Abstract
Neonatal transection of the infraorbital nerve (ION; the trigeminal, V, branch that supplies the mystacial vibrissae follicles) results in an upregulation of galanin in the central arbors of primary afferent axons. The present study was undertaken to evaluate the synaptic organization of these galanin-positive primary afferents and compare it with that of normal neurobiotin/biocytin-labeled primary afferent axons from animals of the same age. Examination of 1200 neurobiotin/biocytin-labeled profiles in V nucleus principalis (PrV) of rats killed on postnatal day (P-) 7 indicated that 23.3% (n=279) of these profiles made synaptic contacts: 87.4% were axodendritic, 8.9% were axoaxonic, 2.8% were axosomatic, and 0.7% were axospinous. Evaluation of 1200 galanin-positive profiles in PrV from rats that sustained transection of the ION on P-0 and were killed on P-7 indicated that only 64 (5.3%) of these profiles made synaptic contacts (P<0.05 compared with the intact animals). Of the galanin-positive profiles that did make synapses in PrV, 81.2% (n=52) were axodendritic and 18.8% (n=12) were axoaxonic. These results indicate that galanin released by damaged ION primary afferents in PrV is likely to affect the activity of second-order V neurons by a paracrine action rather than by acting at specific synapses.
Similar content being viewed by others
References
Arvidsson J (1986) Transganglionic degeneration in vibrissae innervating primary sensory neurons of the rat: a light and electron microscopic study. J Comp Neurol 249: 392–403
Bates CA, Killackey HP (1985) The organization of the neonatal rat's brainstem trigeminal complex and its role in the formation of central trigeminal patterns. J Comp Neurol 240: 265–287
Bear MF, Colman H (1990) Binocular competition in the control of geniculate cell size depends upon visual cortical N-methyl-d-aspartate receptor activation. Proc Natl Acad Sci USA 87: 9246–9249
Bear MF, Cooper LN, Ebner FF (1987) A physiological basis for a theory of synapse modification. Science 237: 42–48
Belford GR, Killackey HP (1980) The sensitive period in the development of the trigeminal system of the neonatal rats. J Comp Neurol 193: 335–350
Chiaia NL, Hess PR, Rhoades RW (1987) Preventing regeneration of infraorbital axons does not alter the ganglionic or transganglionic consequences of neonatal transection of this trigeminal branch. Brain Res Dev Brain Res 36: 75–88
Chiaia NL, Bennett-Clarke CA, Rhoades RW (1991) Effects of cortical and thalamic lesions upon primary afferent terminations, distributions of projection neurons, and the cytochrome oxidase pattern in the trigeminal brainstem complex. J Comp Neurol 303: 600–616
Chiaia NL, Bennett-Clarke CA, Eck M, White FA, Crissman RS, Rhoades RW (1992) Evidence for prenatal competition among the central arbors of trigeminal primary afferent neurons. J Neurosci 12: 62–76
Constantine-Paton M (1990) NMDA receptor as a mediator of activity-dependent synaptogenesis in the developing brain. Cold Spring Harbor Symp Quant Biol 55: 431–443
Cotman CW, Monaghan DT (1988) Excitatory amino acid neurotransmission: NMDA receptors and hebb-type synaptic plasticity. Annu Rev Neurosci 11: 61–80
Durham D, Woolsey TA (1984) Effects of neonatal whisker lesions on mouse central trigeminal pathways. J Comp Neurol 223: 424–447
Fregnac Y, Burke JP, Smith D, Friedlander MJ (1994) Temporal covariance of preand postsynaptic activity regulates functional connectivity in the visual cortex. J Neurophysiol 21: 1403–1421
Henderson TA, Rhoades RW, Bennett-Clarke CA, Osborne PA, Johnson EM, Jacquin MF (1993) NGF augmentation rescues trigeminal ganglion and principalis neurons, but not brainstem or cortical whisker patterns, after infraorbital nerve injury at birth. J Comp Neurol 336: 243–260
Hoeflinger B, Bennett-Clarke CA, Chiaia NL, Killackey HP, Wall JT, Rhoades RW (1993) Lesion-induced changes in the central terminal distribution of galanin-immunoreactive axons in the dorsal column nuclei. J Comp Neurol 332: 378–389
Hökfelt T, Wiesenfeld-Hallin Z, Villar M, Melander T (1987) Increase of galanin-like immunoreactivity in rat dorsal root ganglion cells after peripheral axotomy. Neurosci Lett 83: 217–220
Hökfelt T, Zhang X, Wiesenfeld-Hallen Z (1994) Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17: 22–30
Ide L, Killackey HP (1985) Fine structural survey of the rat's brainstem sensory trigeminal complex. J Comp Neurol 235: 145–168
Kashiba H, Senba E, Kawai Y, Ueda Y, Tohyama M (1992a) Axonal blockade induces the expression of vasoactive intestinal polypeptide and galanin in rat dorsal root ganglion neurons. Brain Res 577: 19–28
