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The Journal of Neuroscience, January 15, 1999, 19(2):845-858
A Pair of Reciprocally Inhibitory Histaminergic Sensory Neurons Are Activated within the Same Phase of Ingestive Motor Programs in Aplysia
Colin G. Evans1, Vera Alexeeva1, Jurgen Rybak1, Tuula Karhunen1, Klaudiusz R. Weiss1, 2, and Elizabeth C. Cropper1, 2 1 Department of Physiology and Biophysics and the 2 Fishberg Center for Research in Neurobiology, The Mt. Sinai Medical Center, New York, New York 10029
Previous studies have shown that each buccal ganglion in Aplysia contains two B52 neurons, one in each hemiganglion. We now show that there are two B52 neurons in a single buccal hemiganglion and four cells in an animal. We also show that the B52 neurons are histamine-immunoreactive and use reverse phase HPLC to show that the histamine-immunoreactive substance is authentic histamine. Previous studies have shown that the B52 neurons make numerous inhibitory synaptic connections with neurons active during the radula closing/retraction phase of ingestive motor programs. A computational model of the Aplysia feeding central pattern generator has, therefore, suggested that the B52 neurons play a role in terminating closing/retraction. Consistent with this idea we show that both B52 neurons fire at the beginning of radula opening/protraction. We also show that both B52 neurons are sensory neurons. They are depolarized when a flap of connective tissue adjacent to the buccal commissural arch is stretched. During ingestive feeding this is likely to occur at the peak of closing/retraction as opening/protraction begins. In the course of this study we compare the two ipsilateral B52 neurons and show that these cells are virtually indistinguishable; e.g., they use a common neurotransmitter, make the same synaptic connections, and are both sensory as well as premotor neurons. Nevertheless we show that the B52 neurons are reciprocally inhibitory. Our results, therefore, strikingly confirm theoretical predictions made by others that neurons that inhibit each other will not necessarily participate in antagonistic phases of behavior.
Key words: central pattern generator; feeding behavior; proprioceptive input; sensorimotor integration; half-center oscillator; histamine
Copyright © 1999 Society for Neuroscience 0270-6474/99/192845-14$05.00/0
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