Elsevier

Brain Research

Volume 832, Issues 1–2, 19 June 1999, Pages 97-111
Brain Research

Research report
Stimulation of the chewing area of the cerebral cortex induces inhibitory effects upon swallowing in sheep

https://doi.org/10.1016/S0006-8993(99)01483-3Get rights and content

Abstract

Mastication and swallowing are two tightly integrated components of food intake behavior. We investigated the effects of stimulating the chewing area of the fronto-orbital cortex (CCx) on some muscles and medullary interneurons (Ins) or motoneurons (Mns) active during swallowing. For the purpose of comparison, the lingual nerve (LN) was also stimulated during the experiments. Electromyography (EMG) and extracellular neuronal recording were used, and swallowing was reflexly induced (RIS) by stimulation of the superior laryngeal nerve (SLN). RIS was almost totally abolished during long-lasting repetitive stimulation of CCx or LN, and was strongly facilitated after stimulation cessation. Short-duration stimulation (one or a few pulses) of both the CCx and LN also inhibited triggering of deglutition when delivered just before the onset of RIS. This inhibition appeared as a delay or total suppression of the EMG and neuronal swallowing activities. It was obvious at the level of the muscles, the hypoglossal Mns and the premotoneurons (PMns; Ins of the ventral medulla near the nucleus ambiguus), as well as at the level of the Ins of the dorsal medulla (within or around the solitary tract nucleus) which are assumed to be the core of the `central pattern generator' (CPG) for swallowing. In addition to the `chewing-related inhibition', many ventral Ins exhibited a short latency synaptic activation after CCx and/or LN stimulation. Therefore, these Ins may play a pivotal role for reflex or cortical fast control of tongue (and jaw) muscles, and for coordinating their contractions in the context of mastication–deglutition interactions.

Introduction

Swallowing is a centrally programmed motor sequence resulting from the activity of hindbrain neurons belonging to the so-called `swallowing center' 9, 11, 12, 13, 17, 20, 21, 24, 29, 30. This center controls the oropharyngeal and the esophageal motor activity involved in swallowing. It is composed of two intimately connected half-centers, and is located in the medulla and pons. It has three functional components: an afferent input system, an efferent system of motoneurons (Mns), and an organizing system of interneurons (Ins; see Fig. 1 in Ref. [40]). The peripheral afferents involved in swallowing converge onto the solitary tract in the caudal region of the medulla. The Mns are spread over the motor nuclei of several cranial nerves, including trigeminal (V), facial (VII), and hypoglossal (XII) nuclei, and the nucleus ambiguus (NA) in the case of the glossopharyngeal (IX) and vagal (X) Mns projecting to striated muscles. The In system which sets up and programs the entire swallowing motor sequence (oropharyngeal and esophageal stages) is located in the solitary tract nucleus and the surrounding reticular formation. Neurons in this region exhibit a sequential pattern of firing, very similar to the sequential activity observed in the muscles, and constitute what is now called the central pattern generator (CPG) of swallowing. Other Ins also involved in swallowing are located close to the motor nuclei (NA, V, XII) and are supposed to be premotoneurons (PMns) serving to switch the CPG program on to the various Mns 6, 9, 10, 18, 20. Therefore, at the medullary level, 2–4 mm in front of the obex, two groups of swallowing Ins can be found 17, 18, 20: those of the dorsal group in or around the nucleus tractus solitarius (NTS); those of the ventral group near the NA.

In previous works 1, 5, 6, 10, we have shown that different muscles supplied by motor nuclei of V (mylohyoid; anterior digastric: Dig; medial pterygoid: Pt) and XII (geniohyoid: GH; hyoglossus; styloglossus) are active not only during swallowing triggered by stimulation of the superior laryngeal nerve (SLN), but also during rhythmic movements of mastication provoked by repetitive stimulation of the fronto-orbital cortex. Besides, by recording single-unit activity of Mns in V and XII motor nuclei, it was noticed that some Mns are involved in both mastication and swallowing, indicating that interactions must exist between the CPGs responsible for the two functions that obviously cannot take place at the same time.

