Changes in the excitability of hindlimb motoneurons during muscular atonia induced by stimulating the pedunculopontine tegmental nucleus in cats

Abstract

We have previously reported that electrical stimulation delivered to the ventral part of the pedunculopontine tegmental nucleus (PPN) produced postural atonia in acutely decerebrated cats [Neuroscience 119 (2003) 293]. The present study was designed to elucidate synaptic mechanisms acting on motoneurons during postural atonia induced by PPN stimulation. Intracellular recording was performed from 72 hindlimb motoneurons innervating extensor and flexor muscles, and the changes in excitability of the motoneurons following the PPN stimulation were examined. Repetitive electrical stimulation (20-50 microA, 50 Hz, 5-10 s) of the PPN hyperpolarized the membrane potentials of both the extensor and flexor motoneurons by 2.0-12 mV (6.0 +/- 2.3 mV, n = 72). The membrane hyperpolarization persisted for 10-20 s even after termination of the stimulation. During the PPN stimulation, the membrane hyperpolarization was associated with decreases in the firing capability (n = 28) and input resistance (28.5 +/- 6.7%, n = 14) of the motoneurons. Moreover the amplitude of Ia excitatory postsynaptic potentials was also reduced (44.1 +/- 13.4%, n = 14). After the PPN stimulation, these parameters immediately returned despite that the membrane hyperpolarization persisted. Iontophoretic injections of chloride ions into the motoneurons reversed the polarity of the membrane hyperpolarization during the PPN stimulation. The polarity of the outlasting hyperpolarization however was not reversed. These findings suggest that a postsynaptic inhibitory mechanism, which was mediated by chloride ions, was acting on hindlimb motoneurons during PPN-induced postural atonia. However the outlasting motoneuron hyperpolarization was not due to the postsynaptic inhibition but it could be due to a decrease in the activity of descending excitatory systems. The functional role of the PPN in the regulation of postural muscle tone is discussed with respect to the control of behavioral states of animals.