Advertisement

Experimental Brain Research

, Volume 25, Issue 5, pp 469–486 | Cite as

Quantitative studies of intracellular postsynaptic potentials in the lateral geniculate nucleus of the cat with respect to optic tract stimulus response latencies

  • U. Th. Eysel
Article

Summary

LGN cells were intracellularly recorded with glass micropipettes. Electrical stimuli of different amplitude and frequency were applied to the optic tract close to the optic chiasm. The cells were classified according to stimulus response latencies of action potentials as belonging to class I (1.0–1.6 msec) or class II (1.7–3.0 msec).

Class I EPSPs had shorter latencies (1.0–1.5 msec), durations (4–12 msec), rise times to peak (0.5–1.4 msec), and decay times (3.0–8.5 msec); the synaptic transmission time was on the average 0.41 msec. Class II EPSPs (1.6–2.6 msec latency) had longer durations (10–30 msec), rise times (1.6–3.7 msec), and decay times (9.0–25 msec); the synaptic transmission time was on the average 0.67 msec.

With repetitive stimulation the EPSPs of latency class I revealed almost no stimulus frequency dependence between 1 and 120 Hz, while class II EPSPs decreased in amplitude between 30 and 70% with increasing frequency. Comparable temporal summation of excitation occurred in cells of both latency classes. Negative serial correlation coefficients of first order were found for consecutive EPSP amplitudes of all cells recorded for sufficient periods of time.

The IPSPs were subdivided into two groups according to their optic tract response latency. Group 1 IPSPs had shorter latencies (2.0–2.6 msec), durations (15–50 msec), and times from the onset to maximal hyperpolarization (2.4–4.2 msec) than group 2 IPSPs (3.0–4.8 msec latency, 40–100 msec duration, 2.7–7.5 msec time from onset to extremum).

The group 2 IPSPs decreased in amplitude by about 90% when the stimulus frequency was increased from 1 to 50 Hz, while the group 1 IPSPs displayed a comparable decrease in the frequency range between 50 and 120 Hz. Effective temporal summation was found in group 2 IPSPs in the frequency range below 70 Hz, and in group 1 IPSPs at stimulus frequencies between 70 and 120 Hz.

The EPSP peak latencies and the latencies to the minimum of IPSPs proved to be invariant with respect to PSP amplitude and stimulus frequency in individual cells. The latencies to the extrema of EPSPs and IPSPs as well as the amplitude values were symmetrically distributed.

