Extensor motoneurone properties are altered immediately before and during fictive locomotion in the adult decerebrate rat

Abstract

This study examined motoneurone properties during fictive locomotion in the adult rat for the first time. Fictive locomotion was induced via electrical stimulation of the mesencephalic locomotor region in decerebrate adult rats under neuromuscular blockade to compare basic and rhythmic motoneurone properties in antidromically identified extensor motoneurones during: (1) quiescence, before and after fictive locomotion; (2) the 'tonic' period immediately preceding locomotor-like activity, whereby the amplitude of peripheral flexor (peroneal) and extensor (tibial) nerves are increased but alternation has not yet occurred; and (3) locomotor-like episodes. Locomotion was identified by alternating flexor-extensor nerve activity, where the motoneurone either produced membrane oscillations consistent with a locomotor drive potential (LDP) or did not display membrane oscillation during alternating nerve activity. Cells producing LDPs were referred to as such, while those that did not were referred to as 'idle' motoneurones. LDP and idle motoneurones during locomotion had hyperpolarized spike threshold (Vth ; LDP: 3.8 mV; idle: 5.8 mV), decreased rheobase and an increased discharge rate (LDP: 64%; idle: 41%) during triangular ramp current injection even though the frequency-current slope was reduced by 70% and 55%, respectively. Modulation began in the tonic period immediately preceding locomotion, with a hyperpolarized Vth and reduced rheobase. Spike frequency adaptation did not occur in spiking LDPs or firing generated from sinusoidal current injection, but occurred during a sustained current pulse during locomotion. Input conductance showed no change. Results suggest motoneurone modulation occurs across the pool and is not restricted to motoneurones engaged in locomotion.

Figure 1

Rhythmic discharge during ramp current injection Ramp current injection (Ac, Bc) with resulting intracellular motoneurone recording (membrane potential, E_m; Ab, Bb), and alternating flexor/extensor peripheral nerves (Aa, Ba) for an idle (A) and LDP (B) motoneurone. A, recordings from before locomotion, just before the tonic period, and during locomotion for an idle cell. The arrows indicate the rheobase for each ramp from left to right: before, 14.6 nA; tonic, 11.4 nA; locomotion, 8.7 nA. B, recordings from the tonic period, LDP generation during locomotion, and the period following locomotion (two additional ramps are not illustrated) for an LDP cell. The arrows represent the rheobase for the ramps left to right: tonic, 18.5 nA; locomotion, 6.7 nA; and after 14 nA. Note that the current amplitude and ramp duration (Ac, Bc) remain equal for the entire epoch. In B, after an initial response to excitation following locomotion, the motoneurone fails to fire 20 s after locomotion ceased but was able to respond to other measurements of motoneurone properties (IC and rheobase, for example). Ca and b, the after-hyperpolarization period of spikes generated from the motoneurone illustrated in B, in quiescence before locomotion (not shown in B) and during fictive locomotion (spike truncated for illustration purposes). Note the difference in the relative size (denoted by the dashed lines in Ca and b) and the hyperpolarized membrane potential at spike initiation during locomotion compared to before locomotion.

Figure 2

Ramp current injection during the tonic period Motoneurone discharge (B) in response to ramp current injection (C) before locomotion (left) and during the tonic period (right). Note that discharge during the tonic period starts at a lower rheobase. The top panel illustrates the rising ENG amplitude (A) during the lead up to locomotion. The neurograms in the top panel are time locked to the ramps in panels B and C. The ramp before locomotion and that shown during the tonic period are separated by 20 s.

Figure 3

Motoneurone input conductance Mean and individual input conductance for locomotor drive potential-generating (A) and idle (B) motoneurones. Error bars represent standard deviation. No difference in mean input conductance existed.

Figure 4

Motoneurone frequency–current relationship slope Representative data are illustrated from an LDP (A) and an idle motoneurone (B). The slopes of the frequency–current relationships are shown during Quiescence, before fictive locomotion (continuous line); Quiescence, after fictive locomotion (dashed line); and Fictive Locomotion (dotted line) for an LDP cell. For Idle motoneurones (B), the example also includes the slope of the Tonic period (dash-dot-dash line). Tables1 and 2 show the mean ± SD for the different groups.

Figure 5

No evidence of spike frequency adaptation in LDPs or discharge from sinusoidal current injection The mean and coefficient of variation of motoneurone discharge (A) from MLR-driven locomotor drive potentials (B) are relatively consistent across the 20 s locomotor bout. The mean and coefficient of variation of motoneurone discharge (C) resulting from intracellular sinusoidal current injection (D) are also relatively consistent. Neither the LDP nor idle motoneurones show spike frequency adaptation.