Advertisement

Journal of Comparative Physiology A

, Volume 157, Issue 6, pp 717–737 | Cite as

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

  • Masahiko Satou
  • Toshiya Matsushima
  • Hiroaki Takeuchi
  • Kazuo Ueda
Article

Summary

  1. 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. 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. 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. 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. 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. 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. 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.

     

Keywords

Electrical Stimulus Optic Tectum Hypoglossal Nerve Neuronal Pathway Hypoglossal Nucleus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

PMN

tongue-protractor motoneuron

RMN

tongue-retractor motoneuron

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Black D (1917) The motor nuclei of the cerebral nerves in phylogeny. A study of the phenomena of neurobiotaxis. II. Amphibia. J Comp Neurol 28:379–427Google Scholar
  2. Camhi JM (1984) Neuroethology. Nerve cells and the natural behavior of animals. Sinauer, SunderlandGoogle Scholar
  3. Collins III WF (1983) Organization of electrical coupling between frog lumbar motoneurons. J Neurophysiol 49:730–744Google Scholar
  4. Comer C, Grobstein P (1981) Involvement of midbrain structures in tactually and visually elicited prey acquisition behavior in the frogRana pipiens. J Comp Physiol 142:151–160Google Scholar
  5. Dean J (1980) Encounters between bombardier beetles and two species of toads (Bufo americanus, B. marinus): Speed of prey-capture does not determine success. J Comp Physiol 135:41–50Google Scholar
  6. Eccles JC (1964) The physiology of synapse. Springer, Berlin Heidelberg New YorkGoogle Scholar
  7. Erulkar SD, Soller RW (1980) Interactions among lumbar motoneurons on opposite sides of the frog spinal cord: Morphological and electrophysiological studies. J Comp Neurol 192:473–488Google Scholar
  8. Ewert J-P (1967) Aktivierung der Verhaltensfolge beim Beutefang der Erdkröte (Bufo bufo L.) durch elektrische Mittelhirnreizung. Z Vergl Physiol 54:455–481Google Scholar
  9. Ewert J-P (1976) The visual system of the toad: Behavioral and physiological studies on a pattern recognition system. In: Fite KV (ed) The amphibian visual system. Academic Press, New York San Francisco London, pp 141–202Google Scholar
  10. Ewert J-P (1980) Neuroethology. An introduction to the neurophysiological fundamentals of behavior. Springer, Berlin Heidelberg New YorkGoogle Scholar
  11. Ewert J-P (1984) Tectal functions underlying prey-catching and predator avoidance behaviors in toads. In: Vanegas H (ed) Neurology of the optic tectum. Plenum Press, New York, pp 247–416Google Scholar
  12. Ewert J-P, Burghagen H, Schürg-Pfeiffer E (1983) Neuroethological analysis of the innate releasing mechanism for preycatching behavior in toads. In: Ewert J-P, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, London New York, pp 413–475Google Scholar
  13. Gallyas F (1979) Light insensitive physical developers. Stain Technol 54:173–176Google Scholar
  14. Gans C, Gorniak GC (1982a) How does the toad flip its tongue? Test of two hypotheses. Science 216:1335–1337Google Scholar
  15. Gans C, Gorniak GC (1982b) Functional morphology of lingual protrusion in marine toads (Bufo marinus). Am J Anat 163:195–222Google Scholar
  16. Gaupp E (1899) A Ecker's and R Widersheim's Anatomie des Frosches. Zweite Abteilung. Vieweg, BraunschweigGoogle Scholar
  17. Görcs T, Antal M, Oláh E, Székely G (1979) An improved cobalt labeling technique with complex compounds. Acta Biol Acad Sci Hung 30:78–86Google Scholar
  18. Grinnell AD (1966) A study of the interaction between motoneurons in the frog spinal cord. J Physiol 182:612–648Google Scholar
  19. Grobstein P, Comer C (1983) The nucleus isthmi as an intertectal relay for the ipsilateral oculotectal projection in the frogRana pipiens. J Comp Neurol 217:54–74Google Scholar
