Cytoarchitecture of the extranuclear and commissural dendrites of hypoglossal nucleus neurons as revealed by conjugates of horseradish peroxidase with cholera toxin

Wan, X. Steven; Trojanowski, John Q.; Gonatas, Jacqueline O.; Liu, C.N.

doi:10.1016/0014-4886(82)90198-4

Cited by 92 publications

(35 citation statements)

References 19 publications

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“…6a,b;7b,d,f;9f,g). This observation is consistent with several previous reports (Ramon y Cajal, 1909;Odutola, 1976;Wan et al, 1982a;Altschuler et al, 1994). Dendrites directed medially traversed the medial subcompartment (Fig.…”

Section: Discussionsupporting

confidence: 94%

Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat

Aldes

1995

J of Comparative Neurology

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The extent and myotopic organization of the ventral (protrusor) compartment of the hypoglossal nucleus (nXII) in the rat is controversial. Of particular concern is the location of motoneurons that innervate the intrinsic (verticalis, transversus) as compared to extrinsic (genioglossus) tongue protrusor muscles. These issues were investigated with retrograde transport, lesion/degeneration/immunocytochemical, and classic Golgi staining techniques. Results from these experiments demonstrate the following: (1) the ventral compartment extends the entire rostrocaudal length of nXII and is organized into three longitudinally oriented subcompartments, one medial and one lateral within the boundaries of nXII, and one outside the confines of nXII, defined as the lateral accessory subcompartment; 2) the medial and lateral subcompartments contain motoneurons that innervate the intrinsic (verticalis, transversus) and extrinsic (genioglossus) tongue protrusor muscles, respectively, while the lateral accessory subcompartment innervates the geniohyoid muscle; (3) ventral subcompartments are unequal in size and vary along the rostrocaudal dimension of nXII. The medial subcompartment is largest caudally and smallest rostrally, while the converse is true for the lateral subcompartment. By contrast, the lateral accessory subcompartment is present only along the caudal one-half of nXII; (4) medial and lateral subcompartments are further organized into smaller subgroups. Medial and centromedial subgroups are discernible within the medial subcompartment, lateral and centrolateral subgroups within the lateral subcompartment. Both medial and lateral subgroups extend throughout the rostrocaudal length of nXII, whereas the centromedial and centrolateral subgroups are present only along the middle two-thirds of nXII where they form a central motoneuron band; (5) there is an inverse myotopic organization within the medial and lateral subcompartments such that proximal and distal portions of intrinsic and extrinsic protrusor muscles receive innervation from rostral and caudal motoneurons, respectively; and (6) there is a correlation between motoneuron morphology (size, shape and dendritic field domains), subcompartment localization, and myotopic specificity. Motoneurons in the medial subcompartment are small (mean = 23.08 microns), round to globular, with dendrites oriented medially, dorsomedially, dorsolaterally, and caudally, whereas lateral subcompartment motoneurons are large (mean = 29.49 microns), round to triangular, with dendrites directed mainly mediolaterally and dorsally. These data are relevant to understanding the functional organization of nXII and the motor control of the tongue. Results are further discussed relative to the convergence of multifunctional afferent systems in the ventromedial subcompartment of nXII.

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Section: Discussionsupporting

confidence: 94%

Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat

Aldes

1995

J of Comparative Neurology

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“…In the case of GDNF, the pattern of grain distribution was marked by linear arrays of grain accumulation (Fig. 1 F) that closely reflect the known distribution of hypoglossal motoneuron dendrites (Wan et al, 1982). These data indicate that after the retrograde transport of GDNF to hypoglossal cell bodies, a significant fraction of GDNF may be sorted to hypoglossal dendrites, similar to the known movement of tetanus toxin (Fishman and Carrigan, 1987).…”

Section: Resultssupporting

confidence: 66%

Synaptic Targeting of Retrogradely Transported Trophic Factors in Motoneurons: Comparison of Glial Cell Line-Derived Neurotrophic Factor, Brain-Derived Neurotrophic Factor, and Cardiotrophin-1 with Tetanus Toxin

