Evidence that Trigeminal Brainstem Interneurons Form Subpopulations to Produce Different Forms of Mastication in the Rabbit

Abstract

To determine how trigeminal brainstem interneurons pattern different forms of rhythmical jaw movements, four types of motor patterns were induced by electrical stimulation within the cortical masticatory areas of rabbits. After these were recorded, animals were paralyzed and fictive motor output was recorded with an extracellular microelectrode in the trigeminal motor nucleus. A second electrode was used to record from interneurons within the lateral part of the parvocellular reticular formation (Rpc-␣, n ϭ 28) and ␥-subnucleus of the oral nucleus of the spinal trigeminal tract (NVspo-␥, n ϭ 68). Both of these areas contain many interneurons projecting to the trigeminal motor nucleus.The basic characteristics of the four movement types evoked before paralysis were similar to those seen after the neuromuscular blockade, although cycle duration was significantly decreased for all patterns.Interneurons showed three types of firing pattern: 54% were inactive, 42% were rhythmically active, and 4% had a tonic firing pattern. Neurons within the first two categories were intermingled in Rpc-␣ and NVspo-␥: 48% of rhythmic neurons were active during one movement type, 35% were active during two, and 13% were active during three or four patterns.Most units fired during either the middle of the masseter burst or interburst phases during fictive movements evoked from the left caudal cortex. In contrast, there were no tendencies toward a preferred coupling of interneuron activity to any particular phase of the cycle during stimulation of other cortical sites. It was concluded that the premotoneurons that form the final commands to trigeminal motoneurons are organized into subpopulations according to movement pattern.Key words: rhythmical movements; pattern generation; mastication; trigeminal system; brainstem; rabbit To be effective, motor patterns need to be adapted to the needs of the organism. As a result, the same body parts often participate in several stereotyped behaviors that differ only in the ordering and scaling of commands to the same pools of motoneurons (e.g., walking vs running and chewing on the right vs chewing on the left). The way in which neural circuits generate these different patterns has been investigated in many species, particularly in invertebrates, and evidence has been found that three basic forms of architecture exist: dedicated circuitry, distributed circuitry, and reorganizing circuitry (for review, see Morton and Chiel, 1994). It is probable, however, that most of the circuits controlling complex movements have features of more than one of the basic models.Dedicated circuits can generate only one pattern, and when they are triggered by a sensory input, they suppress other ongoing behaviors. The circuit that generates wing retraction in the mollusk Clione limacina seems to be an example of this type (Morton and Chiel, 1994). Reorganizing circuits generate different patterns when the effectiveness of synaptic connections between members of the total population of neurons changes. The key feature...

Transneuronal tracing of vestibulo-trigeminal pathways innervating the masseter muscle in the rat

“…Our data are concordant with the conclusions of most physiological studies, which showed that the latencies of vestibular-elicited masseter muscle responses are too long for these responses to be mediated through direct connections between the VN and Mo5 (Tolu and Pugliatti 1993;Tolu et al 1994Tolu et al , 1996Deriu et al 1999). Potential relays from the VN and PH to masseter motoneurons could include several regions of the pontomedullary reticular formation, particularly the reticular zone surrounding the Mo5, which has been reported to contain neurons that are components of the network responsible for the generation of rhythmic jaw movements (Donga and Lund 1991;Inoue et al 1992;Westberg et al 1998) and to be involved in modulating trigeminal motoneuron activity induced by peripheral and cortical inputs (Sessle 1977;Nozaki et al 1986 a,b;Westberg and Olsson 1991).…”

Strong interactions between spinal cord networks for locomotion and scratching

“…Dual-referent phase analysis relates phase to function more precisely than single-referent phase analysis for rhythmic motor patterns in which duty cycle varies substantially (Berkowitz and Stein 1994). Dual-referent phase analysis is now conventionally used to analyze turtle scratching and swimming and has also been used to analyze rabbit mastication (Westberg et al 1998), neonatal rat locomotor rhythms Kiehn 1999, 2000), neonatal mouse locomotor-like activity (Kwan et al 2009;Nishimaru et al 2006;Zhong et al 2006aZhong et al , b, 2007Zhong et al , 2010Zhong et al , 2011, human walking (Reisman et al 2005), and leech crawling and swimming (Briggman and Kristan 2006).…”

Input–output organization of jaw movement‐related areas in monkey frontal cortex

“…In this context, the supraV may be a key structure for the induction of RJMs. It should also be noted, however, that, together with the supraV, the dorsal part of the principal sensory trigeminal nucleus (Tsuboi et al, 2003), the oral subnucleus of the spinal trigeminal nucleus, and the interV adjacent to this subnucleus (Inoue et al, 1994;Westberg et al, 1998) contain many neurons of which unit activities are synchronized with the jawclosing or jaw-opening phase during fictive mastication induced by cortical stimulation.…”