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The Journal of Neuroscience, September 15, 2001, 21(18):7331-7339

Long-Term Maintenance of Channel Distribution in a Central Pattern Generator Neuron by Neuromodulatory Inputs Revealed by Decentralization in Organ Culture

Adi Mizrahi¹, Patsy S. Dickinson¹, Peter Kloppenburg², Valerie Fénelon¹, Deborah J. Baro², Ronald M. Harris-Warrick², Pierre Meyrand¹, and John Simmers¹

¹ Laboratoire de Neurobiologie des Réseaux, Université Bordeaux I and Centre National de la Recherche Scientifique, Talence 33405, France, and ² Department of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853

Organotypic cultures of the lobster (Homarus gammarus) stomatogastric nervous system (STNS) were used to assess changes in membrane properties of neurons of the pyloric motor pattern-generating network in the long-term absence of neuromodulatory inputs to the stomatogastric ganglion (STG). Specifically, we investigated decentralization-induced changes in the distribution and density of the transient outward current, I_A, which is encoded within the STG by the shal gene and plays an important role in shaping rhythmic bursting of pyloric neurons. Using an antibody against lobster shal K⁺ channels, we found shal immunoreactivity in the membranes of neuritic processes, but not somata, of STG neurons in 5 d cultured STNS with intact modulatory inputs. However, in 5 d decentralized STG, shal immunoreactivity was still seen in primary neurites but was likewise present in a subset of STG somata. Among the neurons displaying this altered shal localization was the pyloric dilator (PD) neuron, which remained rhythmically active in 5 d decentralized STG. Two-electrode voltage clamp was used to compare I_A in synaptically isolated PD neurons in long-term decentralized STG and nondecentralized controls. Although the voltage dependence and kinetics of I_A changed little with decentralization, the maximal conductance of I_A in PD neurons increased by 43.4%. This increase was consistent with the decentralization-induced increase in shal protein expression, indicating an alteration in the density and distribution of functional A-channels. Our results suggest that, in addition to the short-term regulation of network function, modulatory inputs may also play a role, either directly or indirectly, in controlling channel number and distribution, thereby maintaining the biophysical character of neuronal targets on a long-term basis.

Key words: crustacean; stomatogastric ganglion; motor network; identified pyloric neuron; organ culture; decentralization; shal K⁺ channel; shal immunodetection; voltage clamp

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Copyright © 2001 Society for Neuroscience  0270-6474/01/21187331-09$05.00/0

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