One of us [39] has observed that stimulation of the lingual nerve (LN, a branch of V), which triggered a jaw-opening reflex (possible component of chewing activity), could delay or suppress swallowing normally induced by SLN stimulation. Moreover, when deglutition was already in progress, LN stimulation was able to interrupt the process. These inhibitory effects could be due to interactions between chewing and swallowing CPGs. But, they might also be explained by another hypothesis according to which the LN contains a great variety of sensitive fibers, some of them having opposite effects upon swallowing.

The aim of the present work was to test the hypothesis of interactions between chewing and swallowing CPGs. Using electrophysiological techniques (electromyography: EMG; single-unit recording of swallowing neurons in the medulla oblongata), we investigated the effects of stimulating the chewing area of the cerebral cortex (CCx, located in the fronto-orbital region [7]) upon swallowing induced by SLN stimulation. For the purpose of comparison, LN was also stimulated during the experiments.

Section snippets

Surgery

Experiments were carried out on 24 adult ewes (Merinos, 20–30 kg) of various ages (mostly between 2 and 6 years) under a protocol that respects the `principles of laboratory animal care' (NIH publication No. 86-23, revised 1985) and the French Law on the Protection of Animals (10/19/1987). Anesthesia was induced with a short-duration barbiturate anesthetic, sodium thiopentone (Nesdonal, 40 mg/kg body weight, i.v.) to perform cannulation of the trachea, femoral artery and saphenous vein.

Inhibition of swallowing by stimulation of CCx

In lightly anesthetized sheep, SLN stimulation (100–300 μA or 0.5–3 V; 0.1–0.2 ms; single pulse or short train of pulses at 30 or 200–500 Hz) induced complete motor sequences of deglutition with oropharyngeal and esophageal (peristalsis) components, as indicated by the EMGs of GH, Dig, Pt and CE, respectively (Fig. 1A1, B1, Fig. 2B1). The effects of stimulating the CCx (12–15 V; 0.1–0.5 ms; 3–10 pulses at 500 Hz) were studied from a twofold point of view: triggering and progression of

Discussion

Our data indicated that stimulation of CCx was able to block triggering of reflex deglutition, but not its progression once initiated. This appeared clearly on EMGs of jaw and tongue muscles and also on the activity of medullary swallowing neurons either Mns of XII or Ins of the `swallowing center'. Besides, inhibition of swallowing triggering was still more obvious during a long-lasting repetitive stimulation of CCx (Fig. 2, Fig. 3). But, whatever the parameters of this stimulation, inhibition

Acknowledgements

The authors are grateful to D. Catalin for technical assistance and for preparing the illustration. This study was supported by CNRS (ESA 6034)

References (40)

  • A. Car

    La commande corticale du centre deglutiteur bulbaire

    J. Physiol. (Paris)

    (1970)
  • A. Car

    La commande corticale de la deglutition: I. Sa voie d'expression

    J. Physiol. (Paris)

    (1973)
  • A. Car et al.

    Etude des neurones déglutiteurs pontiques chez la brebis: I. Activité et localisation

    Exp. Brain Res.

    (1982)
  • A. Car et al.

    Activity of neurons located in the region of the hypoglossal motor nucleus during swallowing in sheep

    Exp. Brain Res.

    (1987)
  • A. Car et al.

    Déglutition et contractions oesophagiennes réflexes produites par la stimulation du bulbe rachidien

    Exp. Brain Res.

    (1970)
  • R.W. Doty, Neural organization of deglutition, Handbook of Physiology, Section VI, Vol. IV, Alimentary Canal, Am....
  • R. Dubner, B.J. Sessle, A.J. Storey (Eds.), The Neural Basis of Oral and Facial Function, Plenum, New York, 1978, 483...
  • S. Hamdi et al.

    The cortical topography of human swallowing musculature in health and disease

    Nature Medicine

    (1996)
  • N. Hashimoto et al.

    Induction of rhythmic jaw movements by stimulation of the mesencephalic reticular formation in the guinea pig

    J. Neurosci.

    (1989)
  • F.J. Ingelfinger

    Oesophageal motility

    Physiol. Rev.

    (1958)
  • Cited by (0)

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