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The cellular mechanisms by which afferents influence their target neurons were investigated using a slice preparation of the chick brain- stem auditory system. Each brain slice contained portions of the auditory nerve and the second-order auditory nucleus, nucleus magnocellularis (NM), bilaterally. NM neurons on one side of the slice were stimulated either orthodromically, via activation of the ipsilateral auditory nerve, or antidromically, via electrical stimulation of their axons. NM neurons on the other side of the slice were not stimulated and served as a within-animal control population. Evoked activity was monitored extracellularly in all preparations. Orthodromic activation of NM neurons for either 1.5 or 3.5 hr resulted in enhanced protein synthesis by these neurons. This result is similar to those of previous in vivo experiments (Steward and Rubel, 1985; Born and Rubel, 1988). When slices were maintained in a medium having low Ca2+ and high Mg2+ concentrations, both synaptic transmission from the auditory nerve to NM and also the difference in protein synthesis between the stimulated and unstimulated sides of the brain were blocked. Antidromic activation of NM neurons did not enhance protein synthesis, but rather resulted in reliably less synthesis by the stimulated cells. Together, these results suggest that activity- dependent release of some “trophic” substance from the auditory nerve is necessary for this form of transneuronal regulation. Electrical activity of the postsynaptic neuron per se is not sufficient for increasing protein synthesis in these cells.

Transneuronal regulation of protein synthesis in the brain-stem auditory system of the chick requires synaptic activation