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Journal of Neuroscience, Vol 8, 49-63, Copyright © 1988 by Society for Neuroscience
An identified histaminergic neuron can modulate the outputs of buccal- cerebral interneurons in Aplysia via presynaptic inhibition
HJ Chiel, I Kupfermann and KR Weiss
Center for Neurobiology and Behavior, New York State Psychiatric Institute, College of Physicians and Surgeons, Columbia University, New York 10032.
We have identified 2 buccal-cerebral interneurons (BCIs), B17 and B18, that
appear to be involved in the coordination of feeding behavior in Aplysia.
The BCIs have their cell bodies in the buccal ganglion, but send axons to
the cerebral ganglion via the cerebral-buccal connectives. The BCIs appear
to make monosynaptic connections with neurons in the cerebral ganglion that
modulate extrinsic muscles involved in feeding behavior. B17 and B18 are
activated antiphasically during a motor program induced by stimulating the
esophageal nerve and appear to "read out" different phases of the buccal
program to different cells in the cerebral ganglion. B17 and B18 are not
necessary, and probably not sufficient, to generate the buccal program.
These BCIs, and other cells like them in the buccal ganglion, may be
capable of coordinating the activity of the intrinsic muscles of the buccal
mass with the activity of its extrinsic muscles, and perhaps with those of
the lips, mouth, and tentacles. Identified histaminergic neuron, C2, can
modulate the outputs of the BCIs onto their synaptic followers in the
cerebral ganglion. Firing of C2 inhibits spiking of the BCIs, probably via
cerebral-buccal interneurons. C2 also decreases the size of the EPSP that
B17 and B18 evoke in cerebral neuron C4. C2 appears to do so
monosynaptically, and it decreases the conductance of C4, ruling out one
possible postsynaptic mechanism of action. Variance analysis of the EPSPs
evoked by B18 supports the hypothesis that C2 acts presynaptically to
decrease the release of transmitter. Applications of histamine to the
solution bathing the neuron mimic the effect of firing C2 and reduce the
size of the EPSPs B18 induces in C4. The bath-applied histamine appears to
act directly on B18, since it elicits a voltage-dependent increased
conductance hyperpolarization recorded in the soma of B18, and the
hyperpolarization persists in a solution in which synaptic transmission has
been blocked. Histamine did not produce any marked changes of the duration
of a TEA-broadened somatic action potential of B18. To the extent that the
soma of B18 reflects the membrane properties of its synaptic terminal
region, the data suggest that histamine may produce presynaptic inhibition
by hyperpolarizing the synaptic terminal region.
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