Development of terminals and synapses in laminae I and II of the rat medullary dorsal horn after infraorbital nerve transection at birth.
Infraorbital nerve damage at birth kills neurons and alters anatomical, physiological, and biochemical properties of surviving cells in all portions of the trigeminal brainstem complex, with the exception of laminae I and II of the medullary dorsal horn. The resiliency of laminae I and II may be due to rapid terminal sprouting and reactive synaptogenesis in this region. To test this hypothesis, quantitative electron microscopy revealed the types and numbers of terminals, synapses, and degenerating and growth cone-like profiles in the left laminae I and II at 1, 4, 17, and 90 days after left infraorbital nerve section. Control data were derived from normal newborns and from the right laminae I and II and the left infraorbital nerve of every experimental animal. Deafferented laminae I and II contained a median of 11.7, 8.2, 21.8, and 38.2 synapses/100 microm3 on days 1, 4, 17, and 90, respectively. At corresponding ages, there were 17.1, 19.4, 36.2, and 32 terminals; 14.4, 4.2, 5.1, and 0.3 degenerating profiles; and 4.6, 2.2, 0.1, and 0 growth cone-like profiles/100 microm2. Significant differences from the control right side are: 1) The percentage area occupied by terminals is less on days 1 and 17; 2) terminal density does not increase from day 0 to day 4 as it does on the control side; 3) the density of degenerating profiles is higher on day 17; 4) growth cones are less dense on days 4 and 17; and 5) synapse density is lower on days 1 and 4. Axon number in the infraorbital nerve was highly predictive of terminal and synapse densities in deafferented laminae I and II at all ages. Thus, in laminae I and II, 1) the time course and nature of development are altered by deafferentation at birth; 2) reorganization of terminals and synapses occurs within a day of the lesion; 3) by day 90, there are no remaining lesion effects; and 4) the status of the injured nerve predicts central terminal and synapse densities. These are signs of injury-induced transganglionic degeneration and sprouting. The source of the latter is unknown, although areal fraction data suggest that "replacement" terminals may not be of primary afferent origin.
Golden
J P
JP
Department of Neurology, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
Demaro
J A
JA
Robinson
P L
PL
Jacquin
M F
MF
D000818:Animals; D000831:Animals, Newborn; D003714:Denervation; D005260:Female; D008297:Male; D008526:Medulla Oblongata / Q000166:cytology / Q000254:growth & development*; D008854:Microscopy, Electron; D009410:Nerve Degeneration / Q000502:physiology; D009473:Neuronal Plasticity / Q000502:physiology; D009475:Neurons, Afferent / Q000502:physiology / Q000648:ultrastructure; D009915:Orbit / Q000294:innervation; D017729:Presynaptic Terminals / Q000502:physiology / Q000648:ultrastructure; D051381:Rats; D017207:Rats, Sprague-Dawley / Q000502:physiology*; D013569:Synapses / Q000502:physiology / Q000648:ultrastructure; D014276:Trigeminal Nerve / Q000601:surgery; D014278:Trigeminal Nuclei / Q000166:cytology / Q000254:growth & development*; D014738:Vibrissae / Q000294:innervation