Central pupillary light reflex circuits in the cat: I. The olivary pretectal nucleus

Abstract

The central pathways subserving the feline pupillary light reflex were examined by defining retinal input to the olivary pretectal nucleus (OPt), the midbrain projections of this nucleus, and the premotor neurons within it. Unilateral intravitreal wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP) injections revealed differences in the pattern of retinal OPt termination on the two sides. Injections of WGA-HRP into OPt labeled terminals bilaterally in the anteromedian nucleus, and to a lesser extent in the supraoculomotor area, centrally projecting Edinger-Westphal nucleus, and nucleus of the posterior commissure. Labeled terminals, as well as retrogradely labeled multipolar cells, were present in the contralateral OPt, indicating a commissural pathway. Injections of WGA-HRP into the anteromedian nucleus labeled fusiform premotor neurons within the OPt, as well as multipolar cells in the nucleus of the posterior commissure. Connections between retinal terminals and the pretectal premotor neurons were characterized by combining vitreous chamber and anteromedian nucleus injections of WGA-HRP in the same animal. Fusiform-shaped, retrogradely labeled cells fell within the anterogradely labeled retinal terminal field in the OPt. Ultrastructural analysis revealed labeled retinal terminals containing clear spherical vesicles. They contacted labeled pretectal premotor neurons via asymmetric synaptic densities. These results provide an anatomical substrate for the pupillary light reflex in the cat. Pretectal premotor neurons receive direct retinal input via synapses suggestive of an excitatory drive, and project directly to nuclei containing preganglionic motoneurons. These projections are concentrated in the anteromedian nucleus, indicating its involvement in the pupillary light reflex.

Keywords: Edinger-Westphal; luminance; oculomotor; parasympathetic; pretectum.

Figure 1

Brightfield (A) and darkfield (B-D) photomicrographs demonstrating the olivary pretectal nucleus (OPt) and the pattern of labeling in this nucleus following a WGA-HRP injection of the left vitreous chamber. Anterogradely labeled retinal terminal fields were heavier on the right (contralateral) side (B&D) than the left (ipsilateral) side (B&C). A Nissl-stained section (A) at about the same level as B shows the cytoarchitecture of OPt and adjacent structures for reference. Scale in A=B, C=D.

Figure 2

Distribution of labeled cells and terminals in the midbrain following an injection of WGA-HRP into the left olivary pretectal nucleus (OPt). In this and all subsequent chartings, sections are arranged from rostral (A) to caudal (F), retrogradely labeled cells are indicated by dots, anterogradely labeled terminals are indicated by fine stipple and fine lines represent labeled axon fibers. Injection site and tracer spread area are indicated by black and shaded areas, respectively (A-D). The injection site was centered in OPt and spread slightly into adjacent parts of the medial pretectal nucleus (MPt), the nucleus of the optic tract (NOT), and the anterior pretectal nucleus (APt). Terminals are present bilaterally in the anteromedian nucleus (AM) (A-D), and to a lesser extent in the centrally projecting Edinger-Westphal nucleus (EWcp), supraoculomotor area (SOA) and between the oculomotor nuclei (III). Terminals are also present in the ipsilateral periaqueductal gray (PAG)(A-E), both nuclei of Darkschewitsch (ND)(A-F), and contralaterally in OPt (B-D), MPt (B-D), the nucleus of the posterior commissure (NPC)(B-D) and the interstitial nucleus of Cajal (INC)(B&C). Labeled cells are present in contralateral OPt, MPt, APt and NPC (B-D).

Figure 3

Darkfield micrographs of WGA-HRP labeled terminals in the anteromedian nucleus (AM) (A, B) and cells and terminals in the contralateral pretectum (C, D) following an olivary pretectal nucleus injection like that shown in figure 2. Examples of labeled terminals are indicated by arrows (B) and labeled cells are indicated by arrowheads (D). Scale in A=C, B=D.

Figure 4

Distribution of labeled cells and terminals in midbrain following a WGA-HRP injection into the anteromedian nucleus (AM). Note labeled cells (dots) in and ventral to the olivary pretectal nucleus (OPt) (E, F). Labeled cells were also present in the nucleus of the posterior commissure (NPC)(A-I).

Figure 5

Darkfield photomicrographs showing retrogradely labeled cells in the olivary pretectal nucleus (OPt)(A, B), and in the nucleus of the posterior commissure (NPC)(C, D) following a WGA-HRP injection into the anteromedian nucleus (AM) like that shown in figure 4. Examples of the labeled cells are indicated by arrows (B,D&F). The region selected for the high magnification views (B&D) is indicated in the low magnification views (A&C). Scale in A=D.

Figure 6

Distribution of labeling in the pretectum following injections of WGA-HRP into left vitreous chamber and into the anteromedian nucleus (AM)(A&B). Anterogradely labeled retinal terminals (stipple) are present in the olivary pretectal nucleus (OPt)(A-F) and in the nucleus of the optic tract (NOT)(C-F). Retrogradely labeled cells (dots) from the AM injection are present in OPt (B-E). Their distribution overlaps with that of the retinal terminals. Labeled cells, which are outside of the retinal terminal field, are also present in the medial pretectal nucleus (MPt)(A-F), in the area ventral to OPt (B-E), in the nucleus of the posterior commissure (NPC) (A-F), and in the posterior pretectal nucleus (PPt)(F).

Figure 7

Darkfield photomicrographs showing labeling in the olivary pretectal nucleus (OPt) following combined injections of WGA-HRP into the left vitreous chamber and into the anteromedian nucleus. Lower magnification (A&B) and higher magnification (C&D) views from regions indicated by boxes reveal distribution of label in the left (A&C) and right (B&D) OPt. Premotor neuons retrogradely labeled from the AM nucleus overlaped with anterogradely labeled retinal terminals. Examples of these labeled cells are indicated by arrows. Scale in A=B. C=D.

Figure 8

Electron micrographs of WGA-HRP labeled retinal terminals and WGA-HRP labeled premotor neurons in the olivary pretectal nucleus. Anterogradely labeled retinal terminals (At*) can be distinguished from unlabeled terminal profiles (At) by the presence of electron dense, flocculent reaction product. The labeled terminals contained clear spherical vesicles, but generally lacked dense-cored vesicles (arrows). The labeled terminals synaptically contacted (arrowheads) either retrogradely labeled somata (Soma*)(A&B) or dendrites (Den*)(C&D), which also contained the reaction product. Scale in C=D.

Figure 9

Schematic diagram summarizing the results of this study. Retinal terminals contact fusiform premotor cells in the olivary pretectal nucleus, with a contralateral predominance. Both ipsilateral and contralateral projections to the anteromedian nucleus are present, with a slight contralateral predominance. The anteromedian nucleus is the source of the preganglionic output that underlies the direct and consensual pupillary response. The olivary nucleus also contains a population of multipolar commissural neurons. In addition to targeting the anteromedian nucleus, the olivary pretectal nucleus also projects to the contralateral nucleus of the posterior commissure, which may provide an indirect pathway to preganglionic motoneurons in the anteromedian nucleus.