Skip to main content
SpringerLink
Log in

Inhibition in branched afferent neurons of the bullfrog tongue

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

Single fibers of the bullfrog glossopharyngeal nerve give rise to several peripheral branches, each innervating separate fungiform papillae on the dorsal surface of the tongue. Extracellular electrodes were used to stimulate and record simultaneously from several papillae and from the central branch.

Minor changes in centrally recorded neural output were caused by collision of action potentials originating in separate branches of a common fiber.

Following an antidromic or orthodromic action potential in any branch, a series of excitability changes occured in that branch. Normal excitability was regained within 5 msec of an action potential, but was followed by a secondary decrease in excitability, which reached a minimum approximately 50 msec after the spike, and returned to normal within 200–400 msec after the spike. Subthreshold stimuli caused no depression, while doubling the stimulus strength above threshold did not enhance depression. After several spikes, both amplitude and duration of depression increased. Depression could be evoked even after the gustatory receptors were surgically removed.

Post-stimulus depression in fiber branches is suggested as one source of gustatory adaptation, and may also contribute to interference between stimulating substances.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bittner, G.D.: Differentiation of nerve terminals in the crayfish opener muscle and its functional significance. J. gen. Physiol.51, 731–758 (1968)

    Google Scholar 

  • Brodwick, M.S., Junge, D.: Post-stimulus hyperpolarization and slow potassium conductance increase inAplysia giant neurone. J. Physiol. (Lond.)223, 549–570 (1972)

    Google Scholar 

  • Brush, A.D., Halpern, B.P.: Centrifugal control of gustatory responses. Physiol. Behav.5, 743–746 (1970)

    Google Scholar 

  • Cattell, M., Hoagland, H.: Response of tactile receptors to intermittent stimulation. J. Physiol. (Lond.)72, 392–404 (1931)

    Google Scholar 

  • Catton, W.T.: Excitation and recovery of frog skin tactile receptors. Proc. International Union Physiol. Sci.2, 1025 (1962)

    Google Scholar 

  • Chernetski, K.E.: Sympathetic enhancement of peripheral sensory input in the frog. J. Neurophysiol.27, 493–515 (1964)

    Google Scholar 

  • Clark, J.W., Jr., Plonsey, R.: Fiber interaction in a nerve trunk. Biophys. J.11, 281–294 (1971)

    Google Scholar 

  • Cohen, M.J., Hagiwara, S., Zotterman, Y.: The response spectrum of taste fibres in the cat: a single fibre analysis. Acta physiol. scand.33, 316–332 (1955)

    Google Scholar 

  • Crane, H.D.: Possibilities for signal processing in axon systems, p. 138–153. In: Neural theory and modeling, R.F. Reiss (ed.). Stanford: Stanford University Press 1964

    Google Scholar 

  • Dowling, J.E.: Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates. Proc. roy. Soc. B170, 205–228 (1968)

    Google Scholar 

  • Eaton, D. C.: Potassium ion accumulation near a pace-making cell ofAplysia. J. Physiol. (Lond.)224, 421–440 (1972)

    Google Scholar 

  • Emmers, R.: Modifications of sensory modality codes by stimuli of graded intensity in the cat thalamus. Brain Res.21, 91–104 (1970)

    Google Scholar 

  • Erlanger, J., Gasser, H.S.: Electrical signs of nervous activity, 2nd ed. p. 12, 58. Philadelphia: Univ. Pennsylvania Press 1937

    Google Scholar 

  • Esakov, A.I., Dmitrieva, T.M.: Mechanism of reciprocal interaction between tactile receptors of the skin. Bull. exp. Biol. Med.65, 357–359 (1968) (English translation)

    Google Scholar 

  • Eyzaguirre, C., Fidone, S., Zapata, P.: Membrane potentials recorded from the mucosa of the toad's tongue during chemical stimulation. J. Physiol. (Lond.)221, 515–532 (1972)

    Google Scholar 

  • Fernández, C.: The innervation of the cochlea (guinea pig). Laryngoscope (St. Louis)61, 1152–1172 (1951)

