An identified histaminergic neuron can modulate the outputs of buccal-cerebral interneurons in Aplysia via presynaptic inhibition.
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.
Chiel
H J
HJ
Center for Neurobiology and Behavior, New York State Psychiatric Institute, College of Physicians and Surgeons, Columbia University, New York 10032.
Kupfermann
I
I
Weiss
K R
KR
D000704:Analysis of Variance; D000818:Animals; D001048:Aplysia; D001921:Brain / Q000166:cytology / Q000502:physiology*; D002610:Cheek / Q000294:innervation*; D004435:Eating; D004558:Electric Stimulation; D006632:Histamine / Q000502:physiology*; D007395:Interneurons / Q000502:physiology*; D009043:Motor Activity / Q000502:physiology; D009433:Neural Inhibition; D009474:Neurons / Q000502:physiology*; D013569:Synapses / Q000502:physiology*
D006632:Histamine