Perinatal switch from synchronous to asynchronous activity of motoneurons: link with synapse elimination

Synaptic competition is a basic feature of developing neural connections. To shed light on its dependence on the activity pattern of competing inputs, we investigated in vivo rat motoneuronal firing during late embryonic and early neonatal life, when synapse elimination occurs in muscle. Electromyographic recordings with floating microelectrodes from tibialis anterior and soleus muscles revealed that action potentials of motoneurons belonging to the same pool have high temporal correlation. The very tight linkage, a few tens of milliseconds, corresponds to the narrow time windows of published paradigms of activity-dependent synaptic plasticity. A striking change occurs, however, soon after birth when motoneuronal firing switches to the adult uncorrelated type. The switch precedes the onset of synapse elimination, whose time course was determined with confocal microscopy. Interestingly, the soleus muscle, whose motoneurons switch to desynchronized activity later than those of the tibialis anterior muscle, also exhibits delayed synapse elimination. Our findings support a developmental model in which synchronous activity first favors polyneuronal innervation, whereas an asynchronous one subsequently promotes synapse elimination.