Dendritic development and preferential growth into synaptogenic fields: A quantitative study of Golgi‐impregnated spinal motor neurons

Vaughn, James E.; Barber, Robert P.; Sims, Terry J.

doi:10.1002/syn.890020110

Cited by 84 publications

(47 citation statements)

References 38 publications

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“…These findings are similar to those reported for the postnatal development of other morphological classes, such as multipolar nonpyramidal neurons of the Wistar rat visual cortex . Our results are also consonant with the growth patterns observed for Golgiimpregnated mouse spinal MNs during late embryonic development (Vaughn et al, 1988). In that work, dendrites of embryonic MNs (E11-14) project into the ventrolateral white matter, but at birth project equally into the dorsal and medial gray matter.…”

Section: Discussionsupporting

confidence: 91%

Developmental changes in spinal motoneuron dendrites in neonatal mice

Brewer

Burke

et al. 2005

J of Comparative Neurology

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We examined the age-dependent morphological changes of lumbar spinal motoneurons (MNs) in neonatal Swiss-Webster mice during the first 2 weeks of postnatal life. Neurons labeled by intracellular injection of biocytin in hemisected lumbosacral spinal cords in vitro were reconstructed from serial sections. Digitized data were compared for young (P3; postnatal days 2-4; n ϭ 9) and older animals (P11; postnatal days 10 -13; n ϭ 8). As expected, measures of dendritic size (e.g., stem branch diameter, total surface area, maximum distance to tips, and lateral tree spread) were all significantly greater for P11 than for P3 mice. In contrast, the number of dendrites per MN and parameters related to tree topology (e.g., terminations per tree and maximum branch order), although slightly greater for P11 animals, were not significantly different between the two ages. Dendrite growth appeared to be proportional throughout the tree because the ratios between average terminal and internal branch lengths were similar for the two groups. Furthermore, this elongation was proportional to enlargement of overall spinal cord dimensions. A variety of other morphometric measures showed no significant difference between age groups. The relative constancy of MN dendritic topology up to P13 was surprising, given the striking maturation in motor function during this time period. J. Comp. Neurol. 483:304 -317, 2005 Dendrites are essential elements in understanding neural network connectivity and input/output properties of individual neurons in the central nervous system (see Stuart et al., 2001). Much of our current understanding of the linkage between dendritic morphology and the biophysics of electrotonic current flows within neuronal dendrites is based on early studies of spinal motoneurons (MNs) (Rall, 1959(Rall, , 1960(Rall, , 1977Burke and ten Bruggencate, 1971;Iansek and Redman, 1973;Jack et al., 1975). Aside from historical importance, the influence of MN dendrite morphology on the input/output relations of these cells is clearly relevant to understanding the control of motor unit recruitment. In addition, their involvement in amyotrophic lateral sclerosis (ALS) and other motor neuron diseases has generated considerable interest in the structural and functional development of mammalian MNs in fetal (Allan and Greer, 1997) and early postnatal life (Cameron and He, 1989;Curfs et al., 1993; Nuñ ez-Abades et al., 1993Nuñ ez-Abades and Cameron, 1995;Ramirez and Ulfhake, 1991;Walton and Navarrete, 1991; reviewed in Cameron and Nuñ ez-Abades, 2000).Because of the availability of spontaneous and genetically engineered neurological mutants, the mouse has become a key model species for studies of the influence of specific molecular pathways in the development and maintenance of neuronal dendrites (e.g

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Section: Discussionsupporting

confidence: 91%

Developmental changes in spinal motoneuron dendrites in neonatal mice

Brewer

Burke

et al. 2005

J of Comparative Neurology

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“…Interestingly, in the cervical region this gray matter projection is well established by El 5, the first day in which dorsal root afferent axons can be seen entering the spinal cord. This is in contrast to the developmental sequence reported in amphibia (Jackson and Frank, 1987) and in some previous studies in mammals (Vaughn et al, 1988).…”