Rind

Butowt²,

Bartheld³

2005

J. Neurosci.

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Glial cell line-derived neurotrophic factor (GDNF), brain-derived neurotrophic factor (BDNF), and cardiotrophin-1 (CT-1) are the most potent neurotrophic factors for motoneurons, but their fate after retrograde axonal transport is not known. Internalized trophic factors may be degraded, or they may be recycled and transferred to other neurons, similar to the known route of tetanus toxin. We tested whether neonatal rat hypoglossal motoneurons target retrogradely transported trophic factors to synaptic sites on their dendrites within the brainstem and subsequently transfer these trophins across the synaptic cleft to afferent synapses (transsynaptic transcytosis). Motoneurons retrogradely transport from the tongue radiolabeled GDNF, BDNF, and CT-1 as well as tetanus toxin. Quantitative autoradiographic electron microscopy showed that GDNF and BDNF were transported into motoneuron dendrites with labeling densities similar to those of tetanus toxin. Although tetanus toxin accumulated rapidly (within 8 h) at presynaptic sites, GDNF accumulated at synapses more slowly (within 15 h), and CT-1 never associated with synapses. Thus, some retrogradely transported neurotrophic factors are trafficked similarly but not identically to tetanus toxin. Both GDNF and BDNF accumulate at the external (limiting) membrane of multivesicular bodies within proximal dendrites. We conclude that tetanus toxin, GDNF, and BDNF are released from postsynaptic sites and are internalized by afferent presynaptic terminals, thus demonstrating transsynaptic transcytosis. CT-1, however, follows a strict degradation pathway after retrograde transport to the soma. Synaptic and transcytotic trafficking thus are restricted to particular neurotrophic factors such as GDNF and BDNF.

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“…The nearest terminals in the tamarin were found in the reticular formation immediately bordering the hypoglossal nucleus, but the closest terminals in the tree shrew were found further distant, namely in the reticular formation bordering the spinal trigeminal nucleus and in the solitary tract nucleus. According to Altschuler et al [1994] and Wan et al [1982], the dendrites of the hypoglossal motoneurons are not limited to the hypoglossal nucleus itself, but reach into the adjacent reticular formation. Therefore, we cannot exclude the suggestion, that there are direct cortico-motoneuronal connections in the tamarin; such connections, if they exist, are limited, however, to the most distal dendrites of the hypoglossal motoneurons.…”

Section: Discussionmentioning

confidence: 99%

Anterograde Projections of the Motorcortical Tongue Area in the Saddle-Back Tamarin <i>(Saguinus fuscicollis)</i>

Alipour¹,

Chen²,

Jürgens³

2002

Brain Behav Evol

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In the New World monkey Saguinus fuscicollis, the anterograde projections of the motorcortical tongue area were studied. Three animals were analyzed. In two, biotin dextran amine was used as tracer; in the third, Phaseolus vulgaris leucoagglutinin was used. Identification of the tongue area was carried out by electrical brain stimulation. Intracortical projections were found into the neighboring primary motor cortex, ventral premotor cortex, frontoopercular cortex, and primary and secondary somatosensory cortex. Projections also ended in the ventrolateral prefrontal cortex, orbital cortex, supplementary motor area, anterior cingulate cortex and agranular as well as granular insula. In addition, weaker labeling was found in the inferior and dorsal parietal cortex, and perirhinal and inferotemporal cortex. Subcortically, there was a heavy projection into the ventral putamen, a moderate projection into the caudate nucleus and claustrum, and a weak projection into the anterior, central and lateral amygdala. In the thalamus, terminal labeling was found in the nuclei ventralis posterior medialis, ventralis lateralis, reticularis, centralis lateralis, medialis dorsalis, pulvinaris oralis, centrum medianum, reuniens and suprageniculatus in an order of intensity. Subthalamically, weak projections could be traced into the zona incerta and lateral hypothalamus. In the midbrain, labeling was found in the deep layers of the colliculus superior, area praetectalis, dorsal reticular formation and, very sparsely, in the periaqueductal gray. In the lower brainstem, fibers ended in the griseum pontis, medial and lateral parabrachial nuclei, lateral pontine and medullary reticular formation, paramedian and dorsal reticular nuclei, solitary tract nucleus and principal as well as spinal trigeminal nuclei. No terminals were found in the hypoglossal nucleus itself; there were, however, terminals in the immediately bordering reticular formation.

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Cytoarchitecture of the extranuclear and commissural dendrites of hypoglossal nucleus neurons as revealed by conjugates of horseradish peroxidase with cholera toxin

Cited by 92 publications

References 19 publications

Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat

Subcompartmental organization of the ventral (protrusor) compartment in the hypoglossal nucleus of the rat

Synaptic Targeting of Retrogradely Transported Trophic Factors in Motoneurons: Comparison of Glial Cell Line-Derived Neurotrophic Factor, Brain-Derived Neurotrophic Factor, and Cardiotrophin-1 with Tetanus Toxin

Anterograde Projections of the Motorcortical Tongue Area in the Saddle-Back Tamarin <i>(Saguinus fuscicollis)</i>

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