Expansion of the dendritic tree of motoneurons innervating neck muscles of the adult cat after permanent axotomy

Abstract

The morphologic characteristics of neck motoneurons with intact axons were compared with those of neck motoneurons that had been permanently axotomized for 11 to 17 weeks. Motoneurons were identified antidromically, intracellularly stained with horseradish peroxidase (HRP) and examined after reconstructions of their entire dendritic tree. Axotomized motoneurons differed qualitatively and quantitatively from motoneurons with intact axons. The distal branches of axotomized motoneurons exhibited two novel features: some gave rise to tangled appendages that exhibited growth cone-like specializations resembling lamellipodia and filopodia; others followed a meandering path and had unusually large diameters. These branches showed a discontinuous pattern of staining that was similar to the appearance of myelinated axons stained intra-axonally with HRP. A quantitative analysis of the dendritic trees of 13 completely reconstructed dendritic trees (five axotomized motoneurons and eight motoneurons with intact axons) showed that total dendritic surface area, total dendritic length, and total number of branches increased 38, 34, and 215%, respectively, after axotomy. These measurements were confirmed by comparing the sizes of a larger number of motoneurons (16 axotomized and 21 intact), calculated on the basis of correlations between dendritic tree size and proximal dendritic diameter. We conclude, therefore, that neck motoneurons, in contrast to other types of motoneurons, expand their dendritic trees after axotomy. It is suggested that this expansion is a consequence of two mechanisms: one involves dendritic growth, possibly leading to new synaptic connections; the other causes a conversion of some dendrites into axons.

Electrophysiological characterization of spontaneous recovery in deep dorsal horn interneurons after incomplete spinal cord injury

“…axotomy in cats) motoneuron dendritic tree size actually increases, compared to intact motoneurons, well after the initial injury (11-17 wks; Rose and Odlozinski, 1998). This expansion and increased complexity in dendritic trees would enhance electrotonic filtering as we have observed in the DDH interneurons of long-term SCI mice.…”

Effect of Nonlinear Summation of Synaptic Currents on the Input–Output Properties of Spinal Motoneurons

“…These motoneurons were selected for two reasons. 1) Their qualitative (i.e., dendritic distribution) and quantitative (i.e., dendritic tree surface area) features were typical of a much larger population of motoneurons innervating the same muscle group (Rose 1981;Rose and Odlozinski 1998). 2) Although similar in many respects, each cell had one or more distinctive features.…”

“…In the present study, we have taken advantage of detailed measurements of the dendritic geometry of dorsal neck motoneurons in the cat (Rose and Odlozinski 1998) to construct morphologically realistic compartmental models. These models were further constrained by electron microscopic studies of the density of synapses on these cells (Rose and Neuber-Hess 1991) and physiological studies of the conductance and time course of excitatory and inhibitory synapses on hindlimb motoneurons (Finkel and Redman 1983;Stuart and Redman 1990).…”

Dendrite-Derived Supernumerary Axons on Adult Axotomized Motor Neurons Possess Proteins That Are Essential for the Initiation and Propagation of Action Potentials and Synaptic Vesicle Release

“…Tissue sections containing thick branches of ALPs that did not taper and matched the staining characteristics of myelinated "dendrites" (indicated by the disappearance and reappearance of the process as it traveled through the section) (Cullheim and Kellerth, 1978;Rose and Odlozinski, 1998;Rose et al, 2001) were processed immunohistochemically with either the pan-sodium channel antibody or an antibody against Nav1.2. Other tissue sections that contained ALPs that gave off fine branches that arborized extensively and had structures resembling boutons were processed immunohistochemically for SV2 and/or synaptophysin.…”

“…There is considerable evidence that proximal axotomy may trigger a similar reorganization of neuronal polarity both in vitro (Bradke and Dotti, 2000;Gomis-Rüth et al, 2008) and in vivo (Lindå et al, 1985(Lindå et al, , 1992Havton and Kellerth, 1987;Rose and Odlozinski, 1998;Rose et al, 2001;MacDermid et al, 2002MacDermid et al, , 2004. This reorganization is manifested in the emergence of axon-like processes (ALPs) from the terminals of distal dendrites (Lindå et al, 1985(Lindå et al, , 1992Rose et al, 2001;MacDermid et al, 2002MacDermid et al, , 2004Gomis-Rüth et al, 2008).…”