Neuronal maturation and synaptogenesis in the rat ventrobasal complex: Alignment with developmental changes in rate and severity of axon reaction

Matthews, Murray A.; Narayanan, C. H.; Narayanan, Y.; Onge, M. F. St.

doi:10.1002/cne.901730407

Cited by 39 publications

(9 citation statements)

References 71 publications

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“…Many active caspase-3-positive cell bodies were Ϸ10 m in diameter (Fig. 5), which is in agreement with the diameter of mouse and rat somatosensory relay neurons during the first week of postnatal development (and more than twice the diameter of nonneuronal cells in the VB) (36,37). Moreover, even though they were dying, in the VB some of these cells displayed morphologies that are typical of barreloid thalamacortical relay neurons ( Fig.…”

Section: Resultssupporting

confidence: 79%

NMDA receptors promote survival in somatosensory relay nuclei by inhibiting Bax-dependent developmental cell death

Vaccari

Casey

Aleem

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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Naturally occurring cell death is a universal feature of developing nervous systems that plays an essential role in determining adult brain function. Yet little is known about the decisions that select a subset of CNS neurons for survival and cause others to die. We report that postnatal day 0 NMDA receptor subunit 1 (NMDAR1) knockout mice display an Ϸ2-fold increase in cell death in the brainstem trigeminal complex (BSTC), including all four nuclei that receive somatosensory inputs from the face (principalis, oralis, interpolaris, and caudalis). Treatment with the NMDA receptor antagonist dizocilpine maleate (MK-801) for 24 h before birth also caused an increase in cell death that reached statistical significance in two of the four nuclei (oralis and interpolaris). The neonatal sensitivity to NMDA receptor hypofunction in the BSTC, and in its main thalamic target, the ventrobasal nucleus (VB), coincides with the peak of naturally occurring cell death and trigeminothalamic synaptogenesis. At embryonic day 17.5, before the onset of these events, NMDAR1 knockout does not affect cell survival in either the BSTC or the VB. Immunostaining for active caspase-3 and the neuronal marker Hu specifically confirms the presence of dying neurons in the BSTC and the VB of NMDAR1 knockout neonates. Finally, genetic deletion of Bax rescues these structures from the requirement for NMDA receptors to limit naturally occurring cell death. Taken together, the results indicate that NMDA receptors play a survival role for somatosensory relay neurons during synaptogenesis by inhibiting Bax-dependent developmental cell death.brainstem ͉ neuroprotection ͉ sensory systems ͉ trophic ͉ ventrobasal N eurons in the peripheral nervous system avoid developmental cell death by successfully competing for a limiting supply of neurotrophins from synaptic target tissues (1). The situation in the developing CNS is less clear, where the survival-promoting action of neurotrophins on central neurons is complemented, facilitated, or replaced by other forms of support (2). A strong candidate for this role is the electrical activity that is present in developing neurons and neural circuits (3-5). Most neurons, including those in the somatosensory relay nuclei, express NMDA receptors before or just after exiting the cell cycle, well before synapses are established (6-10). Eliminating NMDA receptor function dramatically increases neuronal cell death during development (11-17), and NMDA receptor hypofunction has been proposed to play a causal role in fetal alcohol syndrome and schizophrenia (18,19). However, the biological significance and the molecular mechanisms of NMDA receptor-regulated neuronal survival in the intact brain remain largely unknown.NMDA receptors are best known for their role in synaptic plasticity. In the adult brain many forms of long-term potentiation and long-term depression require NMDA receptor function (20). During development, the refinement and plasticity of nascent synapses have also been shown to be dependent on NMDA receptors (2...

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Section: Resultssupporting

confidence: 79%

NMDA receptors promote survival in somatosensory relay nuclei by inhibiting Bax-dependent developmental cell death

Vaccari

Casey

Aleem

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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“…However, the target site and the presynaptic input exert retrograde and anterograde transynaptic effects, respectively, on the biochemical and morphological maturation of the neuron (Landmesser & Pilaf, 1976;Matthews et al, 1977;Black et al, 1979). Based on the present findings, the fate of the neuron after peripheral nerve injury as well as its perisomatic response is in part determined by the developmental stage at which the neuron interacts with its target site and its afferent input.…”

Section: Discussionmentioning

confidence: 98%

“…A phagocytosing cell does not usually engulf a normal-appearing cell part but only one that shows signs of degeneration (Gray & Guillery, 1966;Torvik, 1972;Matthews et al, 1977). It is uncertain whether engulfment leads to enzymatic degradation of the enclosed cell part.…”

Section: Neuronal Engulfment Of Cell Processesmentioning

confidence: 98%

Perisomatic changes in the maturing hypoglossal nucleus after axon injury

Borke

1982

J Neurocytol

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The perisomatic retrograde reactions to peripheral nerve injury during postnatal maturation were investigated by quantitative light and electron microscopy. The hypoglossal nerve was crushed, ligated or transected in 10 and 21 day postnatal (dpn) rats. Only crush injury was made in 7 dpn rats. Survival periods ranged from 3 to 40 days postoperative (dpo). Normal and sham operated animals of corresponding ages served as controls. A remarkable, transient response of neuronal somata in the young (7-10 dpn) rats, following all three types of axon injury, was the formation of excrescences which engulfed neuronal processes: boutons, dendrites, small neurites and a few myelinated axons in adjacent neuropil. The somal engulfment was rarely evident after nerve injury to 21 dpn rats. Bouton displacement from the somal surface, accompanied by glial incursion, followed each type of nerve injury but was less extensive and occurred later in the young rats. There seemed to be no association in the amount of boutons displaced from neuronal somata with the type of nerve injury for any of the three experimental age groups. However, the rate and intensity of the perineuronal glial reaction were related to the severity of the nerve injury in the older (21 dpn) but not in the younger (7-10 dpn) rats. Substantial loss of neurons occurred in the affected nucleus after each type of trauma to the young neurons. The degree of neuronal loss was related to the age and the volume of axoplasm disrupted. Only nerve transection in 21 dpn rats resulted in appreciable neuronal loss. The responses of axotomized neurons, their afferent axon terminals and the surrounding glia are quantitatively and qualitatively different in the hypoglossal nucleus of rats of increasing postnatal ages.

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“…The elaboration of RER was prevented by axotomy to immature, central neurons (Matthews et al, 1977). The lesion, however, unavoidably damaged afferent and efferent fibres.…”

Section: Timetable Of Nuclear and Organized Rer Involvement In The Inmentioning

confidence: 99%

Intrasomatic changes in the maturing hypoglossal nucleus after axon injury

Borke

1983

J Neurocytol

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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.

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Neuronal maturation and synaptogenesis in the rat ventrobasal complex: Alignment with developmental changes in rate and severity of axon reaction

Cited by 39 publications

References 71 publications

NMDA receptors promote survival in somatosensory relay nuclei by inhibiting Bax-dependent developmental cell death

NMDA receptors promote survival in somatosensory relay nuclei by inhibiting Bax-dependent developmental cell death

Perisomatic changes in the maturing hypoglossal nucleus after axon injury

Intrasomatic changes in the maturing hypoglossal nucleus after axon injury

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