Development of synchronized activity of cranial motor neurons in the segmented embryonic mouse hindbrain.

Abstract

Spontaneous electrical activity synchronized among groups of related neurons is a widespread and important feature of central nervous system development. Among the many places from which spontaneous rhythmic activity has been recorded early in development are the cranial motor nerve roots that exit the hindbrain, the motor neuron pool that, at birth, will control the rhythmic motor patterns of swallow, feeding and the oral components of respiratory behaviour. Understanding the mechanism and significance of this hindbrain activity, however, has been hampered by the difficulty of identifying and recording from individual hindbrain motor neurons in living tissue. We have used retrograde labelling to identify living cranial branchiomeric motor neurons in the hindbrain, and [Ca2+]i imaging of such labelled cells to measure spontaneous activity simultaneously in groups of motor neuron somata. We find that branchiomeric motor neurons of the trigeminal and facial nerves generate spontaneous [Ca2+]i transients throughout the developmental period E9.5 to E11.5. During this two-day period the activity changes from low-frequency, long-duration events that are tetrodotoxin insensitive and poorly coordinated among cells, to high-frequency short-duration events that are tetrodotoxin sensitive and tightly coordinated throughout the motor neuron population. This early synchronization may be crucial for correct neuron-target development.