Advertisement

Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

An electrophysiological study of a transient ipsilateral interpositorubral projection in neonatal cats

  • 27 Accesses

  • 3 Citations

Summary

We examined whether transient projections in the developing central nervous system of Mammalia form functional synapses on their target neurons, using transient ipsilateral interpositorubral (iIR) projection in kittens as a model system. Intracellular recordings were made from red nucleus (RN) neurons in 26 kittens aged 6–26 postnatal days (PD6-26). RN neurons were identified by monosynaptic excitatory postsynaptic potentials (EPSPs) evoked by stimulation of contralateral nucleus interpositus (IN), and additionally by intracellular staining in a few cells. Sixty-nine out of 362 RN neurons responded to stimulation of the ipsilateral IN. Of the 69 cells, 25 showed depolarizing responses with relatively short latency (2.1–6.7 ms) in kittens up to PD20. Such responses were not observed in older animals. Varying stimulus strength revealed that the potentials were unitary. Paired-pulse facilitation of the potential was observed, suggesting that the depolarizations are EPSPs. Several lines of evidence were obtained suggesting that the EPSPs are evoked monosynaptically. They followed high-frequency stimulation up to 50 Hz, and their latencies remained constant with varying stimulus strength. The latencies of ipsilaterally induced EPSPs were always longer than those of contralateral ones, evidence consistent with the longer course of ipsilaterally projecting axons than that of contralateral ones (Song and Murakami 1990). The age of disappearance of the monosynaptic EPSPs, i.e., PD20, also corresponds roughly with that of the anatomically demonstrable iIR fibers (PD15–PD25; Song and Murakami 1990). It is thus concluded that the transient iIR fibers in kittens form functional synapses on RN neurons.

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

References

  1. Armstrong DM (1988) The supraspinal control of mammalian locomotion. J Physiol (Lond) 405:1–37

  2. Brown TH, Kairiss EW, Keenan CL (1990) Hebbian synapses: biophysical mechanisms and algorithms. Annu Rev Neurosci 13:475–511

  3. Buchanan J, Sun Y-A, Poo M-M (1989) Studies of nerve-muscle interactions in Xenopus cell culture: fine structure of early functional contacts. J Neurosci 9(5):1540–1554

  4. Campbell G, Shatz CJ (1992) Synapses formed by identified retinogeniculate axons during the segregation of eye input. J Neurosci 12:1847–1858

  5. Changeux J-P, Danchin A (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264:705–712

  6. Clarke PGH (1985) Neuronal death in the development of the vertebrate nervous system. Trends Neurosci 8:345–349

  7. Constantine-Paton M, Cline HT, Debski E (1990) Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. Annu Rev Neurosci 13:129–154

  8. Gorodnov VL, Fanardjian VV (1987) Functional properties of the cerebellorubral synapses in the cat. Brain Res 410:340–342

  9. Hebb DO (1949) The organization of behavior. Wiley, New York

  10. Horikawa K, Armstrong WE (1988) A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25:1–11

  11. Innocenti GM, Fiore L, Caminiti R (1977) Exuberant projection into the corpus callosum from the visual cortex of newborn cats. Neurosci Lett 4:237–242

  12. Jackson H, Parks TN (1982) Functional synapse elimination in the developing avian cochlear nucleus with simultaneous reduction in cochlear nerve axon branching. J Neurosci 2:1736–1743

  13. Jeffery G, Arzymanow BJ, Lieberman AR (1984) Does the early exuberant retinal projection to the superior colliculus in the neonatal rat develop synaptic connections? Brain Res Dev Brain Res 14:135–138

  14. Leonard CT, Goldberger ME (1987) Consequences of damage to the sensorimotor cortex in neonatal and adult cats. II. Maintenance of exuberant projections. Brain Res Dev Brain Res 32:15–30

  15. Lichtman JW (1977) The reorganization of synaptic connexions in the rat submandibular ganglion cells during post-natal development. J Physiol (Lond) 273:155–177

