Organization of projections from the principal sensory trigeminal nucleus to the hypoglossal nucleus in the rat: an experimental light and electron microscopic study with axonal tracer techniques

Abstract

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.

Trigeminal projections to hypoglossal and facial motor nuclei in the rat

“…Although the major projection from the 5c, 5i, and 5o originated from neurons located in the dorsal part of the nuclei, some neurons scattered in the intermediate and ventral regions of the 5i/5o and in the ventral and lateral part of the 5c are also sources of projection to the XII. In agreement with previous data, only neurons located dorsally in the 5P project to the XII (Travers and Norgren, 1983;Aldes and Boone, 1985). With regard to the target neurons in the XII, our anterograde and retrograde tracing methods demonstrate that both dorsal and ventral regions of the motor nucleus receive a trigeminal projection.…”

“…Earlier reports in rats have identified the dorsal portion of the 5c, 5o, 5i, and 5P as sources of hypoglossal afferents (Borke et al, 1983;Travers and Norgren, 1983;Aldes and Boone, 1985;Borke and Nau, 1987;Dobbins and Feldman, 1995). Recently, after injections of pseudorabies virus in the lateral branch of the XIIth nerve, Dobbins and Feldman (1995) were not able to confirm a trigeminal 5P projection to the XII but noted additional few transsynaptic labeled neurons in the ventral 5c and 5i.…”

“…Direct observations based on retrograde or anterograde tracing experiments showed trigeminohypoglossal projections from neurons located in the dorsal part of the 5P, 5o, and 5i (Borke et al, 1983;Travers and Norgren, 1983;Aldes and Boone, 1985). Only few data exist about 5c-hypoglossal connections (Dobbins and Feldman, 1995).…”

Dysfunctional Sensory Modalities, Locus Coeruleus, and Basal Forebrain: Early Determinants that Promote Neuropathogenesis of Cognitive and Memory Decline and Alzheimer’s Disease

“…The afferent sensory information arising from the intranasal, intraoral-faucial, and pharyngeal areas are transmitted via trigeminal nerve (V) to the sensory trigeminal complex in the pontomedullary reticular formation (PRF) (Zerari-Mailly et al 2001;Daulatzai 2011Daulatzai , 2012b. The sensory information is then projected to motor nuclei of the XIIth nerve, also located in the PRF (Aldes and Boone 1985;Dauvergne et al 2001). Further, this area receives a significant input from the visual, vestibular, proprioceptive, and somatosensory stimuli; there is a convergence, therefore, of various sensory modalities here.…”

“…The hypoglossal premotor neurons in the rat (and possibly other mammals) are located in the pontomedullary reticular formation (Li et al 1993;Popratiloff et al 2001). This region is largely involved in respiration (Aldes and Boone 1985). The hypoglossal motor nuclei, through the XIIth cranial nerve hypoglossal, precisely coordinate tongue movements and buccopharyngeal behavior in the upper airway functions.…”