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

Abstract

The vertebrate ciliary ganglion (CG) is a relay station in the parasympathetic pathway activating the iris sphincter and ciliary muscle to mediate pupillary constriction and lens accommodation, respectively. While the postganglionic motoneurons in the CG are cholinergic, as are their inputs, there is evidence from avian studies that GABA may also be involved. Here, we used light and electron microscopic methods to examine the GABAergic innervation of the CG in Macaca fascicularis monkeys. Immunohistochemistry for the gamma aminobutyric acid synthesizing enzyme glutamic acid decarboxylase (GAD) and choline acetyltransferase (ChAT) revealed that all CG neurons are contacted by ChAT-positive terminals. A subpopulation of 17.5% of CG neurons was associated with terminal boutons expressing GAD-immunoreactivity in addition. Double-labeling for GAD and synaptophysin confirmed that these were synaptic terminals. Electron microscopic analysis in conjunction with GABA-immunogold staining showed that (1) GAD-positive terminals mainly target dendrites and spines in the perisomatic neuropil of CG neurons; (2) GABA is restricted to a specific terminal type, which displays intermediate features lying between classically excitatory and inhibitory endings; and (3) if a CG neuron is contacted by GABA-positive terminals, virtually all perisomatic terminals supplying it show GABA immunoreactivity. The source of this GABAergic input and whether GABA contributes to a specific CG function remains to be investigated. Nevertheless, our data indicate that the innervation of the ciliary ganglion is more complex than previously thought, and that GABA may play a neuromodulatory role in the control of lens or pupil function.

An Anatomic Characterization of the Midbrain Near Response Neurons in the Macaque Monkey

“… 51 In this regard, the organization of the ciliary motoneurons is noteworthy. At the ultrastructural level, their somata are surrounded by a perisomatic neuropil that contains numerous synaptic contacts, 52 – 54 but they also emit a few dendrites. Both these characteristics were evident in the virus-labeled postganglionic motoneurons ( Figs.…”

Neural basis of location-specific pupil luminance modulation

“…The SCi connects to a downstream parasympathetic structure, the Edinger-Westphal (EW) nucleus, mainly via projections through the central mesencephalic reticular formation (40,41). The EW nucleus projects to the ciliary ganglion with excitatory and inhibitory connections (42) and can therefore produce constriction and dilation. Additionally, the EW nucleus receives projections from topographically organized the pretectal olivary nucleus (PON), which receives luminance signals directly from the retina (43)(44)(45).…”

Maturation of Temporal Saccade Prediction from Childhood to Adulthood: Predictive Saccades, Reduced Pupil Size, and Blink Synchronization

“…Indeed, Figure 5A,B shows that this relaxation effect was replicated using pupil size, which was smaller for predictive versus reactive saccade trials. NE has been shown to have a neuromodulatory effect on the parasympathetic oculomotor complex via LC inputs to SC (Edwards et al, 1979) and SC's corresponding projection through Edinger-Westphal nucleus (Harting et al, 1980) to the ciliary ganglion, which can be both excitatory and inhibitory (Barnerssoi et al, 2017), providing a potential pathway for a decreased pupil size and thereby arousal for predictive saccades. This pupil effect is complementary to a previous fMRI study by Lee et al (2016) that demonstrated strong activation of the default mode network (DMN), a neural network that increases its metabolic activity during relaxation, when adults made predictive saccades in the metronome task.…”