Skip to main content
Log in

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

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

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 via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Song, WJ., 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

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00229028

Key words

Navigation