Cortical influences on cervical motoneurons in the rat: recordings of synaptic responses from motoneurons and compound action potential from corticospinal axons

Abstract

The synaptic responses of cervical motoneurons to intracortical stimulation (ICS) of the motor cortex were studied in the rat by means of intracellular recordings. Motoneurons (n = 80) were identified either by their antidromic response to peripheral nerve electrical stimulation and/or by intracellular staining with biocytin. As a result of ICS (0.6-1.5 mA) of the contralateral motor cortex, the vast majority of motoneurons responded with EPSPs (77 out of 80), while only three motoneurons exhibited IPSPs. For increasing ICS intensities, the amplitude of the EPSPs in a given motoneuron increased, whereas their latency was not substantially affected. For the whole population of motoneurons, identified mainly by their antidromic response, the latency of the EPSPs was on average 8.45 ms (SD 1.6 ms), ranging from 4.7 to 12.6 ms. A very comparable latency distribution was obtained from the subpopulation of biocytin stained motoneurons (n = 23). In 7 of 19 tested motoneurons EPSPs could follow high frequencies (50-100 Hz) of stimulation without change of latency. The compound action potential (descending volley) travelling along corticospinal fibers reached the level of intracellular recording with a minimal latency estimated to be about 3 ms after ICS. The conduction velocity of corticospinal axons contributing to the descending volley was calculated to range from 9 to 19.7 m/s, based on morphometric measurements of conduction distance from the motor cortex and duration of the compound action potential. The time delay between the latency of descending volley and the latency of early EPSPs on the one hand, and frequency following properties of EPSPs on the other hand, suggest that some cervical motoneurons receive secure, most likely, indirect (presumably disynaptic) inputs from fast conducting corticospinal axons or direct contacts from slower conducting corticospinal fibers. The biocytin labeled cervical motoneurons exhibited extraordinary long dendritic trees, extending both laterally in the white matter near the edge of the spinal cord and medially in the gray matter as far as the midline of the spinal cord. The motoneurons were also characterized by the presence of one or several recurrent axon collaterals, ramifying profusely in the neuropil, with numerous boutons en passant and terminaux contacting most likely neighboring cervical neurons.