Morphology of developing rat genioglossal motoneurons studied in vitro: Relative changes in diameter and surface area of somata and dendrites

Abstract

This study describes the postnatal change in size of motoneurons in the hypoglossal nucleus that innervate the genioglossus muscle. Such anatomical information is essential for determining the cellular mechanisms responsible for the changes observed in the electrical properties of these motoneurons during postnatal development. The cells analyzed here are part of an earlier study (Núñez-Abades et al. [1994] J. Comp. Neurol. 339:401-420) where 40 genioglossal (GG) motoneurons from four age groups (1-2, 5-6, 13-15, and 19-30 postnatal days) were labeled by intracellular injection of neurobiotin in an in vitro slice preparation of the rat brainstem and their cellular morphology was reconstructed in three-dimensional space. The sequence of postnatal dendritic growth can be described in two phases. The first phase, between birth (1-2 days) and 13-15 days, was characterized by no change in either dendritic diameter (any branch order) or dendritic surface area of GG motoneurons. However, maturation of the dendritic tree produced more surface area at greater distances from the soma by redistributing existing membrane (retracting some terminal branches). During the second phase, between 13-15 days and 19-30 days, the dendritic surface area doubled as a result of an increase in the dendritic diameter across all branch orders and a generation of new terminal branches. In contrast to the growth exhibited by the dendrites, there was little discernible postnatal growth of somata. At all ages, dendrites of GG motoneurons show the largest amount of tapering in the first-and second-order dendrites. The calculated dendritic trunk parameter deviated from a value 1.0, indicating that the dendritic tree of developing GG motoneurons cannot be modeled accurately as an equivalent cylinder. However, the value of this parameter increased with age. Strong correlations were found between the diameter of the first-order dendrite and the dendritic surface area, dendritic volume, combined dendritic length, and, to a lesser extent, the number of terminal dendrites in GG motoneurons. Correlations were also found between somal and dendritic geometry but only when data were pooled across all age groups. These data support earlier studies on kitten phrenic motoneurons, which concluded that postnatal growth of motoneurons was not a continuous process. Based on the fact that there was no growth in the first 2 weeks, the changes in the membrane properties described during this phase of postnatal development (e.g., decrease in input resistance) cannot be attributed to increases in the total membrane surface area of these motoneurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Developmental changes in spinal motoneuron dendrites in neonatal mice

“…As found in rat cranial MNs (Nuñ ez-Abades and Cameron, 1995) and adult cat MNs (Ulfhake and Kellerth, 1981;Cullheim et al, 1987a), we found a clear correlation between the diameters of stem dendrites and the total surface area of the trees (Fig. 8A).…”

“…There is evidence that, in cat and rat motoneurons, the branching structure (topology) of MN dendrites exhibits some simplification during postnatal development (Cameron et al, 1991a; Nuñ ez-Abades et al, 1994; Nuñ ezAbades and Cameron, 1995). In contrast, we found little evidence for such changes during the first 2 postnatal weeks in mice (Table 2).…”

“…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).…”

Postnatal Development of Serotonergic Innervation, 5-HT1AReceptor Expression, and 5-HT Responses in Rat Motoneurons

“…Indeed, activation of 5-HT 1A receptors has been shown to influence neurite growth and synapse formation and to cause release of factors that promote neuronal survival (e.g., S100␤) (WhitakerAzmitia et al, 1990;Whitaker-Azmitia, 1991;Lauder, 1993). In this respect it is interesting to note that, coincident with the time of their maximal 5-HT 1A receptor expression, HMs undergo a period of dendritic reshaping in which the total number of dendritic branches is reduced markedly (Núñez-Abades et al, 1994;Núñez-Abades and Cameron, 1995). It remains to be determined whether the transient expression of 5-HT 1A receptors by HMs participates in some way to orchestrating normal postnatal development in the rat brainstem.…”

Glutamate uptake block triggers deadly rhythmic bursting of neonatal rat hypoglossal motoneurons

“…In the neonatal as well as in the adult rat (Nunez-Abades & Cameron, 1995), HMs comprise the largest population (about 90%; Viana et al 1990) of neurons within the XII nucleus, are large cells (25-50 μm), multipolar in shape and distributed throughout this nucleus (Kitamura et al 1983;Boone & Aldes, 1984). Conversely, interneurons (10-18 μm somatic diamater) are round-to oval-shaped neurons and are much less numerous (Boone & Aldes, 1984).…”