Abstract
The motor outflow for the pupillary light reflex originates in the preganglionic motoneuron subdivision of the Edinger–Westphal nucleus (EWpg), which also mediates lens accommodation. Despite their importance for vision, the morphology, ultrastructure and luminance-related inputs of these motoneurons have not been fully described in primates. In macaque monkeys, we labeled EWpg motoneurons from ciliary ganglion and orbital injections. Both approaches indicated preganglionic motoneurons occupy an EWpg organized as a unitary, ipsilateral cell column. When tracers were placed in the pretectal complex, labeled terminals targeted the ipsilateral EWpg and reached contralateral EWpg by crossing both above and below the cerebral aqueduct. They also terminated in the lateral visceral column, a ventrolateral periaqueductal gray region containing neurons projecting to the contralateral pretectum. Combining olivary pretectal and ciliary ganglion injections to determine whether a direct pupillary light reflex projection is present revealed a labeled motoneuron subpopulation that displayed close associations with labeled pretectal terminal boutons. Ultrastructurally, this subpopulation received synaptic contacts from labeled pretectal terminals that contained numerous clear spherical vesicles, suggesting excitation, and scattered dense-core vesicles, suggesting peptidergic co-transmitters. A variety of axon terminal classes, some of which may serve the near response, synapsed on preganglionic motoneurons. Quantitative analysis indicated that pupillary motoneurons receive more inhibitory inputs than lens motoneurons. To summarize, the pupillary light reflex circuit utilizes a monosynaptic, excitatory, bilateral pretectal projection to a distinct subpopulation of EWpg motoneurons. Furthermore, the interconnections between the lateral visceral column and olivary pretectal nucleus may provide pretectal cells with bilateral retinal fields.
Highlights
The preganglionic motoneurons whose axons travel with the third cranial nerve are located in the preganglionic subdivision of the Edinger–Westphal nucleus (EWpg) (Kozicz et al 2011; May et al 2008a), a cell group associated with the oculomotor nucleus (III) that was first described by Edinger (1885) and Westphal (1887) over a century ago
These cells contain melanopsin and have been characterized as intrinsically photoreceptive retinal ganglion cells, they receive photoreceptor input (Güler et al 2008; Hannibal et al 2014). They send their axons to the olivary pretectal nucleus (OPt), with the temporal retina projecting to the ipsilateral OPt and the nasal retina providing input via the chiasm to the contralateral OPt
They formed a tight cluster as the EWpg, which was located in the supraoculomotor area (SOA) dorsal to III at its rostral end (Fig. 2b, g)
Summary
The preganglionic motoneurons whose axons travel with the third cranial nerve are located in the preganglionic subdivision of the Edinger–Westphal nucleus (EWpg) (Kozicz et al 2011; May et al 2008a), a cell group associated with the oculomotor nucleus (III) that was first described by Edinger (1885) and Westphal (1887) over a century ago. There are two populations within EWpg: one controls lens accommodation by activating the ciliary muscle and the other controls pupillary constriction by activating the pupillary sphincter muscle (Gamlin et al 1984, 1994; Hultborn et al 1973; McDougal and Gamlin 2015; May et al 2019b) Two behaviors use this parasympathetic outflow: the near response and the pupillary light reflex. The cells in OPt are classified as broad-field luminance detectors (Gamlin et al 1995) This nucleus is believed to subsequently project to the EWpg. This nucleus is believed to subsequently project to the EWpg The action of this pathway is inhibited when there is increased activation of sympathetic pathways to the pupillary dilator muscle under low illumination conditions and due to changes in the state of the animal. The pupils dilate in response to increased states of attention, arousal and/or cognitive load (Kahneman and Beatty 1966; Beatty 1982; Gabay et al 2011; Szabadi 2013; Joshi et al 2016), as well as with saccades (Wang and Munoz 2015)
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