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Neural circuits underlying tongue movements for the prey-catching behavior in frog: distribution of primary afferent terminals on motoneurons supplying the tongue

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Abstract

The hypoglossal motor nucleus is one of the efferent components of the neural network underlying the tongue prehension behavior of Ranid frogs. Although the appropriate pattern of the motor activity is determined by motor pattern generators, sensory inputs can modify the ongoing motor execution. Combination of fluorescent tracers were applied to investigate whether there are direct contacts between the afferent fibers of the trigeminal, facial, vestibular, glossopharyngeal-vagal, hypoglossal, second cervical spinal nerves and the hypoglossal motoneurons. Using confocal laser scanning microscope, we detected different number of close contacts from various sensory fibers, which were distributed unequally between the motoneurons innervating the protractor, retractor and inner muscles of the tongue. Based on the highest number of contacts and their closest location to the perikaryon, the glossopharyngeal–vagal nerves can exert the strongest effect on hypoglossal motoneurons and in agreement with earlier physiological results, they influence the protraction of the tongue. The second largest number of close appositions was provided by the hypoglossal and second cervical spinal afferents and they were located mostly on the proximal and middle parts of the dendrites of retractor motoneurons. Due to their small number and distal location, the trigeminal and vestibular terminals seem to have minor effects on direct activation of the hypoglossal motoneurons. We concluded that direct contacts between primary afferent terminals and hypoglossal motoneurons provide one of the possible morphological substrates of very quick feedback and feedforward modulation of the motor program during various stages of prey-catching behavior.

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Abbreviations

C2:

Dorsal root of second cervical spinal nerve

DM:

Dorsomedial subnucleus of hypoglossal nerve

FDA:

Fluorescein dextran amine

GEN:

Geniohyoid muscle

GGL:

Genioglossus muscle

HYO:

Hyoglossus muscle

IM:

Intermediate subnucleus of hypoglossal nerve

IX–X:

Glossopharyngeal–vagal nerves

LOPI:

Last-order premotor interneurons

mesV:

Mesencephalic tract of trigeminal nerve

OMO:

Omohyoid muscle

PB:

Phosphate buffer

RDA:

Tetramethyl-rhodamine dextran amine

ST:

Solitary tract

STE:

Sternohyoid muscle

TP:

Tongue prehension behavior

tspV:

Spinal tract of trigeminal nerve

V:

Trigeminal nerve

VII:

Facial nerve

VIII:

Vestibular nerve

VL:

Ventrolateral subnucleus of hypoglossal nerve

XII:

Hypoglossal nerve

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Acknowledgments

The authors thank Ms Timea Horvath for skillful technical assistance. This research was supported by the European Union and the State of Hungary, co-financed by the European Social Fund in the framework of TÁMOP-4.2.4. A/2-11/1-2012-0001 ‘National Excellence Program’; and MTA-TKI 11008.

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Kecskes, S., Matesz, C., Gaál, B. et al. Neural circuits underlying tongue movements for the prey-catching behavior in frog: distribution of primary afferent terminals on motoneurons supplying the tongue. Brain Struct Funct 221, 1533–1553 (2016). https://doi.org/10.1007/s00429-014-0988-1

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