The potential for understanding the synaptic organization of human motor commands via the firing patterns of motoneurons

Abstract

Motoneurons are unique in being the only neurons in the CNS whose firing patterns can be easily recorded in human subjects. This is because of the one-to-one relationship between the motoneuron and muscle cell behavior. It has long been appreciated that the connection of motoneurons to their muscle fibers allows their action potentials to be amplified and recorded, but only recently has it become possible to simultaneously record the firing pattern of many motoneurons via array electrodes placed on the skin. These firing patterns contain detailed information about the synaptic organization of motor commands to the motoneurons. This review focuses on parameters in these firing patterns that are directly linked to specific features of this organization. It is now well established that motor commands consist of three components, excitation, inhibition, and neuromodulation; the importance of the third component has become increasingly evident. Firing parameters linked to each of the three components are discussed, along with consideration of potential limitations in their utility for understanding the underlying organization of motor commands. Future work based on realistic computer simulations of motoneurons may allow quantitative "reverse engineering" of human motoneuron firing patterns to provide good estimates of the relative amplitudes and temporal patterns of all three components of motor commands.

Keywords: electrode array; motoneuron; motor unit.

Fig. 1.

Illustration of the 2 types of electrode arrays that are currently being used for high-density motor unit recordings of the muscle. Ai: rigid arrays are used for multiunit recordings directly on the muscle surface in vivo in animal experiments. Aii and Aiii: flexible arrays are used on the surface of the skin for multiunit recordings in humans. B: spike trains from a human subject experiment illustrating the spike trains from 19 motor units during an increasing/decreasing torque ramp. IED, interelectrode distance.

Fig. 2.

Three basic interaction patterns for excitatory and inhibitory inputs to motoneurons: 1) Excitation (green) can vary against a background of tonic (constant) inhibition (red); 2) excitation and inhibition can vary out of phase of each other in a “push-pull” fashion, producing a larger net change in excitability than varying each input individually; and 3) excitation and inhibition can vary in phase in a “balanced” fashion.

Fig. 3.

Intracellular recording of a spinal motoneuron. A triangular current ramp is injected via the intracellular recording electrode. In the absence of persistent inward currents (PICs) (low neuromodulatory state) the change in firing frequency is linear and follows the pattern of current injection (red trace). When PICs are present (high neuromodulatory state) the firing behavior is nonlinear and shows strong initial acceleration and on-off hysteresis (green trace).

Fig. 4.

A: computer simulations of motoneuron firing patterns in response to slowly increasing and decreasing synaptic conductances. The acceleration, saturation, and hysteresis typically seen in motoneurons with prominent persistent inward currents in vivo are evident. Firing rate is presented in impulses per second (imp/s). B: motor unit discharge patterns from 2 motor units from the tibialis anterior muscle from a human subject in response to slow isometric contractions. Discharge rate is presented in pulses per second (pps). The firing behavior is strikingly similar to the simulations in A, showing the key characteristics imparted by persistent inward currents. The “ΔF” technique compares the firing rates between a higher (test)- and a lower (control)-threshold motor unit. The control unit’s firing rate is used to estimate the synaptic drive to the motor pool. During slowly increasing and decreasing contractions the control unit firing rate at recruitment and derecruitment is compared to the corresponding firing rates of the test unit. This technique measures changes in the recruitment/derecruitment thresholds of the test unit to detect changes in intrinsic excitability (presence of persistent inward currents).

Fig. 5.

Schematic of the distribution of synaptic inputs across motoneuron types shows that synaptic sources are not uniformly distributed. Additionally, synaptic sources do not have a uniform effect on each type of motoneuron (S vs. F). Cortical and rubrospinal inputs produce much greater (up to 9 times) effects in F motoneurons than they do in S motoneurons. Vestibular inputs are about twice as strong in F motoneurons than in S. Ia inputs have the strongest effect in S motoneurons, being about twice that in F motoneurons. This nonuniform distribution and effect of inputs on motoneurons greatly affects recruitment by compressing threshold ranges across motoneuron type.

Fig. 6.

Computer simulation of 3 possible combinations of inhibition and excitation and the resulting firing patterns each produces: 1) a background of steady inhibition (red) superimposed on increasing then decreasing excitation (green); 2) inhibition changing out of phase with excitation, the “push-pull’ arrangement; 3) inhibition and excitation covarying in phase, the “balanced” arrangement. Arrangements 1 and 2 closely resemble firing patterns seen in animal and human experiments.