  16. Mariani J, Changeux J-P (1981) Ontogenesis of olivocerebellar relationships. I. Study by intracellular recordings of the multiple innervation of Purkinje cells by climbing fibers in the developing rat cerebellum. J Neurosci 1:696–702

  17. Masuda Y, Suzuki Y (1981) Establishment of an experimental cat breeding colony. In: Nakano K, Maejima K (eds) The cat as an experimental animal (in Japanese). Soft Science, Tokyo, pp 100–107

  18. Murakami F, Higashi S (1988) Presence of crossed corticorubral fibers and increase of crossed projections after unilateral lesions of the cerebral cortex of the kitten: a demonstration using anterograde transport of Phaseolus vulgaris leucoagglutinin. Brain Res 447:98–108

  19. Murakami F, Saito Y, Higashi S, Oikawa H (1991) Synapses formed by ectopic corticofugal axons: an electron microscopic study of crossed corticorubral projections in kittens. Neurosci Lett 131:49–52

  20. Panneton WM, Tolbert DL (1984) The collateral origin of a transient cerebrocerebellar pathway in kittens. A study using fluorescent double-labeling techniques. Brain Res Dev Brain Res 14:247–254

  21. Purves D, Lichtman JW (1980) Elimination of synapses in the developing nervous system. Science 210:153–157

  22. Purves D, Lichtman JW (1985) Rearrangement of developing neuronal connections. In: Purves D, Lichtman JW (eds) Principles of neural development. Sinauer, Sunderland, pp 271–300

  23. Rakic P (1986) Mechanism of ocular dominance segregation in the lateral geniculate nucleus: competitive elimination hypothesis. Trends Neurosci 9:11–15

  24. Redfern PA (1970) Neuromuscular transmission in new-born rats. J Physiol (Lond) 209:701–709

  25. Shatz CJ (1990) Impulse activity and the patterning of connection during CNS development. Neuron 5:745–756

  26. Shatz CJ, Kirkwood PA (1984) Prenatal development of functional connections in the cat's retinogeniculate pathway. J Neurosci 4:1378–1397

  27. Song W-J, Murakami F (1990) Ipsilateral interpositorubral projection in the kitten and its relation to post-hemicerebellectomy plasticity. Brain Res Dev Brain Res 56:75–85

  28. Song W-J, Kobayashi Y, Yamazaki M, Murakami F (1990) Regressive aberrant projections in the developing CNS of mammalia are functional (abstract). Neurosci Res [Suppl] 11:34

  29. Sretavan DW, Shatz CJ (1986) Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus. J Neurosci 6:234–251

  30. Stanfield BB (1984) Postnatal reorganization of cortical projections: the role of collateral elimination. Trends Neurosci 7:37–41

  31. Stanfield BB, O'Leary DDM, Fricks C (1982) Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature 298:371–373

  32. Stent GS (1973) A physiological mechanism for Hebb's postulate of learning. Proc Natl Acad Sci USA 70:997–1001

  33. Tolbert DL, Panneton WM (1983) Transient cerebrocerebellar projections in kittens: postnatal development and topography. J Comp Neurol 221:216–228

  34. Tsukahara N, Kosaka K (1968) The mode of cerebral excitation of red nucleus neurons. Exp Brain Res 5:102–117

  35. Tsukahara N, Toyama K, Kosaka K (1967) Electrical activity of red nucleus neurons investigated with intracellular microelectrodes. Exp Brain Res 4:18–33

  36. Tsukahara N, Fuller DRG, Brooks VB (1968) Collateral cortical influences on the corticorubrospinal system. J Neurophysiol 31:467–484

  37. Tsukahara N, Fujito Y, Kubota M (1983) Specificity of the newly-formed corticorubral synapses in the kitten red nucleus. Exp Brain Res 51:45–56

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Song, W., Kobayashi, Y. & Murakami, F. An electrophysiological study of a transient ipsilateral interpositorubral projection in neonatal cats. Exp Brain Res 92, 399–406 (1993). https://doi.org/10.1007/BF00229028

Download citation

Key words

  • Transient projection
  • Synapse elimination
  • Red nucleus
  • Nucleus interpositus
  • Intracellular recording
  • Cat