    Google Scholar 

  • Filin, V.A., Esakov, A.I.: Interaction between taste receptors. Bull. exp. Biol. Med.65, 9–11 (1968). (English Translation)

    Google Scholar 

  • Florey, E., Florey, E.: Microanatomy of the abdominal stretch receptors of the crayfish (Astacus fluviatilis L.). J. gen. Physiol.39, 69–85 (1955)

    Google Scholar 

  • Frank, M., Pfaffmann, C.: Taste nerve fibers: a random distribution of sensitivities to four tastes. Science164, 1183–1185 (1969)

    Google Scholar 

  • Gasser, H.S.: The classification of nerve fibers. Ohio J. Sci.41, 145–159 (1941)

    Google Scholar 

  • Gray, E.G.: The spindle and extrafusal innervation of a frog muscle. Proc. roy. Soc. B146, 416–430 (1957)

    Google Scholar 

  • Habgood, J.S.: Sensitization of sensory receptors in the frog's skin. J. Physiol. (Lond.)111, 195–213 (1950)

    Google Scholar 

  • Hagiwara, S., Nakajima, S.: Differences in Na and Ca spikes as examined by application of tetrodotoxin, procaine and manganese ions. J. gen. Physiol.49, 793–806 (1966)

    Google Scholar 

  • Hannam, A.G.: Receptor fields of periodontal mechanosensitive units in the dog. Arch, oral Biol.15, 971–978 (1970)

    Google Scholar 

  • Hellekant, G.: Postexcitatory depression of gustatory receptors. Acta physiol. scand.74, 1–9 (1968)

    Google Scholar 

  • Henkin, R.I.: The metabolic regulation of taste acuity, p. 574–585. In: Olfaction and taste III, C. Pfaffmann (ed.). New York: Rockefeller Univ. Press 1969

    Google Scholar 

  • Icihoka, M.: Neural correlates of taste sensation quality. Experientia (Basel)28, 523–524 (1972)

    Google Scholar 

  • Junge, D., Brodwick, M.S.: Stimulation of frog gustatory units by calcium. Comp. Biochem. Physiol.35, 623–630 (1970)

    Google Scholar 

  • Kallius, E.: Sinnesorgane. Geruchsorgan (Organon olfactus) und Geschmacksorgan, S. 115–270. In: Handbuch der Anatomie des Menschen. K.v. Bardeleben (Hrsg.). Bd. 5, Section 1, Teil 2. Jena: Gustav Fischer 1905

    Google Scholar 

  • Katz, B., Schmitt, O.H.: Electric interaction between two adjacent nerve fibres. J. Physiol. (Lond.)97, 471–488 (1940)

    Google Scholar 

  • Kusano, K.: Analysis of the single unit activity of gustatory receptors in the frog tongue. Jap. J. Physiol.10, 620–633 (1960)

    Google Scholar 

  • Lewis, T., Harris, K.E., Grant, R.T.: Observations relating to the influence of the cutaneous nerves on various reactions of the cutaneous vessels. Heart14, 1–18 (1927)

    Google Scholar 

  • Lindblom, U.F.: Excitability and functional organization within a peripheral tactile unit. Acta physiol. scand.44 (Suppl. 153), 1–84 (1958)

    Google Scholar 

  • Macdonald, J.A.: Interaction between gustatory papillae of the bullfrog tongue. Proc. International Union Physiol. Sci.9, 1056 (1971)

    Google Scholar 

  • Miller, I.J., Jr.: Peripheral interactions among single papilla inputs to gustatory nerve fibers. J. gen. Physiol.57, 1–25 (1971)

    Google Scholar 

  • Mulloney, B., Selverston, A.: Antidromic action potentials fail to demonstrate known interactions between neurons. Science177, 69–72 (1972)

    Google Scholar 

  • Nomura, H., Sakada, S.: Local potential changes at sensory nerve fiber terminals of the frog tongue, p. 345–351. In: Olfaction and taste III, C. Pfaffmann (ed.). New York: Rockefeller Univ. Press (1969)

