Intracellular analysis of trigeminal motoneuron rhythmical activity during stimulation of pontomedullary reticular formation in anesthetized guinea pig

1989 ◽  
Vol 62 (6) ◽  
pp. 1225-1236 ◽  
Author(s):  
S. M. Gurahian ◽  
S. H. Chandler ◽  
L. J. Goldberg

1. The effects of repetitive stimulation of the nucleus pontis caudalis and nucleus gigantocellularis (PnC-Gi) of the reticular formation on jaw opener and closer motoneurons were examined. The PnC-Gi was stimulated at 75 Hz at current intensities less than 90 microA. 2. Rhythmically occurring, long-duration, depolarizing membrane potentials in jaw opener motoneurons [excitatory masticatory drive potential (E-MDP)] and long-duration hyperpolarizing membrane potentials [inhibitory masticatory drive potentials (I-MDP)] in jaw closer motoneurons were evoked by 40-Hz repetitive masticatory cortex stimulation. These potentials were completely suppressed by PnC-Gi stimulation. PnC-Gi stimulation also suppressed the short-duration, stimulus-locked depolarizations [excitatory postsynaptic potentials (EPSPs)] in jaw opener motoneurons and short-duration, stimulus-locked hyperpolarizations [inhibitory postsynaptic potentials (IPSPs)] in jaw closer motoneurons, evoked by the same repetitive cortical stimulation. 3. Short pulse train (3 pulses; 500 Hz) stimulation of the masticatory area of the cortex in the absence of rhythmical jaw movements activated the short-latency paucisynaptic corticotrigeminal pathways and evoked short-duration EPSPs and IPSPs in jaw opener and closer motoneurons, respectively. The same PnC-Gi stimulation that completely suppressed rhythmical MDPs, and stimulus-locked PSPs evoked by repetitive stimulation to the masticatory area of the cortex, produced an average reduction in PSP amplitude of 22 and 17% in jaw closer and opener motoneurons, respectively. 4. PnC-Gi stimulation produced minimal effects on the amplitude of the antidromic digastric field potential or on the intracellularly recorded antidromic digastric action potential. Moreover, PnC-Gi stimulation had little effect on jaw opener or jaw closer motoneuron membrane resting potentials in the absence of rhythmical jaw movements (RJMs). PnC-Gi stimulation produced variable effects on conductance pulses elicited in jaw opener and closer motoneurons in the absence of RJMs. 5. These results indicate that the powerful suppression of cortically evoked MDPs in opener and closer motoneurons during PnC-Gi stimulation is most likely not a result of postsynaptic inhibition of trigeminal motoneurons. It is proposed that this suppression is a result of suppression of activity in neurons responsible for masticatory rhythm generation.

1993 ◽  
Vol 69 (2) ◽  
pp. 595-608 ◽  
Author(s):  
S. Nozaki ◽  
A. Iriki ◽  
Y. Nakamura

1. Single-unit activity was recorded from neurons in the bulbar parvocellular reticular formation (PCRF) dorsal and dorsolateral to the gigantocellular reticular nucleus near its caudal boundary, and the roles of these reticular neurons in induction of rhythmical activity of trigeminal motoneurons by repetitive stimulation of the cerebral cortex (the cortical masticatory area, CMA) were studied in the paralyzed guinea pig anesthetized with urethan or with ketamine and chlorpromazine. 2. One hundred nine PCRF neurons were activated antidromically by microstimulation in either the masseter (MA) or anterior digastric (AD) motoneuron pool in the ipsilateral trigeminal motor nucleus, and orthodromically by stimulation in the contralateral CMA. Repetitive CMA stimulation induced rhythmical burst activity in these PCRF neurons in association with the rhythmical field potential in the contralateral AD motoneuron pool induced by the same CMA stimulation. The burst was synchronous with the rhythmical AD field potential in 81 neurons, 44 and 37 of which responded antidromically to stimulation in the MA and AD motoneuron pools, respectively. The remaining 28 neurons antidromically responded to stimulation in the MA motoneuron pool, and their burst corresponded in time with the period between successive AD field potentials. 3. Spike-triggered averaging of the intracellular potentials of MA and AD motoneurons (MNs) by simultaneously recorded spontaneous spikes of the PCRF neurons, which showed rhythmical burst responses during the jaw-opening phase to repetitive CMA stimulation, revealed a monosynaptic inhibitory postsynaptic potential in MA.MNs in 12 of 34 tested pairs and a monosynaptic excitatory postsynaptic potential (EPSP) in AD.MNs in 14 of 26 tested pairs. An EPSP was also found in MA.MNs after a monosynaptic latency from triggering spikes in 11 of 37 tested PCRF neurons that showed burst activity during the jaw-closing phase. 4. We conclude that both excitatory and inhibitory premotor neurons projecting to MA.MNs as well as excitatory premotor neurons projecting to AD.MNs are located in the PCRF, and that these premotor neurons relay the output of the central rhythm generator for rhythmical jaw movements in the medial bulbar reticular formation to trigeminal motoneurons, and thus participate in induction of rhythmical activities of trigeminal motoneurons by repetitive CMA stimulation.


