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Synaptic Transmission and Modulation in Submandibular Ganglia: Aspects of a Current-Clamp Study

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Synaptic Transmission and Modulation in Submandibular Ganglia: Aspects of a Current-Clamp Study Bull. Tokyo dent. Coll., Vol. 41, No. 4, pp.149ϳ167, November, 2000 149 Review Article SYNAPTIC TRANSMISSION AND MODULATION IN SUBMANDIBULAR GANGLIA: ASPECTS OF A CURRENT-CLAMP STUDY TAKASHI SUZUKI Department of Physiology, Tokyo Dental College, 1-2-2 Masago, Mihama-ku, Chiba 261-8502, Japan Received 8 September, 2000/Accepted for Publication 10 October, 2000 Abstract The superior salivatory nucleus in the medulla oblongata is the parasympathetic center of the sublingual and the submandibular (SM) glands. The preganglionic axons originating in this parasympathetic center connect postganglionic neurons in the sub- mandibular ganglia. In spite of an earlier electrophysiological study by Langley in 189013), intracellular electrical studies on SM ganglion neurons had not been done because of the technical difficulties in impaling neurons. It was in only 1972 that the authors begun the intracellular electrical studies of SM ganglia in adult rats and hamsters. In this review, we describe the membrane properties of neurons, spontaneous activities of neurons, types of connection between pre- and post-ganglionic neurons, synaptic potentials including fast EPSP, slow IPSP, slow EPSP and slow hyperpolarizing synaptic potential, characteris- tics of the reflex spike discharges and modulation of synaptic transmission by biogenic substances in SM ganglion neurons. Transfer of information within the ganglia is more complex than simple nicotinic-cholinergic relay, and seems to be specialized for compat- ibility with the salivary glands. These data reflect the specific characteristics of synaptic transmission in the SM ganglia. Key words: Membrane properties—Spontaneous membrane activities— Postsynaptic potentials—Biogenic substances—Reflex spike discharges INTRODUCTION humans, it causes release of small amounts of saliva with rich organic constituents from The salivary glands5,13) are supplied with major salivary glands. both sympathetic and parasympathetic nerves. Since the end of the 1970s, studies using Both autonomic nerves are secretory nerves. the method of tracing the retrograde axonal Stimulation of the parasympathetic nerve transport of horseradish peroxidase have con- causes copious secretion of watery saliva with firmed the results of the early histological a relatively low content of organic material, studies utilizing the neuronal degeneration while the effect of stimulation of the sympa- method16). The superior and the inferior thetic nerve varies from species to species. In salivatory nuclei consist of parvocellular neu- 149 150 T. SUZUKI rons sparsely scattered in the lateral reticular formation of the medulla at the level of the facial nucleus. The superior subdivision is situated rostral to the inferior subdivision, but there is no anatomical boundary. The rostral part of the parasympathetic center, the supe- rior salivatory nucleus, connects with the sub- mandibular and the sublingual glands. It is also known that some of the pregangli- onic fibers diverge to more than one postgan- glionic neuron14). The postganglionic para- sympathetic nerve fibers are known to con- verge at the glandular cell level8,15). The importance of nerves for salivary secre- tion was revealed in 1850 by Ludwig8), who found that electrical stimulation of the lin- gual nerve in dogs caused secretion of saliva from the submandibular gland. 13) Professor Langley is a noted pioneer in Fig. 1 Compound action potentials of the secretory nerve bundles electrophysiological study of submandibular Stimulus strength: A: 2V, B: 5.8V, C: 7.8V and D: 26 V ganglia. The so-called submandibular (SM) Duration: 0.1msec. Conducting distance: 7.5mm (see ganglia with the smaller cluster in the chordo- ref. 19) lingual triangle and the small ganglion near the hilus of the SM gland are scattered on the course of nerve fibers to the sublingual (SL) count the number of the unmyelinated and the SM glands. His study concluded that fibers19). The myelinated and the unmyeli- secretory fibers of the chorda tympani in dogs nated fibers of less than 3␮m were presumed are paralysed by nicotine in the applied gan- to be the parasympathetic fibers involved glion more readily than the peripheral vasodi- in secretion and vasodilation. Some of the lator nerve. Therefore, Langley’s findings unmyelinated fibers are probably visceral suggested that the SM ganglion included sensory fibers. both secretory and vasodilatory neurons. The major and minor diameters of 604 In 1972, intracellular electrophysiological cells in the same preparation which permitted studies on the SM ganglion cells were con- measurement were 13.2–42.9␮m and 9.9– ducted in the small ganglion near the SM 33.0␮m. The peaks of histograms were at gland of adult rats19). 23.1–26.4␮m and 16.5–19.8␮m, respectively19). 