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Inhibition of Trigeminal Respiratory Activity by Suckling
H. Koizumi*,
K. Nomura,
K. Ishihama,
T. Yamanishi,
A. Enomoto and
M. Kogo
The First Department of Oral and Maxillofacial Surgery, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka 565-0871 Japan
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Figure 1. Trigeminal respiratory activities in a brainstem preparation in vitro. (A) The in vitro brainstem preparation includes the networks for respiration and fictive suckling. The schematic sagittal view of the brainstem and spinal cord shows the trigeminal motor nucleus (V) in the dorsal pons, hypoglossal nucleus (XII) in the dorsal medulla, and pre-Bötzinger Complex (pBC) in the ventral medulla. VII, facial motor nucleus; NA, nucleus ambiguus; SC, superior colliculus; IC, inferior colliculus. (B) The schematic horizontal view of the brainstem preparation shows the trigeminal motor nucleus (V) in the dorso-medial pons medial to the trigeminal sensory nucleus (5SP) and pre-Bötzinger complex (pBC) in the ventro-lateral medulla, and ventral to the nucleus ambiguus (NA). Motoneuron population discharges were recorded from the trigeminal motor nerve (Vn) and hypoglossal nerve (XIIn). Whole-cell patch-clamp and extracellular single-cell recordings of trigeminal motoneurons and pre-Bötzinger complex neurons were also performed. (C) The trigeminal motor nerve and respiratory trigeminal motoneuron show spontaneous inspiratory activities synchronized with inspiratory discharges in the hypoglossal nerve and pre-Bötzinger complex neuron. Whole-cell current-clamp recordings from a respiratory trigeminal motoneuron are also shown (VM: holding at resting membrane potential, -64 mV). (D) The traces show the data segment (rectangular area in C) on an expanded time scale. Inspiratory population discharges of the trigeminal motor nerve and hypoglossal nerve similarly consist of a rapidly peaking, slowly decreasing envelope. The spikes of inspiratory single-neuron discharges of the trigeminal motoneuron and pre-Bötzinger complex neuron show spike-frequency adaptation.
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Figure 2. Trigeminal respiratory activity during fictive suckling. (A) Bath application of N-methyl-D,L-aspartate (NMA: 20 µmol/L) and bicuculline methiodide (BIC: 10 µmol/L) induce fictive suckling in the trigeminal motor nerve, which consists of tonic (> 20 Hz) spikes and rhythmic (6.2 ± 0.4 Hz) burst discharges. The tonic spikes are observed as an upward increase in the integrated signals from 2 min after bath application. The rhythmic burst discharges are observed from 5 min after bath application. The amplitude and duration of the inspiratory discharges in the pre-Bötzinger complex neuron and hypoglossal nerve, as well as the respiratory frequency, are decreased during fictive suckling. The time delay in the responses is due to the diffusion time of the drugs to the targeted region. The raw electrical signals were integrated with a 20-msecond time constant to obtain the sum of the signals. (B) The traces show the data segment (rectangular area in A) on an expanded time scale. The trigeminal nerve exhibits rhythmic (around 5–6 Hz) burst discharges. However, the respiration-trigeminal motoneurons are inhibited and show only tonic (around 12–13 Hz) spikes that are not synchronized with fictive suckling activities in the trigeminal nerve, or with inspiratory activities in the pre-Bötzinger complex neuron and hypoglossal nerve.
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Figure 3. Membrane potential trajectory of trigeminal motoneurons (TMNs) during fictive suckling. (A) The respiration TMN shows spontaneous inspiratory bursts at a resting membrane potential of -64 mV under whole-cell current-clamp conditions (action potential spikes are truncated). Bath application of N-methyl-D,L-aspartate (NMA: 20 µmol/L) and bicuculline methiodide (BIC: 10 µmol/L) causes hyperpolarization (6.4 mV) of the membrane potential and then cessation of the action potentials. The respiratory frequency gradually decreases and the respiratory rhythm then stops. (B) The suckling TMN shows no respiratory activities at a resting membrane potential of -62 mV. Bath application of NMA and BIC causes depolarization (6.8 mV) of the membrane potential, and induces fast rhythmic firing related to fictive suckling (action potential spikes are truncated).
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Figure 4. Respiratory activities in trigeminal motoneurons (TMNs) during local micro-injection of NMA and BIC. (A) Local micro-injection of N-methyl-D,L-aspartate (NMA: 200 µmol/L) and bicuculline methiodide (BIC: 100 µmol/L) into the trigeminal motor nucleus augments the trigeminal nerve discharges, which show rhythmic bursts related to fictive suckling. The inspiratory activities in the respiration TMN are significantly inhibited during micro-injection. The inspiratory activities in the hypoglossal nerve are less affected, which indicates a lack of significant change in either the respiratory rhythm or the amplitude and duration of the discharges. (B) Local micro-injection of NMA and BIC into the pre-Bötzinger complex augments the inspiratory activities in the respiration TMN, trigeminal nerve, and hypoglossal nerve. The respiratory frequency is also significantly increased during micro-injection. The time delay in the responses is due to the diffusion time of the drugs.
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Journal of Dental Research, Vol. 86, No. 11,
1073-1077 (2007)
DOI: 10.1177/154405910708601110
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