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Keywords:

  • classical conditioning;
  • facial;
  • motor learning;
  • neural plasticity;
  • reinnervation

Abstract

The ability of four different brainstem motoneuron pools to perform a newly acquired motor task was studied in alert cats. A classical conditioning of eyelid responses was carried out in (i) unoperated animals, and in animals with (ii) transection, 180° rotation, and re-suture of the zygomatic facial nerve branch, (iii) a crossed anastomosis of the buccal to the zygomatic facial nerve branch and (iv) a hypoglossal–facial nerve anastomosis. Animals were conditioned with a delay paradigm using a tone (350 ms, 600 Hz, 90 dB) as conditioned stimulus, followed 250 ms later by an air puff (100 ms, 3 kg/cm2) as unconditioned stimulus. Animals with zygomatic nerve rotation performed conditioned responses (CRs) at control rate, with significantly larger amplitude, area and velocity, but a de-synchronized oscillatory pattern. Animals with buccal–zygomatic anastomosis acquired CRs at control rate, but these CRs had significantly smaller amplitude than those of controls and a de-synchronized pattern. Animals with a hypoglossal–facial anastomosis were unable to perform CRs. The trigeminal hyper-reflexia triggered by the axotomy was probably the origin of the large CRs after zygomatic nerve rotation. Trigeminal hyper-reflexia could also contribute to generation of the small CRs recorded after buccal–zygomatic anastomosis. Although trigeminal hyper-reflexia was also present following hypoglossal–facial anastomosis, hypoglossal motoneurons did not reach their firing threshold to perform CRs. In accordance with the embryonic origin of involved motoneurons, animals with buccal–zygomatic and hypoglossal–facial anastomoses moved the ipsilateral eyelid synchronously to mouth-related activities. It is suggested that there is a gradient of adaptability in motoneuron pools forced to perform new motor tasks through foreign muscles, which depends on their embryological origins and functional properties.