    Google Scholar 

  • Oakley, B.: The role of taste neurons in the control of the structure and chemical specificity of mammalian taste receptors, p. 63–69. In: Olfaction and taste IV, D. Schneider (ed.). Stuttgart: Wissenschaftliche Verlagsgesellschaft MbH 1972

    Google Scholar 

  • Ogawa, H., Sato, M., Yamashita, S.: Multiple sensitivity of chorda tympani fibres of the rat and hamster to gustatory and thermal stimuli. J. Physiol. (Lond.)199, 223–240 (1968)

    Google Scholar 

  • Ozeki, M.: Conductance change associated with receptor potentials of gustatory cells in rat. J. gen. Physiol.58, 688–699 (1971)

    Google Scholar 

  • Parnas, I.: Differential block at high frequency of branches of a single axon innervating two muscles. J. Neurophysiol.35, 903–913 (1972)

    Google Scholar 

  • Pietra, P., Miraldi, A., Taglietti, V.: Pulse coding in the gustative afferent fibres of the frog gustatory system. Pflügers Arch.331, 307–314 (1972)

    Google Scholar 

  • Rapuzzi, G., Casella, C.: Innervation of the fungiform papillae in the frog tongue. J. Neurophysiol.28, 154–165 (1965)

    Google Scholar 

  • Sato, T.: Adaptation of primary gustatory nerve responses in the frog. Comp. Biochem. Physiol. A43, 1–12 (1972a)

    Google Scholar 

  • Sato, T.: Multiple sensitivity of single taste cells of the frog tongue to four basic taste stimuli. J. Cell Physiol.80, 207–218 (1972b)

    Google Scholar 

  • Sokolove, P.G., Cooke, I.M.: Inhibition of impulse activity in a sensory neuron by an electrogenic pump. J. gen. Physiol.57, 125–163 (1971)

    Google Scholar 

  • Taglietti, V.: Effects of antidromic impulses on frog taste receptors. Arch. Sci. biol.53, 226–234 (1969)

    Google Scholar 

  • Taglietti, V., Casella, C., Ferrari, E.: Interactions between taste receptors in the frog tongue. Pflügers Arch.312, 139–148 (1969)

    Google Scholar 

  • Taglietti, V., Maffini, S., Casella, C.: The recovery cycle of gustatory fibres during chemical stimulation of the tongue. Arch. Sci. biol.55, 155–164 (1971)

    Google Scholar 

  • Tower, S.S.: Unit for sensory reception in cornea. J. Neurophysiol.3, 486–500 (1940)

    Google Scholar 

  • Van Essen, D.C.: The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech. J. Physiol. (Lond.)230, 509–534 (1973)

    Google Scholar 

  • Wall, P.D.: Cord cells responding to touch, damage, and temperature of skin. J. Neurophysiol.23, 197–210 (1960)

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Auckland, Auckland, New Zealand

    John A. Macdonald

  2. Department of Physiology and Pharmacology, Duke University Medical Center, Durham, North Carolina, USA

    Malcolm S. Brodwick

Authors
  1. John A. Macdonald
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Malcolm S. Brodwick
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The authors are particularly grateful for assistance and advice from Dr. Douglas Junge, of the School of Dentistry and Department of Physiology at the University of California, Los Angeles. The reported work was supported by NIDR Contract No. 69-2227 to Dr. Junge, and was carried out while one of the authors (JAM) held a PHS postdoctoral traineeship with the Department of Zoology, U.C.L.A., and the other (MSB) held a NIH predoctoral traineeship with the Department of Anatomy, U.C.L.A. Draughts of the paper have been read and criticized by Dr. Junge and Dr. J. P. Leader, of Auckland University.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Macdonald, J.A., Brodwick, M.S. Inhibition in branched afferent neurons of the bullfrog tongue. J. Comp. Physiol. 87, 293–316 (1973). https://doi.org/10.1007/BF00695265

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00695265

Keywords

Search

Navigation