2001 ◽  
Vol 86 (5) ◽  
pp. 2583-2596 ◽  
Author(s):  
M.-J. Bourque ◽  
A. Kolta

Numerous evidence suggests that interneurons located in the lateral tegmentum at the level of the trigeminal motor nucleus contribute importantly to the circuitry involved in mastication. However, the question of whether these neurons participate actively to genesis of the rhythmic motor pattern or simply relay it to trigeminal motoneurons remains open. To answer this question, intracellular recordings were performed in an in vitro slice preparation comprising interneurons of the peritrigeminal area (PeriV) surrounding the trigeminal motor nucleus (NVmt) and the parvocellular reticular formation ventral and caudal to it (PCRt). Intracellular and extracellular injections of anterograde tracers were also used to examine the local connections established by these neurons. In 97% of recordings, electrical stimulation of adjacent areas evoked a postsynaptic potential (PSP). These PSPs were primarily excitatory, but inhibitory and biphasic responses were also induced. Most occurred at latencies longer than those required for monosynaptic transmission and were considered to involve oligosynaptic pathways. Both the anatomical and physiological findings show that all divisions of PeriV and PCRt are extensively interconnected. Most responses followed high-frequency stimulation (50 Hz) and showed little variability in latency indicating that the network reliably distributes inputs across all areas. In all neurons but one, excitatory postsynaptic potentials (EPSPs) or inhibitory postsynaptic potentials (IPSPs) were also elicited by stimulation of NVmt, suggesting the existence of excitatory and inhibitory interneurons within the motor nucleus. In a number of cases, these PSPs were reproduced by local injection of glutamate in lieu of the electrical stimulation. All EPSPs induced by stimulation of PeriV, PCRt, or NVmt were sensitive to ionotropic glutamate receptor antagonists 6-cyano-7-dinitroquinoxaline and d,l-2-amino-5-phosphonovaleric acid, while IPSPs were blocked by bicuculline and strychnine, antagonists of GABAA and glycine receptors. Examination of PeriV and PCRt intrinsic properties indicate that they form a fairly uniform network. Three types of neurons were identified on the basis of their firing adaptation properties. These types were not associated with particular regions. Only 5% of all neurons showed bursting behavior. Our results do not support the hypothesis that neurons of PeriV and PCRt participate actively to rhythm generation, but suggest instead that they are driven by rhythmical synaptic inputs. The organization of the network allows for rapid distribution of this rhythmic input across premotoneuron groups.


1986 ◽  
Vol 55 (4) ◽  
pp. 826-845 ◽  
Author(s):  
S. Nozaki ◽  
A. Iriki ◽  
Y. Nakamura

The role of the pyramidal tract (PT) in the induction of the rhythmical masticatory activity (RMA) of the anterior digastric motoneurons by repetitive stimulation of the cortical masticatory area (CMA) was studied in the ketamine-anesthetized guinea pig. The coronal section of the medial brain stem at the pontine level did not show any effect on the cortically induced RMA in the digastric EMG, as long as the majority of the PT fibers was spared of the section. In contrast, unilateral section of the PT at the pontine level abolished the RMA in the digastric EMG induced by repetitive stimulation of the ipsilateral CMA, while that induced by the contralateral CMA stimulation was not affected by the PT section. The threshold of repetitive PT stimulation for induction of the RMA of the digastric EMG was much higher at the levels caudal to the facial nucleus than that at more rostral levels, and no RMA was induced by the PT stimulation at the caudal bulbar levels even at the supramaximal intensities for RMA induction of the PT stimulation at more rostral levels. Single shocks applied to the PT at the caudal bulbar levels did not evoke any antidromic field potential in the CMA. Single shocks applied to the CMA evoked a negative field potential in the medial bulbar reticular formation (MBRF) mainly on the contralateral side after a monosynaptic latency, which was largest in amplitude in the region including the most dorsal portion of the nucleus reticularis paragigantocellularis and the area dorsally adjacent to it (dPGC). Stimulation of the oral portion of the nucleus reticularis gigantocellularis (GC) evoked an antidromic negative field potential in the ipsilateral dPGC. Intracellular recording from neurons in the dPGC demonstrated that neurons were located in the dPGC that responded with EPSPs after a monosynaptic latency to single shocks applied to the contralateral CMA and with antidromic spike potentials to stimulation of the oral portion of the ipsilateral GC (GCo). Single shocks applied to the dPGC evoked antidromic field potential in the area in the contralateral cerebral cortex corresponding with the CMA. Injection of horseradish peroxidase (HRP) into the dPGC on one side retrogradely labeled the pyramidal cells with HRP bilaterally in the cerebral cortical area corresponding with the CMA. The number and density of the labeled cells on the contralateral side far exceeded those on the ipsilateral side.(ABSTRACT TRUNCATED AT 400 WORDS)


