Bistability in Spinal Motoneurons in Vivo: Systematic Variations in Rhythmic Firing Patterns

In the presence of the monoamines serotonin and norepinephrine, spinal motoneurons can exhibit bistable behavior, in which a brief period of excitatory input evokes prolonged self-sustained firing. A brief inhibitory input returns the cell to the quiescent state. To determine whether motoneurons differ in their capacity for bistable behavior, intracellular recordings were obtained in the decerebrate cat preparation. To enhance the likelihood of encountering bistable behavior, the noradrenergic alpha1 agonist methoxamine was applied to the ventral surface of the cord. The capacity of the cells to produce bistable behavior was assessed from the duration of self-sustained firing evoked by a brief (1.5 s) excitatory synaptic input from muscle spindle Ia afferents. About 35% (17 of 49) of the cells produced steady self-sustained firing for >3 s and were considered fully bistable. The other 32 cells ( approximately 65%) were partially bistable, with self-sustained firing lasting <3 s. Fully bistable cells tended to have lower current thresholds for spike initiation and slower axonal conduction velocities than did partially bistable cells. This suggests that fully bistable motoneurons innervate fatigue resistant muscle fibers. The frequency-current (F-I) relations of the motoneurons were characterized with slow triangular current ramps. Fully bistable cells displayed an acceleration in firing rate immediately on initiation of rhythmic firing. The F-I gain after completion of the acceleration was positive. Fully bistable cells also displayed a hysteresis in the current level for firing threshold with the ascending threshold occurring at substantially higher current level than the descending one. Additionally, these current thresholds usually were centered about zero current, so that the ascending current threshold was positive while the descending current threshold was negative. This negative offset meant that fully bistable cells could exhibit tonic firing without depolarizing injected current. Partially bistable cells exhibited very different F-I characteristics. Firing rate acceleration was just as large as in fully bistable cells but did not occur until well above the current level needed to initiate rhythmic firing. F-I gain after acceleration was negative, there was little to no hysteresis between the ascending and descending firing thresholds, and both thresholds were above the zero current level. These properties of partially bistable cells suggest their functional role is in tasks requiring relatively brief, high forces. The low thresholds of fully bistable cells mean they will be readily recruited in low force tasks like posture, where their prolonged self-sustained firing would be advantageous.