Experimental Brain Research

, Volume 105, Issue 1, pp 67–75 | Cite as

Transmission characteristics for the 1:1 linkage between slowly adapting type II fibers and their cuneate target neurons in cat

  • B. D. Gynther
  • R. M. Vickery
  • M. J. Rowe
Research Article

Abstract

Transmission from single, identified, slowly adapting type II (SAII) tactile fibers to their target neurons in the cuneate nucleus was examined in anesthetized cats. Simultaneous recordings were made from cuneate neurons and from fine, intact fascicles of the superficial radial nerve in which it was possible to identify and monitor the activity of each group II fiber. Selective activation of individual SAII fibers was achieved by means of skin stimulation with fine probes, in conjunction with extensive forelimb denervation. Responses were studied for seven SAII-driven cuneate neurons. For three there was unequivocal monitoring of the identified SAII input fiber. However, in six of the seven there was evidence that just one SAII fiber provided suprathreshold input to the cuneate neuron, and neither temporal nor spatial summation was required for reliable transmission. Cuneate impulse rates, in response to SAII inputs lasting 1 s, were less than 250 impulses per second, even though the SAII impulse rates could be 500 s-1. Responses to individual SAII impulses consisted of a burst of 2–3 impulses at low SAII input rates, but burst responses disappeared at high SAII rates. In all three SAII-cuneate pairs studied, the transmission security (the percentage of SAII impulses that evoked cuneate spike output) exceeded 80% in response to static skin displacement and in response to certain frequencies of skin vibration, in particular, at 100–200 Hz, exceeded 98% when the SAII fiber responded near the 1∶1 level (one impulse per vibration cycle). Transmission characteristics for the SAII-cuneate linkage resulted in the cuneate neuron showing tight phaselocking of responses to high-frequency (>100 Hz) vibrotactile stimuli and higher impulse rates than its SAII input (up to input rates of ∼50 impulses s-1). Security of transmission across the SAII-cuneate synapse is similar to that demonstrated previously for tactile fibers of the SAI and Pacinian corpuscle (PC)-related classes, which suggests that there is no marked differential specialization in transmission characteristics for dorsal column nuclei neurons that receive input from different tactile fiber classes. Furthermore, it means that the reported failure of individual SAII fiber inputs to generate conscious sensation in man following intraneural microstimulation is not related to transmission failure at the first central relay.

Key words

Slowly adapting type II Cuneate neuron Synaptic transmission Tactile afferent fiber Somatosensory system Cat 