Life ◽  
2020 ◽  
Vol 10 (9) ◽  
pp. 190
Author(s):  
Yoshihide Satoh ◽  
Kojun Tsuji

A previous study indicated that the swallowing reflex is inhibited during rhythmic jaw movements induced by electrical stimulation of the anterior cortical masticatory area. Rhythmic jaw movements were induced by electrical stimulation of the central amygdaloid nucleus (CeA). The swallowing central pattern generator is the nucleus of the solitary tract (NTS) and the lateral reticular formation in the medulla. Morphological studies have reported that the CeA projects to the NTS and the lateral reticular formation. It is therefore likely that the CeA is related to the control of the swallowing reflex. The purpose of this study was to determine if rhythmic jaw movements driven by CeA had inhibitory roles in the swallowing reflex induced by electrical stimulation of the superior laryngeal nerve (SLN). Rats were anesthetised with urethane. The SLN was solely stimulated for 10 s, and the swallowing reflex was recorded (SLN stimulation before SLN + CeA stimulation). Next, the SLN and the CeA were electrically stimulated at the same time for 10 s, and the swallowing reflex was recorded during rhythmic jaw movements (SLN + CeA stimulation). Finally, the SLN was solely stimulated (SLN stimulation following SLN + CeA stimulation). The number of swallows was reduced during rhythmic jaw movements. The onset latency of the first swallow was significantly longer in the SLN + CeA stimulation than in the SLN stimulation before SLN + CeA stimulation and SLN stimulation following SLN + CeA stimulation. These results support the idea that the coordination of swallowing reflex with rhythmic jaw movements could be regulated by the CeA.


1988 ◽  
Vol 59 (3) ◽  
pp. 819-832 ◽  
Author(s):  
S. H. Chandler ◽  
L. J. Goldberg

1. In the ketamine-anesthetized guinea pig, electromyographic (EMG) responses of the digastric muscle and vertical and horizontal movements of the mandible were studied when loci within the caudal pontine and rostral medullary reticular formation were stimulated during rhythmic jaw movements (RJMs) evoked by stimulation of the masticatory area of the cortex. 2. Within these regions electrical brain stem stimulation of the pontis nucleus caudalis and nucleus gigantocellularis (PnC-Gi) of the reticular formation completely blocked RJMs at stimulus intensities as low as 10 microA while suppressing the short-latency digastric EMG response that was time locked to each cortical stimulus in the train. PnC-Gi stimulation did not, however, reduce the excitability of the short-latency corticotrigeminal excitatory pathway to digastric motoneurons when tested by short pulse train stimulation at 2 Hz (3 pulses, 500 Hz, 0.3 ms) in the absence of RJMs. 3. Short trains (80 ms) of PnC-Gi stimuli delivered at various phases of the RJM cycle produced a permanent phase shift of the RJM rhythm. If the stimulus train was delivered at an early phase of the cycle (8-40%) the next cycle onset was advanced; if the train was delivered later in the cycle (60-80%) the next cycle onset was delayed. Long trains of PnC-Gi stimuli (100, 200, 300, and 400 ms) increased the time of onset of the next cycle by an amount directly proportional to the duration of the stimulus train. 4. Digastric EMG activity occurring during cortically evoked RJMs occupied nearly 50% of the cycle. If a short train of PnC-Gi stimuli was delivered between approximately 5 and 125 ms after the onset of the burst, the duration of the burst was significantly shortened. 5. These results demonstrate that the suppression of cortically evoked RJMs resulting from PnC-Gi stimulation is due to direct effects on central circuits responsible for the production of the RJM behavior and not on the motoneurons themselves. The evidence presented is consistent with our previously presented hypothesis that the neurons involved in mediating the short-latency corticotrigeminal pathway to digastric motoneurons are separate and distinct from those neurons comprising the central networks responsible for the production of the fundamental jaw oscillation during RJMs.


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