On the two subdivisions and intrinsic synaptic connexions in the submandibular ganglion of the rat

Abstract

Parasympathetic neurones in the submandibular ganglion of the rat innervate the submandibular and sublingual salivary glands. Neurones which innervate the submandibular gland (s.m. neurones) are usually located along the salivary ducts which drain both glands. Neurones which innervate the sublingual gland (s.l. neurones) are located in the thin sheet of tissue which lies between the salivary ducts and the lingual nerve. The existence and characteristics of intrinsic synaptic connexions were studied electrophysiologically in these two divisions of the submandibular ganglion. Three days or more after denervating the ganglion two types of excitatory intrinsic synaptic potentials--chemical and electrical--were recorded in ganglion cells. Chemical synaptic responses were reversibly blocked by nicotinic antagonists such as hexamethonium (10 microM) and D-tubocurarine (100 microM). Intrinsic chemical synapses were common among s.m. neurones (present in 72% of neurones) but only 12% of s.l. neurones were coupled with chemical synapses. Electrical coupling was found among 31% of s.m. neurones but was not observed between s.l. neurones. Electrotonic coupling in s.m. neurones in denervated and intact ganglia was directly demonstrated by impaling adjacent neurones with separate micro-electrodes. The average coupling ratio for current pulses injected into one cell and recorded in the adjacent cell was 0.06. During the first 30 days after birth, the number of synaptic inputs from preganglionic (chorda tympani) axons was markedly reduced in both s.m. and s.l. neurones, whereas the incidence of electrical synaptic connexions remained unchanged. The effect of long-term denervation (up to 4 months) on intrinsic synapses was examined. The membrane properties of the parasympathetic neurones and the intrinsic synaptic connexions were maintained without marked changes. It is concluded that the submandibular ganglion in the rat consists of two distinct populations of parasympathetic neurones. The two classes of neurones differ in (1) their location within the ganglion, (2) their target organs and (3) the incidence of intrinsic synapses. Possible mechanisms for the development, maintenance and function of these intrinsic synapses are discussed.