Neuronal pathways for the lingual reflex in the Japanese toad

Summary

• 1. Anuran tongue is controlled by visual stimuli for releasing the prey-catching behavior (‘snapping’) and also by the intra-oral stimuli for eliciting the lingual reflex. To elucidate the neural mechanisms controlling tongue movements, we analyzed the neuronal pathways from the glossopharyngeal (IX) afferents to the hypoglossal (XII) tongue-muscle motoneurons.

• 2. Field potentials were recorded from the bulbar dorsal surface over the fasciculus solitarius (fsol) to the electrical stimulation of the ipsilateral IX nerve. They were composed of three successive negative waves: S1, S2 and N wave. The S1 and S2 waves followed successive stimuli applied at short intervals (10 ms or less), whereas the N wave was strongly suppressed at intervals shorter than 500 ms. Furthermore, the S1 wave had lower threshold than the S2 wave.

• 3. Orthodromic action potentials were intra-axonally recorded from IX afferent fibers in the fsol to the ipsilateral IX nerve stimuli. Two peaks found in the latency distribution histogram of these action potentials well coincided with the negative peaks of the S1 and the S2 waves of the simultaneously recorded field potentials. Therefore, the S1 and S2 waves should represent the compound action potentials of two groups of the IX afferent fibers with different conduction velocities.

• 4. Ipsilateral IX nerve stimuli elicited excitatory postsynaptic potentials (EPSPs) in the tongue-protractor motoneurons (PMNs) and the tongue-re-tractor motoneurons (RMNs). Inhibitory postsynaptic potentials were not observed.

• 5. The EPSPs recorded in PMNs had mean onset latencies of 6.4 ms measured from the negative peaks of the S1 wave. The EPSPs were facilitated when paired submaximal stimuli were applied at intervals shorter than 20 ms, but were suppressed at intervals longer than 30 ms. Furthermore, the EPSPs were spatially facilitated when peripherally split two bundles of the IX nerve were simultaneously stimulated.

• 6. On the other hand, the EPSPs recorded in RMNs had shorter onset latencies, averaging 2.5 ms. In 14 of 43 RMNs, early and late EPSP components could be reliably discriminated. The thresholds for the early EPSP components were as low as those for the S1 waves, whereas for the late EPSP components the thresholds were usually higher than those for the S2 waves. The early EPSP components had mean onset latencies of 2.3 ms and followed each of the successive stimuli applied at short intervals with constant latencies and amplitudes. On the other hand, the late EPSP components appeared at 5.3 ms after the onset of the early EPSP components, and were temporally facilitated by successive stimuli at 10 ms intervals.

• 7. Double-labeling experiments (horseradish peroxidase and cobaltic-lysine) revealed that some of the IX afferent terminals with beaded bouton-like structures had direct contacts with the dorsal and lateral dendrites and the somata of the XII motoneurons, but not with their medial dendrites. These direct contacts only occurred in the rostral region of the dorsomedial XII nucleus, where RMNs are reported to predominate.

• 8. Contralateral IX nerve stimuli also elicited EPSPs in both PMNs and RMNs. Latencies measured from the onset of stimuli averaged 10.6 ms and 10.8 ms for PMNs and RMNs, respectively. These EPSPs were smaller than those evoked by the ipsilateral IX nerve stimuli, and were often facilitated by successive stimuli at 10 ms intervals.

• 9. It appears that the ipsilateral IX nerve afferents connect to PMNs polysynaptically, while they connect to RMNs by two kinds of excitatory pathways: short-latency monosynaptic pathways and longer-latency polysynaptic pathways. Furthermore, it appeared that the contralateral IX nerve afferents connect to both of PMNs and RMNs via polysynaptic excitatory pathways.

• 10. We also demonstrated a spatial facilitation between the polysynaptic EPSPs evoked by the IX nerve stimuli and those by the stimulations of the ‘snapping’-evoking area in the optic tetum (OT). These results suggest that some common excitatory interneurons, on which the tectal descending volleys and the IX nerve afferent volleys converge, mediate polysynaptic activation of the tonguemuscle motoneurons.