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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Projections from the nucleus subceruleus (nSC) to the hypoglossal nucleus (XII) were investigated with complementary retrograde and anterograde axonal transport techniques at the light and electron microscopic level in the rat. Injections of WGA-HRP into XII resulted in labeling of neurons in and around the nSC. Labeled nSC neurons were few in number (less than 4 per 40-60 microns sections) and variable in size and shape. Most labeled nSC neurons were medium-sized (mean = 16.89 microns), fusiform, triangular, or oval, with 3-4 dendrites typically oriented dorsomedially and ventrolaterally. These neurons were found throughout the rostrocaudal extent of the nSC but were most numerous medial, dorsomedial, and ventromedial to the motor trigeminal nucleus. Others were observed rostral to the motor trigeminal nucleus and ventral to the parabrachial nuclear complex. Confirmation of retrograde results was obtained following injections of tritiated amino acids or WGA-HRP into the nSC. This resulted in labeling throughout the rostrocaudal extent of XII mainly ipsilaterally. Labeled fibers descended the brainstem in the dorsolateral and, to a lesser extent, in the ventromedial component of Probst's tract. Fibers entered XII mainly rostrally along the lateral border of the nucleus. All regions of XII were recipients of nSC afferents, but the caudoventromedial quadrant contained the greatest density of terminal labeling. Electron microscopic evaluation confirmed that nSC afferents synapsed on motoneurons in XII. Axon terminals containing WGA-HRP reaction product were found contacting dendrites and somata, but primarily the former (81.3% versus 10.6%). Axodendritic terminals synapsed mainly on medium-to-small sized dendrites (less than 3 microns in diameter). The majority of labeled axodendritic terminals (90.1%) contained small, round, and clear synaptic vesicles (S-type: 20-50 nm) and were associated with an asymmetric (60.6%), symmetric (11.4%), or no (18%) postsynaptic specialization. By contrast, most axosomatic terminals contained flattened vesicles (F-type) and formed a symmetric or no postsynaptic specialization (75%). Large dense core vesicles (55-90 nm) were observed within a small proportion of all labeled axon terminals (1.3%). The results from this study demonstrate that the nSC projects to XII, preferentially targets a specific subgrouping of protrusor motoneurons, and synapses on both somata and dendrites, although mainly on the latter. The implications of these data are discussed relative to tongue control.

The organization of projections from the principal sensory trigeminal nucleus (PSN) to the hypoglossal nucleus (XII) in the rat was investigated at the light and electron microscopic level with retrograde and anterograde axonal tracer techniques. Microiontophoretic injection of horseradish peroxidase (HRP) into XII resulted in retrograde labeling of neurons confined to the dorsal one-third of the PSN. Labeled neurons were found bilaterally, although a clear preponderance for ipsilateral distribution was evident. Most labeled neurons were found in the medial one-third and caudal two-thirds of the PSN. Labeled neurons were large (30-50 micron), round-to-pear shaped multipolar cells with dendrites oriented primarily in the mediolateral direction. At the electron microscopic level, HRP reaction product was found throughout the cytoplasm of soma and processes of PSN projection neurons. The ultrastructural characteristics of these cells included a round, centrally placed nucleus and invaginated nuclear envelope, sparse Nissl bodies, numerous free ribosomes, mitochondria, lysosomes and Golgi complexes. Three to four main stem dendrites gradually tapered from the cell body and numerous synaptic terminals impinged upon soma and dendrites of labeled PSN neurons. Microiontophoretic injection of tritiated amino acids or HRP into the dorsal one-third of the PSN resulted in moderately dense terminal labeling in XII bilaterally, although mainly ipsilaterally. Terminal labeling was found diffusely throughout all regions of XII. Fibers descended the brainstem in the dorsolateral reticular formation and entered XII ventrolaterally. At the electron microscopic level, boutons containing HRP reaction product were found to synapse on dendritic processes in XII. Labeled boutons were characterized by clear, spherical vesicles and an asymmetrical postsynaptic density. The significance of these results are discussed in relation to oro-lingual motor behavior.