Elsevier

Brain Research Reviews

Volume 25, Issue 3, December 1997, Pages 291-311
Brain Research Reviews

Full-length review
Identification of rat brainstem multisynaptic connections to the oral motor nuclei using pseudorabies virus: III. Lingual muscle motor systems

https://doi.org/10.1016/S0165-0173(97)00028-3Get rights and content

Abstract

The present experiments complete our investigations of higher order afferent control of the orofacial muscles by examining the premotor systems controlling the lingual musculature. Pseudorabies virus (PRV) was injected into the extrinsic (protruders: genioglossus and geniohyoid; retractors: hyoglossus and styloglossus) and intrinsic tongue muscles in bilaterally sympathectomized rats. Injection volumes ranged from 1 to 12 μl with average titers of 4×108 pfu/ml and maximum survival times of 90 h. Consistent labeling patterns and distributions occurred across each of the individual muscles and between extrinsic and intrinsic muscle groups, as well as in comparison to the results from the previous masticatory and facial muscle experiments. Virus injections produced a predictable myotopic labeling pattern in the hypoglossal nucleus (Mo 12). Transneuronally labeled neurons occurred in regions known to project directly to Mo 12 motoneurons including the nucleus subcoeruleus, trigeminal sensory areas, parvicellular reticular formation, and the dorsal medullary reticular fields. Maximum survival times revealed more distant connections from medial and lateral reticular zones including the periaqueductal gray, dorsal raphe, laterodorsal and pedunculopontine tegmental areas, and substantia nigra in the midbrain, the gigantocellular region, pontine nucleus caudalis and ventralis, and lateral paragigantocellular region in the pons, and the nucleus of the solitary tract, paratrigeminal region, and paramedian field in the medulla. Thus, injections of PRV into the orofacial muscles revealed a complex, but remarkably uniform network of multisynaptic connections in the brainstem that control and coordinate the activity of the masticatory, facial, and lingual muscles.

Introduction

The first two papers in this sequence summarized experiments designed to identify the higher order (multisynaptic) systems involved in the control of the masticatory and facial muscles 38, 39. The present experiments complete the series by examining similar systems controlling the lingual musculature.

Peripheral control of the lingual musculature originates from temporomandibular joint receptors and sensory fibers contained in the trigeminal, glossopharyngeal, and superior laryngeal nerves [85]. Axons from these nerves terminate in the nucleus of the solitary tract (NST; for abbreviations see Table 1) and spinal trigeminal nuclei but not directly on hypoglossal (Mo 12) motoneurons 12, 28, 59, 97, 120, 123. Retrograde tracers injected directly into Mo 12 label only small numbers of NST neurons 1, 15, 122. This suggests NST influence over Mo 12 motoneuronal activity involves at least a disynaptic circuit that, at present, is undefined 11, 72, 84, 85, 109.

Other sources also modulate lingual muscle activity. For example, the phasic activity that the genioglossus muscle displays during inspiration is attenuated during quiet sleep and may cease altogether during active (REM) sleep 10, 91, 107. Genioglossal hypotonia can have severe consequences as the tonic activity of the genioglossus during inspiration prevents it from occluding the pharyngeal cavity due to the reduced intrapharyngeal pressure 10, 16, 17, 27, 33, 94, 130. The neural pathways responsible for generating hypoglossal motoneuron hypotonia during sleep also are unknown.

The purpose of the present series of experiments was to anatomically identify the sources of higher order control of the lingual musculature. Pseudorabies virus was injected into the genioglossus, geniohyoid, hyoglossus, and styloglossus muscles (extrinsic muscles), as well as into the body of the tongue (intrinsic tongue muscles). The results demonstrate a highly ordered pattern of labeling in the brainstem of both the primary and secondary lingual premotor neurons that is similar to the distributions produced by the masticatory and facial muscle investigations 38, 39.

A preliminary report of these data has been previously presented in abstract form [37].

Section snippets

Materials and methods

A total of 52 adult Sprague-Dawley rats weighing between 300–500 g (Charles River) were used in these experiments (Table 2). The animals were housed under standard conditions with free access to food and water. All experiments conformed to the rules and regulations of this institution's Institutional Care and Use Committee and those of the USDA Animal Welfare Act. The surgical procedures involving bilateral sympathectomies and virus injections were performed as described previously [39]. In

Results

The criteria for establishing the success of a particular injection were the same as those discussed in the previous two reports 38, 39, including producing patterns of infected of Mo 12 motoneurons consistent with the established myotopic representation of Mo 12, and infections present in regions known to provide direct connections with Mo 12. At least four consistent experiments were required in order to complete the injection series for a particular muscle.

The efficacy of transneuronal viral

Discussion

Injecting pseudorabies virus into the extrinsic (protruders: genioglossus and geniohyoid; retractors: hyoglossus and styloglossus) and intrinsic tongue muscles produced virally infected neurons in the primary premotor fields and in brainstem areas separated from Mo 12 motoneurons by two or more synapses. Maximum survival times of 90 h post-infection produced infections in specific nuclear divisions in the brainstem, particularly in medial and lateral midbrain nuclear regions, the ventromedial

Acknowledgements

The authors wish to thank R. Malloy for technical assistance and Dr. Richard Miselis (University of Pennsylvania School of Veterinary Medicine) for constructive criticism. This work comprised a chapter of R.F.'s doctoral thesis and was supported by NIH DC 00240. R.N. is a recipient of an NIMH Research Scientist Award (MH 00653).

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