Motor activity in the isolated spinal cord of the chick embryo: synaptic drive and firing pattern of single motoneurons

Abstract

The cellular mechanisms underlying embryonic motility were investigated using intracellular recording from motoneurons and electrotonic recording from muscle nerves during motor activity generated by an isolated spinal cord preparation of 12- to 15-d-old chick embryos. DC-coupled recordings from sartorius (a flexor) and femorotibialis (an extensor) muscle nerves revealed that both sets of motoneurons were depolarized at the same time in each cycle even when the motoneurons fired out of phase. Sartorius motoneurons fired briefly on the rising phase of the depolarization and then stopped firing before discharging a second burst of spikes as the depolarization decayed. By contrast, femorotibialis motoneurons fired at the peak of their depolarization, which was coincident with the interruption in sartorius activity. Intracellular recordings from antidromically identified motoneurons confirmed that flexor and extensor motoneurons were depolarized at the same time during each cycle of activity. The discharge of femorotibialis motoneurons, and others presumed to be extensors, followed changes in membrane potential so that maximal firing occurred during peak depolarization. The relationship between discharge and membrane potential was different in sartorius motoneurons (and in others presumed to be flexors) because they fired briefly on the rising phase of the depolarization and then stopped firing during peak depolarization. In some of these cells firing resumed as the membrane potential decayed back to rest. Intracellular injection of depolarizing current into sartorius motoneurons during motor activity reversed the direction of the membrane potential change from depolarizing to hyperpolarizing during the pause in sartorius discharge. In addition, the discharge evoked by the depolarizing current was blocked during the reversed part of the synaptic potential revealing its inhibitory nature. The occurrence of the IPSP was accompanied by a large reduction in motoneuronal input impedance. Injection of depolarizing current steps into motoneurons produced steady firing with no evidence of a pause in discharge, indicating that the depolarization accompanying synaptic activity was not responsible for the pause in firing of flexor motoneurons. These results suggest that flexor and extensor motoneurons receive a similar depolarizing drive from a common set of excitatory premotor interneurons. The alternating pattern of flexor and extensor discharge is produced, in part, by the timing of a depolarizing IPSP coincident with extensor activity that silences flexor discharge.(ABSTRACT TRUNCATED AT 400 WORDS)

GABA A transmission is a critical step in the process of triggering homeostatic increases in quantal amplitude

“…Therefore, levels of released GABA would be monitored as a proxy for activity. Embryonic movements are likely to be a reliable indicator of spinal SNA because electromyographic recordings in ovo during embryonic movements are remarkably similar to motoneuron recordings during in vitro SNA (30)(31)(32)(33). It is also likely that SNA that recovers after antagonist injections in the egg is similar to SNA before the antagonists were added because similar findings have been observed in the in vitro spinal cord preparation (22).…”

Modeling Spontaneous Activity in the Developing Spinal Cord Using Activity-Dependent Variations of Intracellular Chloride

“…Closely related to this point is the fact that we assumed that the effects of the chloride conductance are exclusively excitatory, but the balance of excitatory and inhibitory effects of GABA depends on the synaptic location (Sernagor et al, 1995;Gulledge and Stuart, 2003). In fact, it has been shown previously that the conductance can sometimes be functionally inhibitory, presumably because of shunting (O'Donovan, 1989;Sernagor et al, 1995;Marchetti et al, 2002).…”

Selective Fasciculation and Divergent Pathfinding Decisions of Embryonic Chick Motor Axons Projecting to Fast and Slow Muscle Regions

“…To address this, we recorded EMGs from the fast and slow regions of the SART, AITIB, and I FI B muscles. Muscle activity, as recorded by EMGs in the chick, has been shown to mimic the activity of the innervating motoneurons (Landmesser and O'Donovan, 1984a,b;O'Donovan, 1989). Therefore, by measuring EMGs, we were able to determine the activity pattern of the motoneurons projecting to fast and slow muscle regions.…”

“…As described previously (Landmesser and O'Donovan, 1984a;O'Donovan, 1989;Ho and O'Donovan, 1993;Sernagor et al, 1995;Sholomenko and O'Donovan, 1995), stimulation of descending input with a single electrical shock to the thoracic cord activates a central pattern generator in the lumbosacral cord, setting off a series of highly stereotyped motoneuron bursts (or cycles) characteristic for each muscle. Figure 9A shows the EMG to one such muscle, the AITIB, after a single stimulus to the cord.…”