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Comparative Study
, 507 (3), 1300-16

Comparison of the Distributions of Urocortin-Containing and Cholinergic Neurons in the Perioculomotor Midbrain of the Cat and Macaque

Affiliations
Comparative Study

Comparison of the Distributions of Urocortin-Containing and Cholinergic Neurons in the Perioculomotor Midbrain of the Cat and Macaque

Paul J May et al. J Comp Neurol.

Abstract

Urocortin is a novel neurotransmitter that appears to play a role in eating and drinking behavior. Most urocortin-positive (urocortin(+)) neurons in rodents are found in the cytoarchitecturally defined Edinger-Westphal nucleus (EW). However, the EW is traditionally described as the source of the preganglionic parasympathetic outflow to the ciliary ganglion. We examined the distribution of urocortin(+) cells and motoneurons by use of immunohistochemical staining for this peptide and for choline acetyltransferase (ChAT) in macaque monkeys, in which most preganglionic motoneurons inhabit the EW, and in cats, in which most do not. In both species, lack of overt double labeling indicated that the ChAT(+) and urocortin(+) cells are separate populations. In the monkey, most nonoculomotor ChAT(+) neurons were found within the EW. In contrast, urocortin(+) cells were distributed mainly between the oculomotor nuclei and in the supraoculomotor area. In the cat, most nonoculomotor ChAT(+) cells were located in the supraoculomotor area and anteromedian nucleus. Few were present in the cat EW. Instead, this nucleus was filled with urocortin(+) cells. These results highlight the fact the term EW has come to indicate different nuclei in different species. Consequently, we have adopted the identifiers preganglionic (EW(PG)) and urocortin-containing (EW(U)) to designate the cytoarchitecturally defined EW nuclei in monkeys and cats, respectively. Furthermore, we propose a new open-ended nomenclature for the perioculomotor (pIII) cells groups that have distinctive projections and neurochemical signatures. This will allow more effective scientific discourse on the connections and function of groups such as the periculomotor urocortin (pIII(U)) and preganglionic (pIII(PG)) populations.

