Adaptation of cat motoneurons to sustained and intermittent extracellular activation.

Abstract

SUMMARY1. The main purpose of this study was to quantify the adaptation of spinal motoneurons to sustained and intermittent activation, using an extracellular route of stimulating current application to single test cells, in contrast to an intracellular route, as has been used previously. In addition, associations were tested between firing rate properties of the tested cells and other type (size)-related properties of these cells and their motor units.2. Motoneurons supplying the medial gastrocnemius muscle of the deeply anaesthetized cat were stimulated for 240 s with microelectrodes which passed sustained extracellular current at 1-25 times the threshold for repetitive firing. Many cells were also tested following a rest period with intermittent 1 s current pulses (duration 600 ms) at the same relative stimulus strength. Cell discharge was assessed from the EMG of the motor unit innervated by the test neuron. The motoneurons and their motor units were assigned to four categories (i.e. types FF, FR, S and F; where F = FF + FR) based on conventional criteria. In all, twenty F (16 FF, 4 FR) and fourteen S cells were studied with sustained stimulation. Thirty of these cells (17 F, 13 S) 4. All cells exhibited a delay from the onset of current to the first spike, followed by a brief accelerating discharge that was followed by a slower drop in firing rate. Some cells (21 of 34 with sustained activation; 20 of 32 with intermittent) exhibited doublet discharges (interspike intervals < 10 ms) that were intermingled with the more predominant singlet discharges. Doublets were more common in the S cell type.5. With sustained activation, the mean delay from the onset of current to the first spike was 2-6 + 1 1 s for F cells, and 3-2 + 1-9 s for S cells. The time required to reach peak frequency of singlet discharge following repetitive firing onset was significantly shorter for F than S cells (7-0 + 5 0 vs. 14-3 + 13-6 s) and the peak singlet frequencies also differed significantly (F, 28-0 + 7-7 Hz vs. S, 15-6 + 2-5 Hz). Subsequently, the mean magnitude of firing rate reduction from the peak to 24 s later was significantly greater for F cells than that for S cells (16-2 + 6 Hz vs. 5X8 + 3 Hz). These gradual reductions in firing frequency for both F and S cells during the course of their sustained stimulation were qualitatively similar to the late adaptation observed in previous studies that had employed intracellular stimulation.6. The time course of firing frequency for each unit with sustained activation was fitted with a double-exponential equation: the first time constant (T1) for the initial increase in frequency was relatively short (F, 2X5 + 2-1 s vs. S, 3-7 + 4-1 s). The second time constant (r2) was significantly shorter for F than S cells (130-7 + 98-4 s vs. 750 0 + 402-4 s). It is argued that the r2 values provided a quantitative description of the type of adaptation termed 'late' in previous studies.7. The responses to intermittent stimulation were qualitatively similar to those seen with sustained activat...

Voluntary Motor Output Is Altered by Spike-Timing-Dependent Changes in the Human Corticospinal Pathway

“…Although the excitability of motoneurons can be altered through repetitive activation (Spielmann et al, 1993;Gandevia et al, 1999) or through ongoing changes in afferent input (Martin et al, 2008), neither of these mechanisms is likely to produce the differential effects observed here, as both afferents and motoneurons experienced the same total extra activity in each conditioning protocol. Furthermore, this extra activity was very little compared with normal motoneuron firing in voluntary contractions (Ͼ15 Hz) (Bellemare et al, 1983).…”

Fatigue-Sensitive Afferents Inhibit Extensor but Not Flexor Motoneurons in Humans

“…Intrinsic motoneuronal properties also change with fatigue. In animals, when motoneurons are repetitively stimulated by sustained intracellular currents, many cells either reduce their discharge or stop firing (Kernell and Monster, 1982a,b;Spielmann et al, 1993;Sawczuk et al, 1997). Similarly, in humans, the synaptic drive necessary to maintain repetitive firing of single motor units increases during weak contractions (Johnson et al, 2004).…”

Beginning at the end: Repetitive firing properties in the final common pathway

“…The second phase is termed late SFA. It follows early SFA, and it occurs over many tens of seconds or even minutes (Kernell and Monster, 1982b;Spielmann et al, 1993). Some studies discuss three phases of SFA, with the addition of an "immediate" phase occurring over the first few spikes of a repetitive train (Sawczuk et al, 1995).…”

“…It is possible, however, that the high variance in interspike interval could occlude an underlying early SFA process. Given that late SFA is seen even with intermittent stimulation (Spielmann et al, 1993), then if it is present during locomotion, one should record an overall slowing of the firing rate over tens of seconds to minutes. We have presented evidence demonstrating late SFA during a period of time following brainstem stimulation but prior to establishment of locomotor activity (Krawitz et al, 1996).…”