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

• Published in: The Journal of physiology 2015-05, Vol.593 (10), p.2327-2342
• Main Authors: MacDonell, C. W., Power, K. E., Chopek, J. W., Gardiner, K. R., Gardiner, P. F.
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Adaptation, Physiological - physiology; Animals; Cats; Decerebrate State - physiopathology; Electric Stimulation; Female; Hindlimb - innervation; Locomotion - physiology; Models, Animal; Motor Neurons - physiology; Neuroscience: Cellular/Molecular; Rats; Rats, Sprague-Dawley - physiology
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/JP270239

Key points This is the first report, in adult decerebrate rats, to examine intracellular hindlimb motoneurone properties during quiescence, fictive locomotion and a tonic period immediately before fictive locomotion that is characterized by increased peripheral nerve activity. It is shown for the first time during fictive locomotion that motoneurones become more responsive in the tonic period, suggesting that the motoneurone pool becomes primed before patterned motor output commences. Spike frequency adaptation exists in quiescence and during fictive locomotion during constant excitation with injected current but not during centrally driven fictive locomotion. Motoneurones within the extensor motor pool show changes in excitability even when they are not directly involved in locomotion. The data show increased responsiveness of motoneurones during locomotion via a lowered threshold for spike initiation and decreased rheobase. 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