Central distribution of cervical primary afferents in the rat, with emphasis on proprioceptive projections to vestibular, perihypoglossal, and upper thoracic spinal nuclei

Abstract

The projections of primary afferents from rostral cervical segments to the brainstem and the spinal cord of the rat were investigated by using anterograde and transganglionic transport techniques. Projections from whole spinal ganglia were compared with those from single nerves carrying only exteroceptive or proprioceptive fibers. Injections of horseradish peroxidase (HRP) or wheat germ agglutinin-horseradish peroxidase conjugate (WGA-HRP) were performed into dorsal root ganglia C2, C3, and C4. Free HRP was applied to the cut dorsal rami C2 and C3, greater occipital nerve, sternomastoid nerve, and to the C1/2 anastomosis, which contains afferents from suboccipital muscles and the atlanto-occipital joint. WGA-HRP injections into ganglia C7 and L5 were performed for comparative purposes. Injections of WGA-HRP or free HRP into rostral cervical dorsal root ganglia and HRP application to C2 and C3 dorsal rami produced labeling in dorsal and ventral horns at the level of entrance, the central cervical nucleus, and in external and main cuneate nuclei. From axons ascending to pontine and descending to upper thoracic spinal levels, medial collaterals were distributed to medial and descending vestibular, perihypoglossal and solitary nuclei, and the intermediate zone and Clarke's nucleus dorsalis in the spinal cord. Lateral collaterals projected mainly to the trigeminal subnucleus interpolaris and to lateral spinal laminae IV and V. Results from HRP application to single peripheral nerves indicated that medial collaterals were almost exclusively proprioceptive, whereas lateral collaterals were largely exteroceptive with a contribution from suboccipital proprioceptive fibers. WGA-HRP injections into dorsal root ganglia C7 and L5 failed to produce significant labeling within vestibular and periphypoglossal nuclei, although they demonstrated classical projection sites within the brainstem and spinal cord. The consistent collateralisation pattern of rostral cervical afferents along their whole rostrocaudal course enables them to contact a variety of precerebellar, vestibulospinal, and preoculomotor neurons. These connections reflect the well-known significance of proprioceptive neck afferents for the control of posture, head position, and eye movements.

Vertigo in patients with cervical spine dysfunction

“…ment C2/C3 are thought unlikely to be a cause of vertigo [27,28]. Clinical experience correlates with anatomical studies, which were able to identify links between cervical spine receptors and vestibular nuclei [1,2,[17][18][19]. A large supply of receptors was found in neck muscles, especially when muscles were short and in close proximity to facet joints [6].…”

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

“…Foremost, it is Fractional areas (FA), percentages of silver grains (%), and LDs in hypoglossal motoneuron cell bodies 8 and 15 h after tongue injections in neonatal rat pups crucial for our claim of retrograde transcytosis that we can rule out the possibility that the radioactive material could have arrived in afferent synapses by any route other than retrograde axonal transport. This is the case, because the rat tongue lacks proprioceptive afferent innervation (Neuhuber and Zenker, 1989), and there is no sensory monosynaptic pathway to the hypoglossal motor nucleus in rats (Fay and Norgren, 1997;Zhang et al, 2001). Thus, the circuitry of the hypoglossal model system chosen for this analysis allows us to draw conclusions that would not be possible in spinal or trigeminal motor circuits.…”

“…This model system was chosen because hypoglossal motoneurons lack direct monosynaptic afferent proprioceptive input from the tongue (Neuhuber and Zenker, 1989;Fay and Norgren, 1997;Zhang et al, 2001), thus providing a "clean" retrograde transport model system devoid of any potential contamination of afferent synapses on motoneurons by anterograde (sensory) axonal transport. We compared the accumulation and transsynaptic transfer of BDNF, GDNF, CT-1, and tetanus toxin in the hypoglossal nucleus.…”

Sex Differences in Brainstem Neural Activation after Injury to the TMJ Region

“…Comparisons with the distribution of central terminals seen after transganglionic labeling of trigeminal [Jacquin et al, 1983;Takemura et al, 1987], upper cervical [Pfaller and Arvidsson, 1988;Neuhuber and Zenker, 1989], or vagal afferent nerves [Contreras et al, 1982], suggested a high percentage of Fos-positive neurons produced at the dPa5 and Vc/C2 junction region resulted from direct input from primary afferent fibers. By contrast, Fos-LI produced at the Vi/Vc-vl transition region more likely represented third-or higher-order neurons since few primary afferent fibers project from the TMJ region to this brainstem area.…”