Rhythmic spontaneous activity in the developing avian auditory system

Abstract

Microelectrode recordings of spontaneous multiple unit activity were made from nucleus magnocellularis (NM) and nucleus laminaris (NL), second- and third-order nuclei in the chick auditory system, between 14 and 19 d of incubation (E14-E19). Spontaneous firing in E14-E18 embryos occurred in synchronous bursts at periodic intervals. A rhythmic pattern of spontaneous firing was also observed in the auditory nerve but not in nonauditory regions of the brain-stem. The mean interburst interval in NM and NL decreased from 4.9 sec at E14-E15 to 2.1 sec at E18. By E19, 2 d prior to hatching, synchronous bursting was replaced by an unpatterned, steady level of firing comparable to the background discharge that is present in NM and NL of hatchling birds. Bursting was not correlated with heart beat or respiration and was not affected by removal of the middle-ear ossicle. Rhythmic bursting could be reset, blocked, or induced by sound stimulation. Cochlea removal or pharmacological blockade of auditory nerve activity with TTX eliminated bursting. These results indicate that the synchrony and rhythmicity of impulse firing reflect normal physiological activity, most likely of cochlear origin. The present findings show that spontaneous activity in the embryonic avian auditory system, like that in the immature mammalian visual pathway (Maffei and Galli-Resta, 1990; Meister et al., 1991), occurs in a synchronously rhythmic pattern. This similarity raises the possibility that such activity may be a general feature of early sensory system development. Patterned spontaneous firing in the chick takes place during a period of embryogenesis when auditory thresholds are high and when it is unlikely that physiological function in ovo is influenced significantly by normally occurring levels of airborne sound. Brainstem auditory neurons undergo substantial changes in structure and innervation during this same period. It is speculated that the temporal pattern of spontaneous discharge may provide cues that contribute to these developmental events.