Intrasomatic changes in the maturing hypoglossal nucleus after axon injury

Abstract

The intrasomatic reactions to different types of peripheral nerve injury during postnatal maturation were investigated by light and electron microscopy. The hypoglossal nerve was crushed in 7 day postnatal (dpn) rats and crushed, ligated or transected in 10 and 21 day rats. Survival intervals ranged from 3 to 40 days postoperative (dpo). Normal and sham operated rats of corresponding ages served as controls. The initial intrasomatic reactions in young (7-10 dpn) rats were identical after each type of nerve injury. These reactions involved the nucleus and the perinuclear cytoplasm: severe nuclear eccentricity and elaborate infoldings of the nuclear membrane were seen. The processes of cytoplasm indenting the nuclear membrane were intensely basophilic and contained numerous polyribosomes and cisterns of rough endoplasmic reticulum (RER). The formation of organized RER was not disrupted after axonal injury. Disorganization, fragmentation and degranulation of the cisterns were not apparent until 13-20 dpo. Comparable nerve injuries to older (21 dpn) rats produced structural alterations of the same organelles. However, the initial intrasomatic response involved the organized RER and the extent of the changes was directly related to the severity of nerve injury. Nuclear changes occurred later and only after nerve ligation and transection. Therefore, two major differences characterized the intrasomatic reactions to axonal injury in young and older motoneurons. The timetable of involvement of two organelles, the nucleus and the organized RER, was reversed in the sequence of intrasomatic reactions after axonal damage during successive periods of postnatal development. The magnitude of intrasomatic reactions to different types of nerve injury was age-dependent.

Axotomy‐induced neuronal death during development

“…In newborn mammals, axotomy leads to morphological changes in both cytoplasmic and nuclear compartments; however, nuclear changes including eccentric nuclear displacement, elaborate infolding of the nuclear membrane, and marked condensation of the nucleolus appear to predominate (Borke, 1983;Clarke, Jones, Lavelle, 199 1 ). As the neurons mature over the next 10 days of life, becoming less dependent on contact with targets for survival, the initial and most pronounced ultrastructural changes occur in cytoplasmic rather than in nuclear structures (Clarke et al,199 1 ) .…”

Alterations in the Local Axonal Environment Influence Target Reinnervation and Neuronal Survival After PostnataI Axotomy

“…In a previous study, only 60% of motoneurons in the hypoglossal nucleus of 10 DPN animals survived until 20 DPO (Blake-Bruzzini et aI., 1997). Another study in which 10 DPN animals were injured and allowed to survive until 13 DPO resulted in 80% survival (Borke, 1983). The slight improvement in neuronal survival in the current study may be explained in several ways.…”

“…Cranial nerve transection in rats one week old produced the death of 60% of hypoglossal motoneurons, whereas transection in animals 3 weeks old produced the death of 30% of hypoglossal motoneurons (Snider and Thanedar, 1989). The 3-week-old animal response was equivalent to the adult animal (Borke, 1983). The differences in neuronal survival between the l-week-old and 3-week-old animals may be due to a feedback loop operating developmentally to prevent neurons from innervating a muscle that has already been properly innervated.…”

“…Differing rates of motoneuron survival have been associated with the age of the animal at the time of injury, the method of nerve injury and the distance of the site of injury from the neuron cell body (Lowrie and Vrbova, 1992). Postnatal animals appear to be especially vulnerable to injury, with 7 DPN rats losing twice the number of hypoglossal neurons following cranial nerve transection as 21 DPN rats (Borke, 1983;Snider and Thanedar, 1989). Failure to reinnervate the tongue musculature may be the cause of a large portion of postnatal motoneuron death in the hypoglossal nucleus after axotomy.…”

Changes of Phospholipid‐Metabolizing and Lysosomal Enzymes in Hypoglossal Nucleus and Ventral Horn Motoneurons During Regeneration of Craniospinal Nerves

“…In this respect, the enhancement of the phospholipase A2 activity observed in the present experiments could probably reflect a sign of a reactive catabolic activity of perineuronal and neuropil glial cells; however, there is no evidence that astrocytes, for instance, take part in significant phagocytosis of presynaptic boutons from the surface of injured neurons (Watson, 1972). On the contrary, it is probable that the stimulated phospholipase A2 activity might be an intrinsic feature of the neuronal metabolism operating on the membranous material (dendritic processes mainly) invaginated into the neuronal cell body during the various phases of chromatolytic soma1 reaction to injury (Veraa et al, 1979;Borke, 1982).…”