Neural circuits underlying jaw movements for the prey-catching behavior in frog: distribution of vestibular afferent terminals on motoneurons supplying the jaw
- 108 Downloads
Coordinated movement of the jaw is essential for catching and swallowing the prey. The majority of the jaw muscles in frogs are supplied by the trigeminal motoneurons. We have previously described that the primary vestibular afferent fibers, conveying information about the movements of the head, established close appositions on the motoneurons of trigeminal nerve providing one of the morphological substrates of monosynaptic sensory modulation of prey-catching behavior in the frog. The aim of our study was to reveal the spatial distribution of vestibular close appositions on the somatodendritic compartments of the functionally different trigeminal motoneurons. In common water frogs, the vestibular and trigeminal nerves were simultaneously labeled with different fluorescent dyes and the possible direct contacts between vestibular afferents and trigeminal motoneurons were identified with the help of DSD2 attached to an Andor Zyla camera. In the rhombencephalon, an overlapping area was detected between the incoming vestibular afferents and trigeminal motoneurons along the whole extent of the trigeminal motor nucleus. The vestibular axon collaterals formed large numbers of close appositions with dorsomedial and ventrolateral dendrites of trigeminal motoneurons. The majority of direct contacts were located on proximal dendritic segments closer than 300 µm to the somata. The identified contacts were evenly distributed on rostral motoneurons innervating jaw-closing muscles and motoneurons supplying jaw-opening muscles and located in the caudal part of trigeminal nucleus. We suggest that the identified contacts between vestibular axon terminals and trigeminal motoneurons may constitute one of the morphological substrates of a very quick response detected in trigeminal motoneurons during head movements.
KeywordsBrainstem Trigeminal nerve Vestibular terminals Motor coordination Neuronal labeling
The authors thank Ms Timea Horvath for skillful technical assistance.
Compliance with ethical standards
The manuscript does not contain clinical studies or patient data.
Conflict of interest
The authors declare no conflict of interest.
This research was supported by financial aid from the Hungarian Academy of Sciences (MTA-TKI 11,008) and from the Hungarian National Research Found (OTKA K115471).
- Birinyi A, Kecskes S, Kovalecz G, Matesz C (2016) Termination of vestibular afferent fibers on the trigeminal motoneurons: possible network mediating jaw movements during prey-catching behavior of the frog. In: Abstract Book of 8th European Conference on Comparative Neurobiology Munich Germany, P2–02Google Scholar
- Corson AJ, Erisir A (2013) Monosynaptic convergence of chorda tympani and glossopharyngeal afferents onto ascending relay neurons in the nucleus of the solitary tract: a high-resolution confocal and correlative electron microscopy approach. J Comp Neurol 521:2907–2926CrossRefPubMedPubMedCentralGoogle Scholar
- Dicke U, Roth G (1993) Tectosipnal pathways in plethodontoid salamanders and their connections to motor nuclei involved in prey capture. In: Elsner N, Heisenberg M (eds) Gene brain behaviour. M. Georg Thieme, Stuttgart, pp 1–92Google Scholar
- Ewert JP, Buxbaum-Conradi H, Dreisvogt M, Glagow C, Merkel-Harff C, Röttgen A, Schürg-Pfeiffer E, Schwippert WW (2001) Neural modulation of visuomotor functions underlying prey-catching behaviour in anurans: perception, attention, motor performance, learning. Comp Bichem Physiol Part A 128:417–461CrossRefGoogle Scholar
- Gaupp E (1904) Ecker’s und R. Wiedersheim’s Anatomie des Frosches. vol 3. Vieweg und Sohn, BraunschweigGoogle Scholar
- Kuruvilla A, Sitko S, Schwartz IR, Honrubia V (1985) Central projections of primary vestibular fibers in the bullfrog: I. The vestibular nuclei. Laryngoscope 5:692–707Google Scholar
- Nishikawa KC, Gans C (1992) The role of hypoglossal sensory feedback during feeding in the marine toad, Bufo marinus. J Exp Biol 264:2511–2529Google Scholar
- Olsson K, Westberg KG (1991) Integration in trigeminal premotor interneurones in the cat. 2. Functional characteristics of neurones in the subnucleus of the oral nucleus of the spinal trigeminal tract with a projection to the digastric motoneurone subnucleus. Exp Brain Res 84:115–124CrossRefPubMedGoogle Scholar
- Sotello C (1976) Morphology of cerebellar cortex. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin, pp 865–891Google Scholar
- Tolu E, Caria MA, Chessa G, Melis F, Simula ME, Podda MV, Solinas A, Deriu F (1996) Trigeminal motoneuron responses to vestibular stimulation in Guinea pig. Arch Ital Biol 134:140–51Google Scholar
- Walkowiak W (2007) Call production and neural basis of vocalization. In: Narins PM, Feng AS, Richard RF, Popper AN (eds) Hearing and sound communication in Amphibians. Springer, Berlin, pp 87–112Google Scholar
- Westberg KG, Sandström G, Olsson K (1995) Integration in trigeminal premotor interneurones in the cat. 3. Input characteristics and synaptic actions of neurones in subnucleus of the oral nucleus of the spinal trigeminal tract with a projection to the masseteric motoneuron subnucleus. Exp Brain Res 104:449–461CrossRefPubMedGoogle Scholar
- Wouterlood FG, van Haeften T, Blijleven N, Perez-Templado P, Perez-Templado H (2002) Double-label confocal laser-scanning microscopy, image restoration, and real-time three-dimensional reconstruction to study axons in the central nervous system and their contacts with target neurons. Appl Immunohistochem Mol Morphol 10:85–95PubMedGoogle Scholar
- Wouterlood FG, Bockers T, Witter MP (2003) Synaptic contacts between identified neurons visualized in the confocal laser scanning microscope. Neuroanatomical tracing combined with immunofluorescence detection of post-synaptic density proteins and target neuron-markers. J Neurosci Methods 128:129–142CrossRefPubMedGoogle Scholar