Computer simulation of group Ia EPSPs using morphologically realistic models of cat α-motoneurons

Morphological and electrophysiological data on the electrotonic structure of six triceps surae α-motoneurons and on the number and location of 202 Group Ia synapses making contact with ankle extensor motoneurons, previously obtained in this laboratory, we used to construct computer models to examine the generation of composite monosynaptic Group Ia excitatory postsynaptic potentials (EPSPs). A total of 300 active synapses, each generating conductance transients based on voltage-clamp data and having activation times temporally dispersed (range ~1.3 ms) according to the conduction velocity profile of Group Ia-afferents, were used to generate composite EPSPs. The shape indexes (foot-to-peak rise times and half widths) of simulated EPSPs matched those of experimentally observed Ia EPSPs reasonably well, although the rise times were, on average, ~0.25 ms longer in the simulated EPSPs. This may indicate that the effective temporal dispersion of actual Group Ia monosynaptic EPSPs is less than that the temporal asynchrony used in the simulations. The peak amplitudes of simulated composite EPSPs (6-14 mV), as well as EPSPs produced by single somatic synapses (80-300 μV), were comparable to those found in experimental data. Simulated EPSPs in motoneuron models with two forms of nonuniform R(m) distribution ('step' increase from low values of R(m) on the soma to much higher but uniform values in the dendrites, versus gradual monotonic 'sigmoidal' increases from soma to distal dendrites) were similar in shape and amplitude. This prevented choosing one or the other R(m) model as more 'correct'. Transmembrane voltages at synaptic sites in motoneuron dendrites during generation of composite Ia EPSPs had peak amplitudes less than twice those of the somatic EPSP. The amount of nonlinearity during EPSP production was assessed by making the delivery of synaptic current independent of the local transmembrane voltage. This non-linearity was modest (<10%) during composite EPSP generation, consistent with previous experimental evidence. The local voltages produced in various parts of different dendrites during composite EPSP generation depended on the number and location of active synapses and on the electrotonic structure of the particular dendrite. The results show that dendrites that project in different directions away from the motoneuron soma could, in principle, exhibit different degrees of interaction between Ia and other synaptic inputs. Although produced by the same number of active synapses, the simulated composite Ia EPSPs varied over a two-fold range of peak amplitude in relation to motor-unit type, cell input resistance, and cell size (total membrane area). One major factor that accounted for this variation was the overall density of active synapses, i.e., synaptic number/total postsynaptic membrane area. Given a constant number of active synapses, the smaller motoneurons had correspondingly higher synaptic densities and larger Ia EPSP amplitudes. A second factor was the high conductance, or 'leakiness', of the juxtasomatic membrane, most conveniently expressed in terms of the dendritic-to-somatic conductance ratio, ρ, that was necessary to reconcile the morphology and electrophysiology of the original neuron models. The motoneurons with relatively high somatic conductance and correspondingly low values of ρ exhibited smaller EPSP amplitudes for a given synaptic density. It remains unclear to what extent high juxtasomatic conductance represents an artifact produced by intracellular penetration.