Section: Discussioncontrasting

confidence: 55%

Interactions between dorsal root axons and their target motor neurons in developing mammalian spinal cord

et al. 1992

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We have utilized the lipid-soluble tracers Dil and DiA to investigate interactions between group la dorsal root afferent axons and their target motor neurons in developing rat spinal cord. We show here that la axons project toward motor pools in fascicles that exhibit a considerable degree of spatial order. A rough topography is present in that axons that innervate medially located axial motor neurons cross over others in the intermediate zone and follow a separate path along the midline toward their appropriate targets. Surprisingly, we have also found that motor neuron dendritic projections are well established in the transverse plane prior to the arrival of la afferents. Although dendrites from motor pools innervating limb muscles project directly in the path of incoming la afferents, they do not guide afferents to appropriate motor pools. The la afferents pass over the distal dendrites and grow all the way to the border between gray and developing white matter. A significant amount of terminal branching and bouton formation is in the vicinity of motor neuron somata and proximal regions of the dendritic arbors. Few boutons are found near dendrites that project dorsal to the motor pools, and virtually no boutons are found on dendrites in white matter. Our results show that la afferent axons are not guided to appropriate motor pools by random encounters with motor dendrites, and raise the possibility that mechanisms exist that promote an orderly projection of la afferents to particular regions of the ventral horn. The striking lack of innervation of white matter and dorsally directed dendrites by la afferents raises the question of whether descending and intersegmental systems have their initial interactions with these regions of the motor neuron dendritic arbor.

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“…In the absence of NO either because of NMDA receptor block or the knock-out of the nNOS gene, some presynaptic inputs may fail to innervate motor neurons. Reduced growth of motor neuron dendrites would result from the deprivation of the tropic effect of synapses as postulated in the synaptotropic hypothesis of Vaughn et al (1988). Such a scenario is supported by in vitro investigations: the branching of motor neuron dendrites is promoted by coculture with interneurons that form synapses on the cell body and dendrites of motor neurons (O'Brien and Fischbach, 1986).…”

Section: Discussionmentioning

confidence: 91%

The Role of Nitric Oxide and NMDA Receptors in the Development of Motor Neuron Dendrites

Inglis¹,

Furia²,

Zuckerman³

et al. 1998

J. Neurosci.

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Nitric oxide (NO) has been implicated in the establishment of precise synaptic connectivity throughout the neuroaxis in several species. To determine the contribution of NO to NMDA receptor-dependent dendritic growth in motor neurons, we administered the NMDA antagonist MK-801 to wild-type mice and neuronal nitric oxide synthase (nNOS) knock-out mice between postnatal days 7 and 14. Compared to saline-treated wild-type animals the number of dendritic bifurcations was significantly reduced in nNOS knock-out animals and MK-801-treated wildtype animals. There was no significant difference in dendritic bifurcation between MK-801-treated wild-type, MK-801-treated nNOS knock-out, and saline-treated nNOS knock-out animals, suggesting that nNOS knock-out and NMDA receptor block had similar effects. The path of the longest dendrite and the number of primary dendrites was the same in all treatment groups, indicating an effect specific to bifurcation. Sholl analysis revealed that differences in bifurcation numbers occurred between 160 and 320 m from the cell body, the distance at which second, third, and fourth order dendrites are most prevalent. Dendrite order analyses confirmed a significant reduction in numbers, but not lengths, of third and fourth order dendrites in nNOS knock-out and drug-treatment groups. Finally, immunohistochemical examination of the developing spinal cord indicated that NMDA receptors and nNOS are colocalized within interneurons surrounding the motor neuron pool. These results support the view that at least part of NMDA receptordependent arborization of motor neuron dendrites is mediated by the local production of NO within the developing spinal cord.

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Dendritic development and preferential growth into synaptogenic fields: A quantitative study of Golgi‐impregnated spinal motor neurons

Cited by 84 publications

References 38 publications

Developmental changes in spinal motoneuron dendrites in neonatal mice

Developmental changes in spinal motoneuron dendrites in neonatal mice

Interactions between dorsal root axons and their target motor neurons in developing mammalian spinal cord

The Role of Nitric Oxide and NMDA Receptors in the Development of Motor Neuron Dendrites

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