Tongue-muscle-controlling motoneurons in the Japanese toad: topography, morphology and neuronal pathways from the ?snapping-evoking area? in the optic tectum

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Abstract
Summary 1. As a step to clarifying the neural bases for the visually-guided prey-catching behavior in the toad, special attention was paid to the flipping movement of the tongue. Tongue-musclecontrolling motoneurons were identified antidromically, and their topographical distribution within the hypoglossal nucleus, the morphology, and the neuronal pathways from the optic tectum including the ‘snapping-evoking area’ (see below) to these motoneurons were investigated in paralyzed Japanese toads using intracellular recording techniques. 2. The morphology of motoneurons innervating the tongue-protracting or retracting muscles (PMNs or RMNs respectively) was examined by means of intracellular-staining (using HRP/cobaltic lysine) and retrograde-labeling (using cobaltic lysine) methods. Both PMNs and RMNs showed an extensive spread of the branching trees of dendrites; 4 dendritic fields were distinguished: (1) lateral/ventrolateral, (2) dorsal/dorsolateral, (3) medial, and (4) in some motoneurons, contralateral dendritic fields, although there was a tendency for the dorsal/dorsolateral dendritic field to be less extensive in the PMNs than in the RMNs. The axons of both PMNs and RMNs arose from thick dendrites, ran in a ventral direction without any axon-collaterals branching off, and then entered the hypoglossal nerve. 3. The PMNs and RMNs were distributed topographically within the hypoglossal nucleus; the RMNs were located rostrally within the nucleus, whereas the PMNs were located more caudally within it. 4. In about 3/4 of the RMNs tested, depolarizing potentials [presumably the excitatory postsynaptic potentials (EPSPs)], on which action potentials were often superimposed, were evoked by electrical stimuli applied to the nerve branch innervating the tongue protractor. These EPSPs were temporally facilitated when the electrical stimuli were applied at short intervals (10 ms). 5. Both PMNs and RMNs showed hyperpolarizing potentials (IPSPs) in response to single electrical stimuli of various intensities (10–200 μA) applied to the ‘snapping-evoking area’ (lateral/ventrolateral part of the optic tectum) on either side. These IPSPs were facilitated after repetitive electrical stimulations at short intervals (10 ms) and of weaker intensities (down to 10 μA); i.e., a temporal facilitation of the IPSPs was observed. On the other hand, large and long-lasting EPSPs which prevailed over the underlying IPSPs were evoked after repetitive electrical stimulations (a few pulses or more) at short intervals (10 ms) and of stronger intensities (generally 90 μA or more); thus, a temporal facilitation of the EPSPs was also observed. Basically similar results were obtained when other regions of the optic tectum (e.g., the rostral, medial, and dorsal parts) were stimulated, although the most effective sites for eliciting these postsynaptic potentials (PSPs) were at the ventrolateral part of the optic tectum. In many of the PMNs and RMNs tested, these PSPs were further spatially facilitated; i.e., the PSPs were facilitated when electrical stimuli were applied simultaneously to 2 different sites in the unilateral or bilateral optic tecta. 6. From these results, it was concluded that: (1) there are 2 separate neuronal pathways, i.e., the polysynaptic excitatory and inhibitory pathways from the optic tectum to the tongue-muscle-controlling motoneurons and (2) the threshold for activating the excitatory pathways is higher than that of the inhibitory ones. It was suggested that the descending tectal efferents converge on the interneurons and that the temporal and spatial facilitation of spike discharges occurs within them. 7. These results were discussed with regard to the control of prey-catching behavior; it was suggested that: (1) these polysynaptic pathways (especially the excitatory ones) from the optic tectum to the tongue-muscle-controlling motoneurons are closely related to the generation of the lingual-flip motor-pattern during the prey-catching behavior and that (2) the temporal and spatial integration of synaptic inputs in the premotor interneurons plays a critical role in the initiation of prey-catching.