A physiological study of brainstem and peripheral inputs to trigeminal motoneurons in lampreys

Abstract

The inputs to trigeminal motoneurons from sensory afferents and rhombencephalic premotor regions were studied in isolated brainstem preparations of adult lampreys ( Petromyzon marinus). Stimulation of both trigeminal nerves, contralateral nucleus motorius nervi trigemini, nucleus sensibilis nervi trigemini and ipsilateral rostral reticular formation elicited large-amplitude excitatory postsynaptic potentials with short latencies. These were significantly attenuated by adding 6-cyano-7-nitroquinoxaline-2,3-dione (10 μM) and 2-amino-5-phosphonopentanoate (200 μM) to the bath, suggesting participation of both α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate and N-methyl- d-aspartate receptors. The inputs from ipsilateral trigeminal afferents included a di- or oligosynaptic glycinergic inhibition. Sustained rhythmical membrane potential oscillations were observed in 52% of the recorded cells upon stimulation of trigeminal afferents or the contralateral nucleus sensibilis nervi trigemini. Two types of rhythm were obtained: (i) low-frequency oscillations (0.1–0.5 Hz), with peak-to-peak amplitudes between 8.5 and 17 mV; and (ii) higher frequency oscillations (1.0–2.8 Hz) with smaller amplitudes (1.8–5.1 mV). The two types of trigeminal rhythm could occur independently of fictive locomotion and fictive breathing. In a decerebrate semi-intact preparation, slow rhythmical trigeminal motoneuron potential oscillations were also evoked by stimulation of the oral disc. This study shows that trigeminal motoneurons receive excitatory synaptic inputs from several brainstem sites, and that membrane potential oscillations can be triggered upon stimulation of trigeminal afferents or the nucleus sensibilis nervi trigemini. We suggest that these oscillations recorded in vitro may represent the centrally generated components that underlie rhythmical feeding in lampreys.