  20. Grobstein P, Comer C, Kostyk SK (1983) Frog prey capture behavior: Between sensory maps and directed motor output. In: Ewert J-P, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York London, pp 331–347Google Scholar
  21. Grobstein P, Reyes A, Zwanziger L, Kostyk SK (1985) Prey orienting in frogs: Accounting for variations in output with stimulus distance. J Comp Physiol A 156:775–785Google Scholar
  22. Grüsser OJ, Grüsser-Cornehls U (1976) Physiology of the anuran visual system. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 297–385Google Scholar
  23. Grüsser-Cornehls U (1984) The neurophysiology of the amphibian optic tectum. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum Press, New York London, pp 211–245Google Scholar
  24. Ingle DJ (1976) Behavioral correlates of central visual function in anurans. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 435–451Google Scholar
  25. Ingle DJ (1983a) Brain mechanisms of visual localization by frogs and toads. In: Ewert J-P, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York London, pp 177–226Google Scholar
  26. Ingle DJ (1983b) Anatomy and function of frog's tectal efferents. Neurosci Abstr 9:1090Google Scholar
  27. Iwamoto Y, Sasaki S, Suzuki I (1984) Morphological study on monosynaptic connections between reticulospinal neurons and dorsal neck motorneurons in the cat. J Physiol Soc Jpn 46:381Google Scholar
  28. Kitai ST, Bishop GA (1982) Horseradish peroxidase: Intracellular staining of neurons. In: Heimer L, Robards MJ (eds) Neuroanatomical tract-tracing methods. Plenum Press, New York London, pp 263–277Google Scholar
  29. Kostyk SK, Grobstein P (1982) Visual orienting deficits in frogs with various unilateral lesions. Behav Brain Res 6:379–388Google Scholar
  30. Krammer EB, Rath T, Lischka MF (1979) Somatotopic organization of the hypoglossal nucleus: a HRP study in the rat. Brain Res 170:533–537Google Scholar
  31. Lázár G (1969) Efferent pathways of the optic tectum in the frog. Acta Biol Acad Sci Hung 20:171–183Google Scholar
  32. Lázár G (1984) Structure and connections of the frog optic tectum. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum Press, New York London, pp 185–210Google Scholar
  33. Lázár G, Tóth P, Csank G, Kicliter E (1983) Morphology and location of tectal projection neurons in frogs: A study with HRP and cobalt-filling. J Comp Neurol 215:108–120Google Scholar
  34. Lowe AA (1981) The neural regulation of tongue movements. Prog Neurobiol 15:295–344Google Scholar
  35. Lundberg A (1970) The excitatory control of Ia inhibitory pathway. In: Anderson P, Jansen JKS (eds) Excitatory synaptic mechanisms. Universitetsforlaget, Oslo, pp 333–340Google Scholar
  36. Maeda M, Magherini PC, Precht W (1977) Functional organization of vestibular and visual inputs to neck and forelimb motoneurons in the frog. J Neurophysiol 40:225–243Google Scholar
  37. Matesz C, Székely G (1977) The dorsomedial nuclear group of cranial nerves in the frog. Acta Biol Acad Sci Hung 28:461–474Google Scholar
  38. Matesz C, Székely G (1978) The motor column and sensory projections of the branchial cranial nerves in the frog. J Comp Neurol 178:157–176Google Scholar
  39. Matsumoto N (1984) Cobaltic lysine as a neuronal tracer. Seitai no Kagaku 35:304–308Google Scholar
  40. Matsushima T, Satou M, Ueda K (1982) Feeding behavior of Japanese toad: An EMG analysis. Zool Mag 91:462Google Scholar
  41. Matsushima T, Satou M, Ueda K (1984a) Synaptic mechanism of glossopharyngeal-hypoglossal reflex in the toad. J Physiol Soc Jpn 46:378Google Scholar
  42. Matsushima T, Satou M, Ueda K (1984b) Toad's snapping pathway: relationship to the excitatory pathways from glossopharyngeal nerve to tongue-muscle motoneurons. Zool Sci 1:881Google Scholar
  43. Matsushima T, Satou M, Ueda K (in press) An electromyographic analysis of electrically-evoked prey-catching behavior by means of stimuli applied to the optic tectum in the Japanese toad. Neurosci ResGoogle Scholar
