Mechanisms underlying type I mGluR-induced activation of lobster gastric mill neurons.
In addition to ionotropic effects, glutamate and acetylcholine have metabotropic modulatory effects on many neurons. Here we show that in the stomatogastric ganglion of the lobster, glutamate, one of the main ionotropic neurotransmitters, modulates the excitability of gastric mill neurons. The neurons in this well-studied system produce rhythmic output to a subset of lobster foregut muscles. Recently, metabotropic glutamate receptor (mGluR) agonists were suggested as modulators of the rhythmic output, in addition to the previously described muscarinic modulation by acetylcholine. However, the cellular mechanisms responsible for these effects on the pattern are not known. Using intracellular recording methods and calcium imaging, we show that glutamate has an excitatory effect on specific neurons in the stomatogastric ganglion, which is mediated by mGluRs. Responses to the application of mGluR type I agonists are transient oscillations in the system, probably arising from network interactions. We show that the excitatory effect is sensitive to phospholipase-C and IP(3) and is G-protein dependent. The G-protein dependency was demonstrated by GDPbetaS and GTPgammaS injection into identified neurons. The depolarizations and oscillations were accompanied by an increase of intracellular Ca(2+) levels and correlated Ca(2+) oscillations. By using cyclopiazonic acid, an endoreticular Ca(2+) uptake inhibitor, we show that some internal calcium release may augment the response, but is not crucial for its production. Interestingly, although Ca(2+) concentration increase is typically associated with the phosphoinositide pathway, in the lobster, the Ca(2+) concentration increase-either voltage dependent or independent-cannot account for the observed depolarization.
Levi
Rafael
R
Institute for Nonlinear Science, University of California-San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0402, USA. rlevi@ucsd.edu
Selverston
Allen I
AI
D000818:Animals; D002118:Calcium / Q000378:metabolism; D002614:Chelating Agents / Q000494:pharmacology; D004533:Egtazic Acid / Q000031:analogs & derivatives / Q000494:pharmacology; D004566:Electrodes; D004594:Electrophysiology; D018690:Excitatory Amino Acid Agonists / Q000494:pharmacology; D018698:Glutamic Acid / Q000378:metabolism; D016244:Guanosine 5'-O-(3-Thiotriphosphate) / Q000494:pharmacology; D066298:In Vitro Techniques; D015544:Inositol 1,4,5-Trisphosphate / Q000502:physiology; D009474:Neurons / Q000187:drug effects / Q000502:physiology*; D033521:Palinuridae / Q000502:physiology*; D016318:Quisqualic Acid / Q000494:pharmacology; D018094:Receptors, Metabotropic Glutamate / Q000819:agonists / Q000502:physiology*; D015290:Second Messenger Systems / Q000502:physiology; D015398:Signal Transduction / Q000502:physiology; D013270:Stomach / Q000294:innervation; D010738:Type C Phospholipases / Q000502:physiology
D002614:Chelating Agents; D018690:Excitatory Amino Acid Agonists; D018094:Receptors, Metabotropic Glutamate; C104077:metabotropic glutamate receptor type 1; D016244:Guanosine 5'-O-(3-Thiotriphosphate); D018698:Glutamic Acid; D004533:Egtazic Acid; D015544:Inositol 1,4,5-Trisphosphate; D016318:Quisqualic Acid; D010738:Type C Phospholipases; C025603:1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid; D002118:Calcium