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References

  1. Amassian VE, Giblin D (1974) Periodic components in the steady-state activity of cuneate neurones and their possible role in sensory coding. J Physiol (Lond) 243: 353–385Google Scholar
  2. Andersen P, Eccles JC, Oshima T, Schmidt RF (1964a) Mechanisms of synaptic transmission in the cuneate nucleus. J Neurophysiol 27: 1096–1116Google Scholar
  3. Andersen P, Eccles JC, Schmidt RF, Yokota T (1964b) Identification of relay cells and interneurons in the cuneate nucleus. JNeurophysiol 27: 1080–1095Google Scholar
  4. Bennett RE, Ferrington DG, Rowe MJ (1980) Tactile neuron classes within second somatosensory area (SII) of cat cerebral cortex. J Neurophysiol 43: 292–309Google Scholar
  5. Brown AG, Gordon, G, Kay RH (1974) A study of single axons in the cat's medial lemniscus. J Physiol (Lond) 236: 225–246Google Scholar
  6. Burgess PR, Petit D, Warren RM (1968) Receptor types in cat hairy skin supplied by myelinated fibers. J Neurophysiol 31: 833–848Google Scholar
  7. Chambers MR, Andres KH, Duering M v, Iggo A (1972) The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. Q J Exp Physiol 57: 417–445Google Scholar
  8. Ferrington DG, Rowe MJ (1980) Differential contributions to coding of cutaneous vibratory information by cortical somatosensory areas I and II. J Neurophysiol 43: 310–331Google Scholar
  9. Ferrington DG, Rowe MJ, Tarvin RPC (1986) High gain transmission of single impulses through dorsal column nuclei of the cat. Neurosci Lett 65: 277–282Google Scholar
  10. Ferrington DG, Rowe MJ, Tarvin RPC (1987a) Actions of single sensory fibers on cat dorsal column nuclei neurons: vibratory signalling in a one-to-one linkage. J Physiol (Lond) 386: 293–309Google Scholar
  11. Ferrington DG, Rowe MJ, Tarvin RPC (1987b) Integrative processing of vibratory information in cat dorsal column nuclei neurons driven by identified sensory fibers. J Physiol (Lond) 386: 311–331Google Scholar
  12. Fyffe REW, Cheema SS, Light AR, Rustioni A (1985) The organization of neurons and afferent fibers in the cat cuneate nucleus. In: Rowe MJ, Willis WD (eds) Development, organization, and processing in somatosensory pathways. Liss, New York, pp 163–173Google Scholar
  13. Golovchinsky V (1980) Patterns of responses of neurons in cuneate nucleus to controlled mechanical stimulation of cutaneous velocity receptors in cat. J Neurophysiol 43: 1673–1699Google Scholar
  14. Greenstein J, Kavanagh P, Rowe MJ (1987) Phase coherence in vibration-induced responses of tactile fibres associated with pacinian corpuscle receptors in the cat. J Physiol (Lond) 386: 263–275Google Scholar
  15. Gordon G, Jukes MGM (1964) Dual organization of the exteroceptive components of the cat's gracile nucleus. J Physiol (Lond) 173: 263–290Google Scholar
  16. Gynther BD, Vickery RM, Rowe MJ (1992a) Responses of slowly adapting type II afferent fibres in cat hairy skin to vibrotactile stimuli. J Physiol (Lond) 458: 151–169Google Scholar
  17. Gynther BD, Vickery RM, Rowe MJ (1992b) Transmission characteristics across a 1∶1 linkage between slowly adapting type II afferents and their cuneate target neurones. Proc Aust Neurosci Soc 3: 75Google Scholar
  18. Macefield G, Gandevia SC, Burke D (1990) Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. J Physiol (Lond) 429: 113–129Google Scholar
  19. Mountcastle VB, Talbot WH, Sakata H, Hyvärinen J (1969) Cortical neuronal mechanisms in flutter vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol 32: 452–484Google Scholar
  20. Ochoa J, Torebjörk E (1983) Sensations evoked by intraneural microstimulation of single mechanoreceptor units innervating the human hand. J Physiol (Lond) 342: 633–654Google Scholar
  21. Rozsos I (1958) The synapses of Burdach's nucleus. Acta Morphol Hung 8: 105–109Google Scholar
  22. Rustioni A, Sotelo C (1974) Synaptic organization of the nucleus gracilis of the cat. Experimental identification of dorsal root fibres and cortical afferents. J Comp Neurol 155: 441–468Google Scholar
  23. Vallbo ÅB, Olsson KÅ, Westberg K-G Clark FJ (1984) Microstimulation of single tactile afferents from the human hand. Sensory attributes related to unit type and properties of receptive field. Brain 107: 727–747Google Scholar
  24. Vickery RM, Gynther BD, Rowe MJ (1992) Vibrotactile sensitivity of slowly adapting type I sensory fibers associated with touch domes in cat hairy skin. J Physiol (Lond) 453: 609–626Google Scholar
  25. Vickery RM, Gynther BD, Rowe MJ (1994) Synaptic transmission etween single slowly adapting type I fibres and their cuneate target neurones in cat. J Physiol (Lond) 474: 379–392Google Scholar
  26. Walberg F (1966) The fine structure of the cuneate nucleus in normal cats and following interruption of afferent fibres. An electron microscopical study with particular reference to findings made in Glees and Nauta sections. Exp Brain Res 2: 107–128Google Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • B. D. Gynther
    • 1
  • R. M. Vickery
    • 1
  • M. J. Rowe
    • 1
  1. 1.School of Physiology and Pharmacology, University of New South WalesSydneyAustralia

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