Reciprocal Ia inhibition contributes to motoneuronal hyperpolarisation during the inactive phase of locomotion and scratching in the cat

• Published in: The Journal of physiology Vol. 589; no. 1; pp. 119 - 134
• Main Authors: Geertsen, Svend S., Stecina, Katinka, Meehan, Claire F., Nielsen, Jens B., Hultborn, Hans
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01.01.2011; Wiley Subscription Services, Inc; Blackwell Science Inc
• Subjects: Animals; Cats; Decerebrate State; Electric Stimulation; Evoked Potentials, Motor; Female; Inhibitory Postsynaptic Potentials; Interneurons - drug effects; Interneurons - physiology; Levodopa - administration & dosage; Locomotion; Male; Membrane Potentials; Motor Neurons - drug effects; Motor Neurons - physiology; Motor Skills; Muscle Contraction; Muscle Relaxation; Muscle, Skeletal - innervation; Neural Inhibition - drug effects; Neuroscience; Patch-Clamp Techniques; Periodicity; Time Factors
• ISSN: 0022-3751; 1469-7793
• DOI: 10.1113/jphysiol.2010.199125

Non‐technical summary During a movement, the contraction of a given muscle group is often coordinated with the simultaneous relaxation of its antagonist muscles. The neural basis of this antagonist relaxation has been investigated in both animal and human experiments for decades and it is believed that activation of the Ia inhibitory interneurones by central motor programmes plays a major role in this relaxation of antagonist muscles. The alternating movements during locomotion would seem to especially require reciprocal actions, but recent studies have raised significant questions about the role of this inhibition. We found that inhibition evoked by these inhibitory interneurones is largest when their target motoneurones are inactive – even in the absence of supraspinal influence. The results of this work provide new evidence for the role of the Ia inhibitory interneurones during rhythmic motor activity. This supports the classical view of reciprocal inhibition as a basis for antagonist relaxation. Despite decades of research, the classical idea that ‘reciprocal inhibition’ is involved in the hyperpolarisation of motoneurones in their inactive phase during rhythmic activity is still under debate. Here, we investigated the contribution of reciprocal Ia inhibition to the hyperpolarisation of motoneurones during fictive locomotion (evoked either by electrical stimulation of the brainstem or by l‐DOPA administration following a spinal transection at the cervical level) and fictive scratching (evoked by stimulation of the pinna) in decerebrate cats. Simultaneous extracellular recordings of Ia inhibitory interneurones and intracellular recordings of lumbar motoneurones revealed the interneurones to be most active when their target motoneurones were hyperpolarised (i.e. in the inactive phase of the target motoneurones). To date, these results are the most direct evidence that Ia inhibitory interneurones contribute to the hyperpolarisation of motoneurones during rhythmic behaviours. We also estimated the amount of Ia inhibition as the amplitude of Ia IPSC in voltage‐clamp mode. In both flexor and extensor motoneurones, Ia IPSCs were always larger in the inactive phase than in the active phase during locomotion (n= 14) and during scratch (n= 11). Results obtained from spinalised animals demonstrate that the spinal rhythm‐generating network simultaneously drives the motoneurones of one muscle group and the Ia interneurones projecting to motoneurones of the antagonist muscles in parallel. Our results thus support the classical view of reciprocal inhibition as a basis for relaxation of antagonist muscles during flexion–extension movements. During a movement, the contraction of a given muscle group is often coordinated with the simultaneous relaxation of its antagonist muscles. The neural basis of this antagonist relaxation has been investigated in both animal and human experiments for decades and it is believed that activation of the Ia inhibitory interneurones by central motor programmes plays a major role in this relaxation of antagonist muscles. The alternating movements during locomotion would seem to especially require reciprocal actions, but recent studies have raised significant questions about the role of this inhibition. We found that inhibition evoked by these inhibitory interneurones is largest when their target motoneurones are inactive – even in the absence of supraspinal influence. The results of this work provide new evidence for the role of the Ia inhibitory interneurones during rhythmic motor activity. This supports the classical view of reciprocal inhibition as a basis for antagonist relaxation.