Figures

Figure 1
Figure 1
Low (A&B) and high (C&D) magnification views of the labeling of neurons in and around the monkey oculomotor nucleus (III) and Edinger-Westphal nucleus (EW) with antibodies to ChAT (A&C) and urocortin (B&D). Arrows in B indicate urocortin+ neurons in between the oculomotor nuclei. Arrowheads in C indicate C&S-group motoneurons. Scale bar = 500:m in A&B and 250:m in C&D.
Figure 2
Figure 2
Rostral (A) to caudal (H) charting of the distribution of urocortin+ neurons in the monkey perioculomotor region. Numerous urocortin+ cells are found within the anteromedian nucleus (AM), as well as dorsal and rostral to it (A–C). Large numbers of urocortin+ cells are also found in the supraoculomotor area (SOA) (D–H), but extend dorsal to this region onto the periventricular gray (PVG) and laterally into the interstitial nucleus of Cajal (InC) (D&E) and midbrain reticular formation (MRF) (E–G). This population does not extend past the caudal central subdivision (H). Scale bar = 1.0 mm.
Figure 3
Figure 3
Combined immunofluorescent images to simultaneously demonstrate urocortin+ (green) and ChAT+ (magenta) neurons in the monkey. Plate A shows a high magnification view of the section shown in B from the middle of the oculomotor nucleus (III), while C is from the rostral end of the oculomotor nucleus. ChAT+ cells are found within the oculomotor nucleus and in paired columns dorsal to the oculomotor nucleus, making up the Edinger-Westphal nucleus (EW). Small magenta cells along the dorsomedial edge of the oculomotor nucleus (arrowheads) represent C&S-group motoneurons. There is overlap between their distribution and that of the urocortin+ cells (A&C). The main body of urocortin+ cells has a fountain-shaped distribution in A&B, beginning medially, between the oculomotor nuclei and extending laterally in the supraoculomotor area (SOA). Note that in B, urocortin+ cells are also present in the midbrain reticular formation (MRF) and a few cells are located within the oculomotor nucleus in A. [N.B. red has been digitally altered to magenta at the request of the journal.] Scale bar = 1.0 mm for B, o.5 mm for A&C.
Figure 4
Figure 4
Charting of the distributions of ChAT+ ( Q) and urocortin+ ( M) neurons in the monkey from sequential fluorescence immunohistochemistry sections like those illustrated in figure 3. AI is a rostral to caudal series. ChAT+ neurons have a more medial, and dorsoventrally constrained distribution in the anteromedian nucleus (AM) than the urocortin+ cells, which also extend dorsal to AM (A–C). At more caudal levels (E–H), urocortin+ cells are primarily found medial to the oculomotor nucleus and dorsal to it in the supraoculomotor area (SOA). Urocortin+ neurons are also found laterally in the midbrain reticular formation (MRF). Most of the ChAT+ cells are found within the oculomotor nucleus (III) or grouped within the Edinger-Westphal nucleus (EW). The urocortin+ distribution ends caudally (I), at the level of the caudal central subdivision (CC). Scale bar = 1.0 mm.
Figure 5
Figure 5
Low (A&C) and high (B&D) magnification views of the labeling of neurons in and around the cat oculomotor nucleus (III) with antibodies to urocortin. In A&B, a section through the middle of the oculomotor nucleus, most of the urocortin positive cells are found within the midline Edinger-Westphal nucleus (EW). However, scattered cells are also present in medially, between the oculomotor nuclei, dorsally in the supraoculomotor area (SOA) and laterally in the midbrain reticular formation (MRF); and even within the oculomotor nucleus proper. In C&D, a section rostral to the oculomotor and anteromedian nuclei, the urocortin+ cells form two columns. Scale bar = 1.0 mm in A&C and 0.5 mm in B&D.
Figure 6
Figure 6
Rostral (A) to caudal (H) charting of the distribution of urocortin+ neurons in the cat perioculomotor region. Urocortin+ cells are found within and lateral to the anteromedian nucleus (AM) (C), as well as rostral to it (A&B), where they form two columns. Large numbers of urocortin+ cells are also found in the Edinger-Westphal nucleus (EW) at more caudal levels (D–H). Scattered cells are located in the supraoculomotor area (SOA) (E–H), and extend laterally into the medial longitudinal fasciculus (MLF) (D–G) and midbrain reticular formation (MRF) (D–G). Scale bar = 1.0 mm.
Figure 7
Figure 7
Fluorescence immunohistochemistry images to simultaneously demonstrate urocortin+ (green) and ChAT+ (magenta) neurons in the cat. B&D show high magnification views of the sections shown in A&C respectively. C&D are from the middle of the oculomotor nucleus (III), while A&B are from the level of AM. Caudally, most ChAT+ cells are found within the oculomotor nucleus (C&D). They are also scattered in the supraoculomotor area (SOA) dorsal to the oculomotor nucleus, and in and ventrolateral to the medial longitudinal fasciculus (MLF). The main body of Urocortin+ cells is contained within the Edinger-Westphal nucleus (EW). Note that a few urocortin+ cells are also present in the SOA and the midbrain reticular formation (arrowheads). Rostrally, the magenta ChAT+ cells are located in and lateral to AM (A&B). The green urocortin+ cells dominate the core of AM, but are also seen lateral to the nucleus. E&F show higher magnification views of the same area of another section as seen through the filters demonstrating the urocortin antibody (green) and ChAT antibody (magenta), respectively. In E, urocortin+ cells fill EW and scattered cells are present in SOA. In F, ChAT+ cells are present in the oculomotor nucleus (III), and a few highly fluorescent ChAT+ cells are located in EW (arrows). Note that some of the urocortin+ cells (E) show low levels of magenta fluorescence (F) (arrowheads). Magnification in A=C, B=D, E=F. Scale bars in C&D = 0.5 mm. [N.B. red has been digitally altered to magenta at the request of the journal.] Scale bar in E = 250 μm.
Figure 8
Figure 8
Charting of the distributions of ChAT+ ( Q) and urocortin+ ( M) neurons in the cat from double label, fluorescence sections like those illustrated in figure 7. A–I is a rostral to caudal series. As shown in C&D, ChAT+ neurons are found in the anteromedian nucleus (AM) and extend lateral to this nucleus. The urocortin+ cells lie within AM (A–C), and extend into lateral wings, which continue rostrally (A&B) as paired columns. At more caudal levels (D–J), urocortin+ cells are primarily located within the Edinger-Westphal nucleus. However, scattered cells are present ventrally, between the oculomotor nuclei, and laterally, in the supraoculomotor area (SOA). A few even lie in the midbrain reticular formation (MRF). The urocortin+ distribution ends caudal to J, at the level of the caudal central subdivision. Most of the ChAT+ cells are found within the oculomotor nucleus (III). Scattered cells are seen in the SOA, lateral and dorsal to EW, and in and below the MLF. Very few ChAT+ cells are located in the Edinger-Westphal nucleus (EW). Scale bar = 1.0.
Figure 9
Figure 9
Schematic diagram showing the distribution for monkey and cat (Above) and known projections (Below) of the perioculomotor urocortin+ population (pIIIU) of cells ( M), and the perioculomotor preganglionic motoneurons (pIIIPG) ( G).

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