Rhythm generation for food-ingestive movements
Introduction
The postnatal development of the conversion from suckling to mastication is a central issue in research on neural mechanisms underlying mammalian food-ingestive movements. It has generally been thought that this conversion is triggered peripherally by the eruption of teeth, because both events coincide in several species, including primates (Bosma,1967, Dubner et al.,1978). Such tooth eruption may not play a generalized essential role, however. For example, dentition is completed at birth in some precocious animals, like the guinea pig (Ainamo, 1971), and yet their nutrition depends totally on suckling during the initial postnatal period. A plastic change in the CNS seems more likely to play a critical role in this species, because the guinea pig is born with a mature oro-facial structure such that its conversion from suckling to mastication can be accomplished without a sensory-input trigger.
Rhythmicity is a fundamental property of both suckling and masticatory movements. It consists of alternating jaw-closing and jaw-opening movements, which are phase-locked to rhythmical activity of the tongue and facial muscles. The overall rhythm is generated centrally by a selected neuronal population in the lower brainstem, which is termed the central rhythm generator (CRG; for review, see Nakamura and Katakura, 1995; see also Grillner and Wallén, Section II; Yamaguchi, and Pearson, Chapters 11 and 12 of this volume). Strikingly, the central issue concerning the postnatal development of the CRG remains open. Is the suckling CRG the same as the masticatory CRG? If different, how is the suckling CRG reorganized to provide mastication?
Substantial data is available on the masticatory CRG, including its localization, cortical and subcortical sources of activation, and the intercalated neurons projecting its output to trigeminal (V) and hypoglossal (XII) motoneurons (Nakamura and Katakura, 1995). Similarly, there is evidence that the suckling CRG is located in the brainstem, and that the corticobulbar projection system involved in its activation is reorganized upon the conversion from suckling to mastication in guinea pigs (Iriki et al., 1988). Despite these noteworthy advances, much remains unknown about the neuronal organization of the CRG for both suckling and mastication. Further advancement requires: (1) identifying the complete neuronal circuitry of the CRG, and its neurons' membrane properties; (2) determining the organization and type of synaptic connections among the CRG neurons; and (3) clarifying the effects of transmitters on these neurons. For such analyses, an in vitro CNS preparation is particularly suitable, like that used in physiological and pharmacological studies on the central rhythm generation for respiration and locomotion. Such latter studies have made use of in vitro CNS block preparations, i.e., those that have included the complete neuronal circuitry for the selected behavior. One such example of this approach is demonstration that excitatory amino acids can initiate and maintain rhythmical locomotor activity in relevant neurons, particularly following activation of their N-methyl-d-aspartate (NMDA) receptors (Nakamura and Katakura, 1995).
In contrast to work on the respiratory and locomotor CRGs, no in vitro preparation has been used previously for study of the suckling and/or masticatory CRG. Here, we report on the development of such a model, using newborn and young rodents.
Section snippets
NMDA-induction of rhythmical activity in n. XII
Figure 1 shows our use of Suzue's (1984) isolated brainstem-spinal cord preparation of the newborn rat. This preparation exhibits spontaneous rhythmical inspiratory burst activities in n. XII and C5 VRs which can continue for >5 h.
Figure 2A shows that bath application of NMDA-induced rhythmical burst activity in n. XII and the C5 VR, following pronounced tonic activity. Under continuous bath application of NMDA, the rhythmical n. XII activity continued steadily for >1 h (Katakura et al., 1995a
Tongue activity inferred from NMDA-induced rhythmical n. XII activity
Rhythmical tongue movements are observed not only during suckling, but also during respiration, mastication and swallowing. Despite such ubiquity, three lines of evidence indicate that NMDA-induced activity in n. XII is the neural representation of rhythmical tongue movements during suckling. (1) NMDA-induced activity in n. XII is distinct from inspiratory activity in cycle length and temporal pattern. (2) Unlike suckling, mastication is not seen in newborn rats. Rather, like the eruption of
Localization of the CRG for NMDA-induced rhythmical n. XII activity
It has been shown that after a midline section of the brainstem, NMDA-induced rhythmical n. XII activity persists on both sides, but with a different rhythm, thereby indicating separate CRGs on each side of the brainstem (Katakura et al., 1995b, Liu, 1997). To identify the neurons of this CRG in the Fig. 1 preparation, we applied sulforhodamine 101, a fluorescent dye taken up by neurons in an activity-dependent manner (Lichtman et al., 1985, Keifer et al., 1992), before and after rhythmical n.
Demonstration of separate CRGs to n. V, VII and XII motoneurons
Both suckling and mastication require coordination of rhythmical jaw, tongue and facial movements. This raises the issue as to whether the rhythmical activities in n. V, VII and XII are generated by a single CRG for these three motoneuron groups or by three separate ones. We addressed this problem in our Fig. 1 preparation, using newborn mice rather than rats, because NMDA-induced n. VII activity is more consistent in the former. First, we recorded simultaneously from n. V's motor root, n. VII
Rhythmical jaw muscle activity induced by pyramidal tract stimulation in an in vitro preparation isolated from the young adult mouse
To study the CRG for masticatory rather than suckling movements in vitro, we developed a preparation as shown in Fig. 1, but it was isolated from adult rats with well-developed mastication. It is not possible to keep a large-size, adult preparation viable solely by diffusion of oxygen from the perfusing solution. It is possible, however, to use Paton's (1996) technique of supplying oxygen by a combination of diffusion from the perfusing solution and transport via the vascular system. (Furuta et
Acknowledgements
Supported by Grants in Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Sciences and Technology.
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1Present address: Department of Welfare and Information, Faculty of Informatics, Teikyo Heisei University, Ichihara 290-0193, Japan. Tel.: +81-436-74-7137; Fax: +81-45-826-4905