Kashiba H, Senba E, Kawai Y, Ueda Y, Tohyama M (1992b) Colocalized but target-unrelated expression of vasoactive intestinal polypeptide and galanin in rat dorsal root ganglion neurons after peripheral nerve injury. Brain Res 582: 47–57
Killackey HP, Shinder A (1981) Central correlates of peripheral pattern alterations in the trigeminal system of the rat. II. The effect of nerve section. Brain Res Dev Brain Res 1: 121–126
Nelson, PG, Yu C, Fields RD, Neale EA (1989) Synaptic connections in vitro: modulation of number and efficacy by electrical activity. Science 244: 585–587
Peters A, Palay SL, Webster HdeF (1991) In: The fine structure of the nervous system. Neurons and their supporting cells, 3rd edn. Oxford University Press, New York, pp 70–100
Rauschecker JP, Singer W (1979) Changes in the circuitry of the kitten visual cortex are gated by postsynaptic activity. Nature 280: 58–59
Renehan WE, Crissman RS, Jacquin MF (1994) Primary afferent plasticity following partial denervation of the trigeminal brain stem nuclear complex in the postnatal rat. J Neurophysiol 14: 721–739
Rhoades RW, Chiaia NL, Macdonald GJ, Jacquin MF (1989) The effect of fetal infraorbital nerve transection upon trigeminal primary afferent projections in the rat. J Comp Neurol 287: 82–97
Savy CS, Margules S, Farkas-Bargeton E, Verley R (1981) A morphometric study of mouse trigeminal ganglion after unilateral destruction of vibrissae follicles at birth. Brain Res 217: 265–277
Scherer WJ, Udin SB (1989) N-Methyl-d-aspartate antagonists prevent interaction of binocular maps in Xenopus tectum. J Neurosci 9: 3837–3843
Schmidt JT (1990) Long-term potentiation and activity-dependent retinotopic sharpening in the regenerating retinotectal projection of goldfish: common sensitive period and sensitivity to NMDA blockers. J Neurosci 10: 233–246
Vaughn JE (1989) Review: fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3: 255–285
Villar MJ, Cortés R, Theodorsson E, Wiesenfeld-Hallin S, Schalling M, Fahrenkrug J, Emson PC, Hökfelt T (1989) Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33: 587–604
Villar MJ, Wiesenfeld-Hallin Z, Xu X-J, Theodorsson E, Emson PC, Hökfelt T (1991) Further studies on galanin-substance P-, and CGRP-like immunoreactivities in primary sensory neurons and spinal cord: effects of dorsal rhizotomies and sciatic nerve lesions. Exp Neurol 112: 29–39
White FA, Hoeflinger BF, Chiaia NL, Bennett-Clarke CA, Crissman RS, Rhoates RW (1994) Evidence for survival of the central arbors of trigeminal primary afferents after peripheral neonatal axotomy: experiments with galanin immunocytochemistry and Di-I labelling. J Comp Neurol 350: 397–411
White FA, Chiaia NL, Macdonald GJ, Rhoades RW (1995) Birthdates and survival after axotomy of neurochemically defined subsets of trigeminal ganglion cells. J Comp Neurol 352: 308–320
Wiesenfeld-Hallin Z, Villar MJ, Hökfelt T (1989) The effects of intrathecal galanin and C-fiber stimulation on the flexor reflex in the rat. Brain Res 486: 205–213
Wiesenfeld-Hallin Z, Xu X-J, Langel U, Bedecs K, Hökfelt T, Bartfai T (1992) Galanin-mediated control of pain: enhanced role after nerve injury. Proc Natl Acad Sci USA 89: 3334–3337
Wiesenfeld-Hallin Z, Xu X-J, Håkanson R, Feng DM, Folkers K, Kristensson K, Villar MJ, Fahrenkrug J, Hökfelt T (1993) On the role of substance P, galanin, vasoactive intestinal peptide, and calcitonin gene-related peptide in mediation of spinal reflex excitability in rats with intact and sectioned peripheral nerves. Ann NY Acad Sci 632: 198–211
Yanagisawa M, Yagi N, Otsuka M, Yanaihara C, Yanaihara N (1986) Inhibitory effects of galanin on the isolated spinal cord of the newborn rat. Neurosci Lett 70: 278–282
Zhang X, Ju G, Elde R, Hökfelt T (1993a) Effect of peripheral nerve cut on neuropeptides in dorsal root ganglia and the spinal cord of monkey with special reference to galanin. J Neurocytol 22: 342–381
Zhang X, Meister B, Elde R, Verge VMK, Hökfelt T (1993b) Large calibre primary afferent neurons projecting to the gracile nucleus express neuropeptide Y after sciatic nerve lesions: an immunohistochemical and in situ hybridization study in rats. Eur J Neurosci 5: 1510–1519
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Crissman, R.S., Zheng, L., Chiaia, N.L. et al. Synaptic organization of damaged infraorbital nerve axons in perinatal rats: demonstration by galanin immunocytochemistry. Exp Brain Res 110, 47–54 (1996). https://doi.org/10.1007/BF00241373
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00241373