  44. Matsushima T, Satou M, Ueda K (in press) Glossopharyngeal and tectal influences on tongue-muscle motoneurons in the Japanese toad. Brain ResGoogle Scholar
  45. Mori K, Kishi K, Ojima H (1983) Distribution of dendrites of mitral, displaced mitral, tufted and granule cells in the rabbit olfactory bulb. J Comp Neurol 219:339–355Google Scholar
  46. Porter R (1967) Cortical actions on hypoglossal motoneurons in cats: a proposed role of a common internuncial cell. J Physiol 193:295–308Google Scholar
  47. Potter HD (1965) Mesencephalic auditory region of the bullfrog. J Neurophysiol 28:1132–1154Google Scholar
  48. Rubinson K (1968) Projections of the tectum opticum of the frog. Brain Behav Evol 1:529–561Google Scholar
  49. Satou M, Ewert J-P (1984) Specification of tecto-motor outflow in toads by antidromic stimulation of tecto-bulbar/spinal pathways. Naturwissenschaften 71:52–53Google Scholar
  50. Satou M, Ewert J-P (1985) The antidromic activation of tectal neurons by electrical stimuli applied to the caudal medulla oblongata in the toad,Bufo bufo L. J Comp Physiol A 157:739–748Google Scholar
  51. Satou M, Mori K, Tazawa Y, Takagi SF (1982) Two types of postsynaptic inhibition in piriform cortex of the rabbit: Fast and slow inhibitory postsynaptic potentials. J Neurophysiol 48:1142–1156Google Scholar
  52. Satou M, Matsushima T, Ueda K (1983a) Prey-catching behavior in the Japanese toad: Analyses of the excitatory pathway from the optic tectum to the tongue-muscle-controlling motoneurons. Proc 5th Annu Meeting Jpn Soc Gen Comp Physiol, p 79Google Scholar
  53. Satou M, Mori K, Tazawa Y, Takagi SF (1983b) Neuronal pathways for activation of inhibitory interneurons in piriform cortex of the rabbit. J Neurophysiol 50:74–88Google Scholar
  54. Satou M, Mori K, Tazawa Y, Takagi SF (1983c) Interneurons mediating fast postsynaptic inhibition in piriform cortex of the rabbit. J Neurophysiol 50:89–101Google Scholar
  55. Satou M, Matsushima T, Ueda K (1984) Neuronal pathways from the tectal ‘snapping-evoking area’ to the tongue-muscle-controlling motoneurons in the Japanese toad: Evidence of the intervention of excitatory interneurons. Zool Sci 1:829–832Google Scholar
  56. Schneider D (1954) Das Gesichtsfeld und der Fixiervorgang bei einheimischen Anuren. Z Vergl Physiol 36:147–164Google Scholar
  57. Stuesse SL, Cruce WLR, Powell KS (1983) Afferent and efferent components of the hypoglossal nerve in the grass frog,Rana pipiens. J Comp Neurol 217:432–439Google Scholar
  58. Székely G (1973) Anatomy and synaptology of the optic tectum. In: Jung R (ed) Central visual information (Handbook of sensory physiology, vol VII/3B). Springer, Berlin Heidelberg New York, pp 1–26Google Scholar
  59. Takei K, Oka Y, Satou M, Ueda K (1984) Localization of motoneurons involved in the prey-catching behavior in the Japanese toad. Zool Sci 1:881Google Scholar
  60. Uemura-Sumi M, Mizuno N, Nomura S, Iwahori N, Takeuchi Y, Matsushima R (1981) Topographical representation of the hypoglossal nerve branches and tongue muscles in the hypoglossal nucleus of macaque monkeys. Neurosci Lett 22:31–35Google Scholar
  61. Weerasuriya A (1983) Snapping in toads: Some aspects of sensorimotor interfacing and motor pattern generation. In: Ewert J-P, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York London, pp 613–627Google Scholar
  62. Weerasuriya A, Ewert J-P (1981) Prey-selective neurons in the toad's optic tectum and sensorimotor interfacing: HRP studies and recording experiments. J Comp Physiol 144:429–434Google Scholar
  63. Wilczynski W, Northcutt RG (1977) Afferents to the optic tectum of the leopard frog: An HRP study. J Comp Neurol 173:219–230Google Scholar

Copyright information

© Springer-Verlag 1985

Authors and Affiliations

  • Masahiko Satou
    • 1
  • Toshiya Matsushima
    • 1
  • Hiroaki Takeuchi
    • 1
  • Kazuo Ueda
    • 1
  1. 1.Zoological Institute, Faculty of ScienceUniversity of TokyoTokyoJapan

Personalised recommendations