Histological demonstration of muscle spindles in the tongue of the rat

doi:10.1016/0003-9969(89)90091-5

Archives of Oral Biology

Volume 34, Issue 7, 1989, Pages 529-534

https://doi.org/10.1016/0003-9969(89)90091-5 Get rights and content

Abstract

The presence and distribution of neuromuscular spindles in the lingual musculature of the laboratory rat is described. The findings counter the commonly held belief that neuromuscular spindles are not found in the tongue musculature of non-primate mammals. The hypothesis that fundamentally different neural systems control lingual movements in primate and non-primate mammals therefore cannot be supported. The differences in the distribution of spindles in primate and non-primate mammals may be related to the patterns of lingual movements and the distribution of muscle fibre types.

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Muscles of the face, tongue and jaws are innervated by motoneurons in the lower brainstem. In most instances, the locations of motoneurons innervating specific muscles have been well characterized. Most of the projections to the oromotor nuclei originate from the brainstem, although in a few instances, cortical and hypothalamic projections have also been identified. Brainstem pathways include projections from orosensory structures (e.g., the trigeminal sensory complex), the nucleus of the solitary tract and the parabrachial nuclei, as well as noradrenergic and serotonergic input from raphe and catecholaminergic nuclei. In addition, midbrain projections to specific subdivisions of the facial nucleus mediate vibrissae, orbital and pinna movements. A large proportion of the projections to the oromotor nuclei, however are from specific regions of the brainstem reticular formation, within which are neurons with projections to multiple oromotor nuclei. These reticular formation structures are integral to the ororhythmic responses of mastication, licking, swallowing, respiration, and whisking.
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Citation Excerpt :
The trigemino-hypoglossal loop may also modulate tongue proprioception and regulate therefore its displacement during suction. This hypothesis is supported by the demonstration that mechanical displacement of the tongue induces afferent activity in the hypoglossal nerve (Bowman and Combs 1968; Zapata and Torrealba 1971; Brancatisano et al., 1999), and although tongue proprioception has still to be clarified, neuromuscular spindles have been described in tongue muscles of many species (see Cooper 1953), including rats (Smith 1989; O'Reilly and Fitzgerald 1990). Another speculation that relates to the findings of double-labelled neurons is supported by data of a previous study in which it has been demonstrated that hypoglossal neurons modulate the electrical activity of the extrinsic pad muscles by inducing different patterns of monosynaptic responses.
We investigated in the rat whether hypoglossal innervation extended to facial muscles other than the extrinsic musculature of the mystacial pad. Results showed that hypoglossal neurons also innervate the masseter muscle. Dil injected into the XII nucleus showed hypoglossal axons in the ipsilateral main trunk of the trigeminal nerve. After Gasser's ganglion crossing, the axons entered into the infraorbital division of the trigeminal nerve and targeted the extrinsic muscles of the mystacial pad. They also spread into the masseter branch of the trigeminal nerve to target the polar portions of the masseter muscle spindles. Retrograde double labelling, performed by injecting Dil into the pad and True Blue into the ipsilateral masseter muscle, showed labelled hypoglossal neurons in the medio-dorsal portion of the XII nucleus. The majority of these neurons were small (15–20 μm diameter), showed fluorescence for Dil and projected to the mystacial pad. Other medium-size neurons (25 μm diameter) were instead labelled with True Blue and projected to the masseter muscle. Finally, in the same area, other small hypoglossal neurons showed double labelling and projected to both structures. Functional hypotheses on the role of these hypoglossal projections have been discussed.
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The distribution of substance P (SP)-containing synaptic terminals in the hypoglossal nucleus (XII) of adult rats was examined by retrograde peroxidase labelling and immunocytochemistry. From the location of peroxidase injections into the tongue and of labelled neurones in the ventral lamina of XII, motor neurones that supply intrinsic vertical, longitudinal and transverse fibres as well as the extrinsic muscle genioglossus appear to have been labelled. SP-containing terminals were found making contact, and sometimes dual synapses, with unlabelled neuronal dendrites but not with retrogradely labelled somata or dendrites. These findings suggest that SP terminals may contact dendrites of interneurones or of neurones supplying other extrinsic muscles located in the anterior part of the tongue. Dual SP-containing synapses between XII motor neurones may be the means by which tongue muscle fibres are recruited and their function synchronized.
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Histological demonstration of muscle spindles in the tongue of the rat

Abstract

Brain Res.

Neurosci. Lett.

Brain Res.

A contribution to the study of the movements of the tongue in animals, with special reference to the cat

J. Anat.

Experimental studies of the mammalian tongue. I. Split tongue experiments

Anat. Rec.

Experimental studies of the mammalian tongue. II. Protrusive mechanism

Anat. Rec.

Motor unitmuscle receptors interactions: design features of the neuromuscular control system

Prog. Clin. Neurophysiol.

Afferent influences on tongue muscle activity

Acta physiol. scand.

Functional anatomy of the association between motor units and muscle receptors

Am. Zool.

Muscle spindles in the intrinsic and extrinsic muscles of the rhesus monkey's (Macaca mulatta) tongue

Anat. Rec.

The sensory component of the hypoglossal nerve in the rabbit

J. Anat., Lond.

Motor unit properties and selective involvement in movement

Exer. Sport. Sci. Rev.

Observations on the problem of the proprioceptive innervation of the tongue

J. Anat., Lond.

Muscle spindles in the intrinsic muscles of the human tongue

J. Physiol.

Morphology-histochemistry of intrinsic lingual muscles in Macaca fasicularis

Neurosci. Abstr.

Afferent fibres of the hypoglossal nerve

J. Anat., Lond.

The structure and source of lingual proprioceptors in the monkey

J. Anat., Lond.

Afferent fibres in the hypoglossal nerve of cat

Acta physiol. scand.