GABAergic innervation of the ciliary ganglion in macaque monkeys – A light and electron microscopic study

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The ciliary ganglion (CG) of vertebrates is a small cluster of nerve cells, located behind the ocular bulb, between the optic nerve and the lateral rectus muscle. It consists of parasympathetic, postganglionic, cholinergic neurons (Martin & Pilar, 1963a; Landmesser & Pilar, 1972) that are driven by preganglionic neurons in the Edinger‐Westphal nucleus (EWpg) and project to the ciliary and sphincter pupillae muscles to mediate lens accommodation and pupillary constriction, respectively (Burde, 1967; Hultborn, Mori, & Tsukahara, 1978; Martin & Pilar, 1963b; Marwitt, Pilar, & Weakley, 1971; Neuhuber & Schrödl, 2011; Reiner, Karten, Gamlin, & Erichsen, 1983). Physiological studies demonstrated that firing rates, recorded from macaque monkey EW units, are correlated with the activity of the ciliary and sphincter pupillae muscles (Gamlin, Zhang, Clendaniel, & Mays, 1994; McDougal & Gamlin, 2015). In birds, an additional subpopulation of CG neurons innervates the choroid (Neuhuber & Schrödl, 2011; Reiner et al., 1983). Traditionally, it is believed that the CG receives its main preganglionic input from parasympathetic, cholinergic motoneurons of the EWpg, which corresponds to the cytoarchitecturally defined EW in monkey and birds (Gamlin & Reiner, 1991; Gamlin, Reiner, Erichsen, Karten, & Cohen, 1984; Horn, Eberhorn, Härtig, Ardeleanu, Messoudi, & Büttner‐Ennever, 2008; Kozicz et al., 2011; May, Reiner, & Ryabinin, 2008a; May, Sun, & Erichsen, 2008b; Narayanan & Narayanan, 1976; Vasconcelos et al., 2003).
Immunohistochemical studies carried out in birds and mammals indicate that, besides the classical preganglionic cholinergic input to CG neurons, a peptidergic input is present (for review, see McDougal & Gamlin, 2015; Neuhuber & Schrödl, 2011). This includes the neuropeptides substance P, enkephalin (Erichsen, Karten, Eldred, & Brecha, 1982a; Erichsen, Reiner, & Karten, 1982b; Kirch, Neuhuber, & Tamm, 1995; Zhang, Tan, & Wong, 1994b), neuropeptide Y (Grimes, Koeberlein, Tigges, & Stone, 1998), and calcitonin gene‐related peptide (CGRP) coexpressed with substance P (Kirch et al., 1995). Ultrastructural analysis using electron microscopic methods (EM) also demonstrated heterogeneity in preganglionic axon terminal properties (May & Warren, 1993). All these observations indicate that transmission through the CG may, in fact, be more complex than previously thought.
In addition to peptides, there is evidence for GABA in the CG. Studies in chick provide strong evidence that the CG neurons are controlled by gamma amino butyric acid (GABA), which is known as a fast‐acting transmitter. This is indicated by the expression of GABA‐A receptors (McEachern, Margiotta, & Berg, 1985), GABA‐immunoreactive terminals on ciliary neurons in the chicken embryonic CG, and the complete block of transmission through the chick CG after application of GABA in in‐vitro and in‐vivo studies (Liu, Neff, & Berg, 2006; Tuttle, Vaca, & Pilar, 1983). To the best of our knowledge, similar studies in mammals have not been carried out. To explore whether a GABAergic innervation of the CG is also present in mammals, we investigated the CG of macaque monkeys (Macaca fascicularis) using immunohistochemical methods in combination with light and electron microscopic techniques.
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