Development of terminals and synapses in laminae I and II of the rat medullary dorsal horn after infraorbital nerve transection at birth

Abstract

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.

Locally released small (non‐protein) ninhydrin‐reacting molecules underlie developmental differences of cultured medullary versus spinal dorsal horn neurons

“…Similar to those found in SDH, neuronal circuits in Vc are very immature at birth (Golden et al. 1997).…”

“…1997). During early post‐natal development, neural degeneration is prominent although the total numbers of terminals and synapses continue to increase during a protracted post‐natal period (Golden et al. 1997).…”

Postnatal development of terminals and synapses in laminae I and II of the rat medullary dorsal horn

“…To reduce interlitter variability, all rats comprising single age groups were taken from the same litter. Tissues were taken from the right, intact brainstems of animals that were subjected within 12 hours of birth to transection of the left infraorbital nerve (for details of this procedure, see the accompanying paper; Golden et al, 1997), a nerve that projects only ipsilaterally . Analysis periods were 12 hours and 1, 4, 17, and 90 days from birth.…”

“…Before discussing these data further, a few methodological issues must be considered. First, with the exception of the cases studied on the day of birth, the animals used here had their left infraorbital nerves cut at birth as part of prior reports (Golden et al, 1993) and the accompanying paper (Golden et al, 1997). Here, the right contralateral brainstem was used to study ''normal'' postnatal development.…”

“…The results indicate that most of the circuits in the superficial medullary dorsal horn develop postnatally. The data also form a baseline for an evaluation of deafferentation-induced plasticity in this region, which is described in the accompanying paper (Golden et al, 1997). Portions of this study have been published in abstract form (Golden et al, 1994).…”