Key words

Lateral geniculate nucleus Postsynaptic potentials Latency classification Stimulus frequency dependence Statistical properties 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adey, W.R., Noda, H.: Influence of eye movements on geniculostriate excitability in the cat. J. Physiol. (Lond.) 235, 805–821 (1973)Google Scholar
  2. Barrett, E.F., Barrett, J.N., Martin, A.R., Rahamimoff, R.: A note on the interaction of spontaneous and evoked release at the frog neuromuscular junction. J. Physiol. (Lond.) 237, 453–463 (1974)Google Scholar
  3. Bishop, G.H., Clare, M.: Sequence of events in optic cortex response to volleys of impulses in the radiation. J. Neurophysiol. 16, 490–498 (1953)Google Scholar
  4. Bishop, P.O.: Properties of afferent synapses and sensory neurones in the lateral geniculate nucleus. Int. Rev. Biol. 6, 191–255 (1964)Google Scholar
  5. Bishop, P.O., Evans, W.A.: The refractory period of the sensory synapses of the lateral geniculate nucleus. J. Physiol. (Lond.) 134, 538–557 (1956)Google Scholar
  6. Bishop, P.O., Burke, W., Davis, R.: The interpretation of the extracellular response of single lateral geniculate cells. J. Physiol. (Lond.) 162, 451–472 (1962)Google Scholar
  7. Bittner, G.D.: Differentation of nerve terminals in the crayfish opener muscle and its functional significance. J. gen. Physiol. 51, 731–758 (1968)Google Scholar
  8. Bittner, G.D., Harrison, J.: A reconsideration of the Poisson hypothesis for transmitter release at the crayfish neuromuscular junction. J. Physiol. (Lond.) 206, 1–23 (1970)Google Scholar
  9. Blum, B., Godel, V., Gitter, S., Stein, R.: Impulse propagation from photically discharged neurones in the visual system. Pflügers Arch. 331, 38–43 (1972)Google Scholar
  10. Burke, W., Sefton, A.J.: Recovery of responsiveness of cells of lateral geniculate nucleus of rat. J. Physiol. (Lond.) 187, 213–229 (1966a)Google Scholar
  11. Burke, W., Sefton, A.J.: Inhibitory mechanisms in lateral geniculate nucleus of rat. J. Physiol. (Lond.) 187, 231–246 (1966b)Google Scholar
  12. Chang, H.T., Kaada, B.: An analysis of primary response of visual cortex to optic nerve stimulation of cats. J. Neurophysiol. 13, 305–318 (1950)Google Scholar
  13. Cleland, B.G., Dubin, M.W., Levick, R.W.: Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. J. Physiol. (Lond.) 217, 473–496 (1971a)Google Scholar
  14. Cleland, B.G., Dubin, M.W., Levick, W.R.: Simultaneous recording of input and output of lateral geniculate neurons. Nature (Lond.) 231, 191–192 (1971b)Google Scholar
  15. Coenen, A.M.L., Vendrik, A.J.H.: Determination of the transfer ratio of cat's geniculate neurons through quasi-intracellular recordings and the relation with the level of consciousness. Exp. Brain Res. 14, 227–242 (1972)Google Scholar
  16. Creutzfeldt, O.D., Fuster, J.M., Herz, A., Straschill, M.: Some problems of information transmission in the visual system. In: Eccles, J.C. (ed.): Brain and conscious experience, pp. 138–164. Berlin-Göttingen-Heidelberg-New York: Springer 1964Google Scholar
  17. Eccles, J.C.: The physiology of synapses. Berlin-Göttingen-Heidelberg-New York: Springer 1964Google Scholar
  18. Eysel, U.Th., Grüsser, O.-J.: Simultaneous recording of pre- and postsynaptic potentials during degeneration of optic tract fiber input to the cat lateral geniculate nucleus. Brain Res. 81, 552–557 (1974)Google Scholar
  19. Eysel, U.Th., Grüsser, O.-J.: Intracellular postsynaptic potentials of cat lateral geniculate cells and the effects of degeneration of the optic tract terminals. Brain Res. 98, 441–455 (1975)Google Scholar
  20. Eysel, U.Th., Grüsser, O.-J., Pecci Saavedra, J.: Signal transmission through degenerating synapses in the lateral geniculate body of the cat. Brain Res. 76, 49–70 (1974)Google Scholar
  21. Freund, H.-J.: Neuronal mechanisms of the lateral geniculate body. In: Handbook of Sensory Physiology. Vol. VII, 3B, pp. 177–246. Berlin-Heidelberg-New York: Springer 1973Google Scholar
  22. Fukada, Y.: Receptive field organisation of cat optic nerve fibers with special reference to conduction velocity. Vision Res. 11, 209–226 (1971)Google Scholar
  23. Fukada, Y., Saito, H.: Directionally selective units in the cat's lateral geniculate nucleus. In: Arden, G.B. (ed.): The visual system, pp. 125–136, Plenum Publishing Corporation (1972)Google Scholar
