Gap junctions are intercellular channels that allow direct, low resistance, electrical and chemical communication between neighbouring cells. Such coupling, which is particularly prevalent early in development, is rapid compared to chemical synaptic transmission and allows the diffusion of relatively large molecules between cells. An important function of electrical coupling is to synchronize neuronal activity (Kiehn & Tresch, 2002). This may be less appropriate to the regulation of more mature networks, indicating that functional de-coupling of gap junctions could contribute to neural network development. In hatchling Xenopus frog embryos, motorneurones that are rhythmically active during swimming, are coupled to their near neighbours via electrical synapses. This coupling is thought to ensure that homonymous motorneurones all fire their single impulse per cycle synchronously (Perrins & Roberts, 1995). However, early in larval development, neurones can fire repetitively in each cycle and ventral root bursts become desynchronized, leading to the hypothesis that a reduction in gap junction coupling might be responsible. We studied the effects of a gap junction blocker, carbenoxolone (CBX; 100-200 µM) on fictive swimming and on the initiation of swimming via skin stimulation in (stage 37/38) Xenopus embryos.We monitored the effects of CBX on the transmission of the skin impulse through the embryos epithelium. Skin cells can generate a cardiac-like impulse of ca. 100mV amplitude and 100ms duration, which propagates to neighbouring cells via gap junctions at rates of ca. 5cm/s-1 (Roberts & Stirling, 1971). CBX reduced conduction rates through the skin; impulses generated by a current pulse applied to the caudal tail skin were delayed in reaching more rostral regions (n=9). Thus CBX can impair transmission through the electrically coupled network of skin cells. In the presence of CBX a single stimulus could lead to multiple skin impulses and impulses could sometimes occur spontaneously. Next, the effects of CBX on fictive swimming were examined. Normally, each cycle comprises a biphasic compound ventral root burst of ca. 5-7 ms. CBX reduced swim episode durations, with an associated increase in motor burst durations (n=6). The increase in burst durations is consistent with a de-synchronization of motor activity leading to the conclusion that electrical coupling is necessary to synchronize motorneurone activity. We propose that a decrease in coupling during development contributes to the maturation of larval swimming.
University of Glasgow (2004) J Physiol 557P, C40
Communications: The gap junction blocker carbenoxolone affects sensory processing and motor pattern generation in Xenopus embryos.
K.T. Sillar, W.J. Heitler and S.D. Merrywest
School of Biology, University of St. Andrews, St. Andrews, UK
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Where applicable, experiments conform with Society ethical requirements.