2. Electrophysiological investigation of the LIGHTMICROSCOPIC OBSERVATIONS secretory nerve The compound action potentials of the 1. The size of preganglionic fibers and secretory nerve bundles were recorded imme- ganglion neurons diately before a small ganglion in the hilus of The approximately 10 secretory nerve bun- the SM gland (shown in Fig. 1) and the con- dles near the origin which branched out from duction velocities were estimated from the the lingual nerve contained 156 fibers. Thirty- latency of each action potential and the con- eight fibers were less than 1.5␮m; 100 fibers, ducting distance. The fastest conduction 1.5–3␮m; 11 fibers, 3–4.5␮m; 3 fibers, 4.5– velocities, 6–12 m/sec, were considered to be 6␮m; 2 fibers, 6–7.5␮m; and 2 fibers, 7.5– those of B fibers or the somatosensory nerve 9␮m in diameter. However, it was difficult to fibers. The conduction velocities of 3.0 m/sec CURRENT-CLAMP STUDY IN SUBMANDIBULAR GANGLIA 151 (in B), 1–1.6 m/sec (in D), 0.32–0.9 m/sec and its mean duration is 250 mV at the level of (in C), 0.21–0.3 m/sec (in D), and 0.17– the mean Em. The values of active membrane 0.21 m/sec (in C) were presumed to be those properties in vitro are similar to those of in of preganglionic B and C fibers. In the ham- vivo20). SM ganglion neurons usually discharge ster SM ganglion, the conduction velocity of a single spike only at the onset of depolarizing some preganglionic fibers was slightly faster current pulses. In bladder ganglion, three than 1m/sec. The mean velocity of the fibers types of neurons can be distinguished on the S.D.) m/sec. The post gangli- basis of the nature of the spike discharge) 0.17עwas 0.24 onic fibers had a conduction velocity of evoked by intrasomatic injection of depolariz- .(m/sec20). ing current pulses9 0.11ע0.24 Hyperpolarizing after-potentials are associ- ated with the spikes in all of autonomic gan- MEMBRANE PROPERTIES OF glion neurons. The after-hyperpolarizing po- SUBMANDIBULAR GANGLION NEURONS tentials summate and are prolonged when spikes are evoked repetitively; their durations Most intracellular electrophysiological stud- are less than 1sec. The ionic mechanisms for ies had been done on ganglia in vitro because the postspike hyperpolarization is an increase of the technical difficulties of impaling the in calcium-activated gK that is triggered by an neurons with microelectrodes in situ. The influx of calcium during the rising phase of work of Suzuki and Kusano20) was exceptional the action potential20). The functional signifi- in that they compared the electrophysiologi- cance of this mechanism in all of the neurons cal properties of hamster SM ganglion neu- is to restrict the frequency of spike discharge. rons in vitro and in vivo. The results indicate Electrophysiological findings in parasym- that the properties of the neurons do not pathetic ganglia indicate that the neurophysi- change in the in vitro situation. ology is more complex than simple nicotinic- cholinergic relay and divergence of pregan- 1. The passive properties glionic information to autonomic effector sys- The resting membrane potentials of SM tems. The transfer function of these ganglia mV is, no doubt, specialized for compatibility with 51מ ganglion neurons in rats are mean mV in vitro19). The mean the effector system they control, and it is 77מ–40מ and range resting Ems of hamster SM ganglion neurons evident that this specialization is associated mV, with heterogenous synaptic interactions and 8.0ע53מ S.D.) mV and) 7.2ע53מ are -mV electrophysiological properties that are sug 70מ–40מ respectively, and the range is in the in vitro and in vivo conditions20). Mean gestive of integrative and modulatory func- membrane input resistances in hamster SM tions within ganglia41). M⍀ and 17.2עganglion neurons are 42.4 M⍀ in the in vitro and on in vivo 26.2ע40.4 conditions, respectively. The range of the SPONTANEOUS ACTIVITY IN membrane time constant is 5–10 msec both in SUBMANDIBULAR GANGLION NEURONS vitro and in vivo20). Spontaneously occurring hyperpolarizing 2. The active properties potentials occur in submandibular ganglion The mean amplitude of the antidromic neurons20) and in the cardiac ganglion neu- S.D.) mV in hamster SM rons of Necturus10). These potentials reflect) 12.4עspike is 71.5 ganglion neurons in the in vivo condition. periodic increases in calcium-dependent gK The mean amplitude of the directly evoked and are similar to the spontaneous IPSPs that mV. The critical level of occur in myenteric neurons40). However, they 9.8עspike is 69.0 mV. The mean ampli- are not synaptic potentials in SM ganglion 5.4עspike firing is 14.4 tude of spike after-hyperpolarization is 13 mV, neurons. Spontaneous transient hyperpolar- 152 T. S UZUKI Fig. 2 Spontaneous hyperpolarizing potentials and effects of caffeine on membrane potential A. In this neuron, the spontaneous HPs occurred with various amplitudes and durations at irregular intervals in normal Krebs solution. B. Application of 2.5mM caffeine induced the HPs at a regular interval. Amplitudes of HPs increased, and spikes fired at the ends of HPs as an off-response.
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