle length is increased, B48-elicited contractions of
the I7 muscle are larger. These increases in contraction amplitude are
accompanied by decreases in contraction latency. 6) We conclude that muscles
I7-I10 contract vigorously in response to strong excitatory input from neuron
B48 and contribute to radula opening. Stretch may potentiate this activity.
Thus, if radula closer muscles contract vigorously and pull on the opener
muscles, the opener muscles will respond by contracting more vigorously
themselves. This may be a mechanism for maintaining amplitude relationships
between antagonistic muscles. Additionally, it is likely that the opener
muscles will develop at least a modest amount of tension during
closure/retraction of the radula. Part of this activation may derive from the
weak excitatory input that they receive from neurons B4/B5. Another part may
derive from the stretch. One function of this co-contraction may be to act as
a brake on closure, bringing this phase of feeding behavior to a smooth halt.
Received 17 January 1996; accepted in final form 19 March 1996.
APS Manuscript Number J27-6.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 1 April 96