  24. Fuster, J.M., Creutzfeldt, O.D., Straschill, M.: Intracellular recordings of neuronal activity in the visual system. Z. vergl. Physiol. 49, 605–622 (1965)Google Scholar
  25. Guillery, R.W.: The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Z. Zellforsch. 96, 1–38 (1969a)Google Scholar
  26. Guillery, R.W.: A quantitative study of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat. Z. Zellforsch. 96, 39–48 (1969b)Google Scholar
  27. Hoffmann, K.P., Stone, J., Sherman, S.M.: Relay of receptive field properties in dorsal lateral geniculate nucleus of the cat. J. Neurophysiol. 35, 518–531 (1972)Google Scholar
  28. Kato, H., Yamamoto, M., Nakahama, H.: Intracellular recordings from the lateral geniculate neurons of cats. Jap. J. Physiol. 21, 307–323 (1971)Google Scholar
  29. Krnjević, K., Miledi, R.: Presynaptic failure of neuromuscular propagation in rats. J. Physiol. (Lond.) 140, 1–22 (1959)Google Scholar
  30. Kuno, M.: Mechanism of facilitation and depression of the excitatory synaptic potential in spinal motoneurones. J. Physiol. (Lond.) 175, 100–112 (1964)Google Scholar
  31. Levick, W.R., Cleland, B.G., Dubin, M.W.: Lateral geniculate neurons of cat: retinal inputs and physiology. Invest. Ophthal. 11, 302–311 (1972)Google Scholar
  32. Mallart, A., Martin, A.R.: The relation between quantum content and facilitation at the neuromuscular junction of the frog. J. Physiol. (Lond.) 196, 593–604 (1968)Google Scholar
  33. McIlwain, J.T., Creutzfeldt, O.D.: Microelectrode study of synaptic excitation and inhibition in the lateral geniculate nucleus of the cat. J. Neurophysiol. 30, 1–21 (1967)Google Scholar
  34. Morlock, N.L., Perlman, H.L., Marshall, W.D.: Single unit study of posttetanic potentiation and second subnormality in the lateral geniculate body of cats. Exp. Neurol. 11, 38–47 (1965)Google Scholar
  35. Ono, T., Noell, W.K.: Characteristics of Pand I-cells of the cat's lateral geniculate body. Vision Res. 13, 639–646 (1973)Google Scholar
  36. Parnas, I.: Differential block at high frequency of branches of a single axon innervating two muscles. J. Neurophysiol. 35, 903–914 (1972)Google Scholar
  37. Singer, W.: The effect of mesencephalic reticular stimulation on intracellular potentials of cat lateral geniculate neurons. Brain Res. 61, 35–54 (1973a)Google Scholar
  38. Singer, W.: Brain stem stimulation and the hypothesis of presynaptic inhibition in cat lateral geniculate nucleus. Brain Res. 61, 55–68 (1973b)Google Scholar
  39. Singer, W., Bedworth, N.: Inhibitory interaction between X- and Y-units in the cat lateral geniculate nucleus. Brain Res. 49, 291–307 (1973)Google Scholar
  40. Singer, W., Creutzfeldt, O.D.: Reciprocal lateral inhibition of on- and off-center neurons in the lateral geniculate body of the cat. Exp. Brain Res. 10, 311–330 (1970)Google Scholar
  41. Singer, W., Dräger, U.: Postsynaptic potentials in relay neurons of cat lateral geniculate nucleus after stimulation of the mesencephalic reticular formation. Brain Res. 41, 214–220 (1972)Google Scholar
  42. Singer, W., Pöppel, E., Creutzfeldt, O.D.: Inhibitory interaction in the cat's lateral geniculate nucleus. Exp. Brain Res. 14, 210–226 (1972)Google Scholar
  43. Stone, J., Hoffmann, K.P.: Conduction velocity as a parameter in the organization of the afferent relay in the cat's lateral geniculate nucleus. Brain Res. 32, 454–459 (1971)Google Scholar
  44. Suzuki, H., Kato, E.: Binocular interaction at cat's lateral geniculate body. J. Neurophysiol. 29, 909–920 (1966)Google Scholar
  45. Suzuki, H., Takahashi, M.: Organisation of lateral geniculate neurons in binocular inhibition. Brain Res. 23, 261–264 (1970)Google Scholar
  46. Szentágothai, J.: Neuronal and synaptic architecture of the lateral geniculate nucleus. In: Handbook of sensory physiology. Vol. VII, 3B, pp. 141–176. Berlin-Heidelberg-New York: Springer 1973Google Scholar
  47. Tasaki, I., Polley, E.H., Orrego, F.: Action potentials from individual elements in cat geniculate and striate cortex. J. Neurophysiol. 17, 454–474 (1954)Google Scholar
  48. Tömböl, Th.: Terminal arborizations in specific afferents in the specific thalamic nuclei. Acta morph. Acad. Sci. hung. 17, 273–284 (1969)Google Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • U. Th. Eysel
    • 1
  1. 1.Physiologisches InstitutFreie Universität BerlinBerlin 33

Personalised recommendations