Neurochemical plasticity of peripherally axotomized mesencephalic trigeminal neurons of the rat

Abstract

The mesencephalic trigeminal nucleus (Me5) is a unique collection of primary afferent neurons located in the brain. Though functionally homogeneous Me5 neurons are chemically heterogeneous and utilize various neurochemicals for synaptic transmission, including classical transmitters, gaseous neuromessengers and calcium-binding proteins. Previous studies have shown that the neuronal content of these transmitter substances is not static and may vary in case of changes in the environmental conditions such as peripheral nerve damage. We set it as a task to follow up the altered neurochemical phenotype of the damaged neurons after peripheral nerve axotomy. Adult Wistar rats of both sexes underwent unilateral transection of the masseteric nerve and the induced neurochemical changes in axotomized Me5 neurons were examined by NADPH-diaphorase histochemistry and immunohistochemistry for glutamate, some neuropeptides and neuronal calcium-binding proteins. The contralateral side served as a control. Following a survival period of 7 days, the mesencephalic trigeminal neurons on the axotomized side displayed a lower immunoreactivity to glutamate, calbindin and parvalbumin compared to the neurons contralaterally. At this time, the number of NADPH-diaphorase-stained neurons was slightly higher than those of the intact Me5 neurons. Moreover, the Me5 neuronal population along the entire extent of the nucleus started expressing neuropeptide Y, galanin and vasoactive intestinal peptide. This tendency persisted until the 28th postoperative day and slowly decreased in the days to follow. 56 days after the axotomy, the number of immunoreactive Me5 neurons was similar to the one found 7 days after intervention. Our results show that axotomy induces down-regulation of glutamate and calcium-binding proteins in Me5, up-regulation of nitric oxide and de novo synthesis of certain neuropeptides. It can be inferred that the described phenomena serve as adaptive mechanisms and trophic factors for survived Me5 neurons, thus implying their previously unsuspected neurochemical plasticity.