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Delineation of motoneuron subgroups supplying individual eye muscles in the human oculomotor nucleus.

Che Ngwa E, Zeeh C, Messoudi A, Büttner-Ennever JA, Horn AK - Front Neuroanat (2014)

Bottom Line: The oculomotor nucleus (nIII) contains the motoneurons of medial, inferior, and superior recti (MR, IR, and SR), inferior oblique (IO), and levator palpebrae (LP) muscles.We studied the transmitter inputs to human nIII and the trochlear nucleus (nIV), which innervates the superior oblique muscle (SO), to outline individual motoneuron subgroups.This study provides a map of the individual subgroups of motoneurons in human nIII for the first time, and suggests that NP may contain upgaze motoneurons.

View Article: PubMed Central - PubMed

Affiliation: Oculomotor Group, Institute of Anatomy and Cell Biology, Department I, Ludwig-Maximilians-University of Munich Munich, Germany.

ABSTRACT
The oculomotor nucleus (nIII) contains the motoneurons of medial, inferior, and superior recti (MR, IR, and SR), inferior oblique (IO), and levator palpebrae (LP) muscles. The delineation of motoneuron subgroups for each muscle is well-known in monkey, but not in human. We studied the transmitter inputs to human nIII and the trochlear nucleus (nIV), which innervates the superior oblique muscle (SO), to outline individual motoneuron subgroups. Parallel series of sections from human brainstems were immunostained for different markers: choline acetyltransferase combined with glutamate decarboxylase (GAD), calretinin (CR) or glycine receptor. The cytoarchitecture was visualized with cresyl violet, Gallyas staining and expression of non-phosphorylated neurofilaments. Apart from nIV, seven subgroups were delineated in nIII: the central caudal nucleus (CCN), a dorsolateral (DL), dorsomedial (DM), central (CEN), and ventral (VEN) group, the nucleus of Perlia (NP) and the non-preganglionic centrally projecting Edinger-Westphal nucleus (EWcp). DL, VEN, NP, and EWcp were characterized by a strong supply of GAD-positive terminals, in contrast to DM, CEN, and nIV. CR-positive terminals and fibers were confined to CCN, CEN, and NP. Based on location and histochemistry of the motoneuron subgroups in monkey, CEN is considered as the SR and IO motoneurons, DL and VEN as the B- and A-group of MR motoneurons, respectively, and DM as IR motoneurons. A good correlation between monkey and man is seen for the CR input, which labels only motoneurons of eye muscles participating in upgaze (SR, IO, and LP). The CCN contained LP motoneurons, and nIV those of SO. This study provides a map of the individual subgroups of motoneurons in human nIII for the first time, and suggests that NP may contain upgaze motoneurons. Surprisingly, a strong GABAergic input to human MR motoneurons was discovered, which is not seen in monkey and may indicate a functional oculomotor specialization.

No MeSH data available.


Proposed map of the motoneurons for individual extraocular muscles in human shown at four representative planes from caudal to rostral. The right half shows corresponding sections in Nissl staining to demonstrate the cytoarchitecture. The central caudal nucleus at most caudal planes contains the motoneurons of the levator palpebrae muscle (LP) (A). The medial rectus muscles (MR) is represented in two groups, the dorsolateral B- and the ventral A-group (A,B). The central group represents the motoneurons of the inferior oblique (IO) and superior rectus (SR) muscle (A,B). The nucleus of Perlia (NP) is separated from the main nucleus, but may contain SR motoneurons as well (B,C). The dorsomedial group corresponds to the inferior rectus motoneurons (IR) (A–C). The centrally projecting neurons of the Edinger–Westphal nucleus (EWcp) appear as a single lateral group on caudal levels dorsal to nIII (A), adjoined by a medial group further rostrally (B), which both merge to a single dorsal group (C). Another ventral extension of the EWcp appears on rostral levels (D). Note that the preganglionic neurons in the EWpg do not form a compact nucleus (B). Scale bar: (A–D) 500 μm.
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Figure 8: Proposed map of the motoneurons for individual extraocular muscles in human shown at four representative planes from caudal to rostral. The right half shows corresponding sections in Nissl staining to demonstrate the cytoarchitecture. The central caudal nucleus at most caudal planes contains the motoneurons of the levator palpebrae muscle (LP) (A). The medial rectus muscles (MR) is represented in two groups, the dorsolateral B- and the ventral A-group (A,B). The central group represents the motoneurons of the inferior oblique (IO) and superior rectus (SR) muscle (A,B). The nucleus of Perlia (NP) is separated from the main nucleus, but may contain SR motoneurons as well (B,C). The dorsomedial group corresponds to the inferior rectus motoneurons (IR) (A–C). The centrally projecting neurons of the Edinger–Westphal nucleus (EWcp) appear as a single lateral group on caudal levels dorsal to nIII (A), adjoined by a medial group further rostrally (B), which both merge to a single dorsal group (C). Another ventral extension of the EWcp appears on rostral levels (D). Note that the preganglionic neurons in the EWpg do not form a compact nucleus (B). Scale bar: (A–D) 500 μm.

Mentions: As in monkey, only selected subgroups within nIII receive a strong input from CR-positive afferents (Zeeh et al., 2013); in human these include the CCN, the CEN group, and NP. Combined tract-tracing and CR-immunostaining experiments in monkey have shown that the CR-positive input was confined to motoneurons participating in upgaze, e.g., SR, IO, and LP in the CCN (Fuchs et al., 1992; Zeeh et al., 2013). Furthermore, tracer injections into the IO or SR muscles in monkey revealed that these two subgroups occupy a similar portion in the central part of the caudal nIII, except for the fact that the SR motoneurons are located contralaterally and tend to lie more medially to the IO motoneurons, which project to the ipsilateral eye muscle. The dendrites of retrogradely labeled IO and SR motoneurons are intimately intermingled and are not confined to any individual cytoarchitectural borders (Spencer and Porter, 1981; Zeeh et al., 2013). Based on the similar anatomical and histochemical features of the CEN group including the selective CR input, the CEN subgroup in the human nIII is considered as the location of SR and IO motoneurons (Figure 8).


Delineation of motoneuron subgroups supplying individual eye muscles in the human oculomotor nucleus.

Che Ngwa E, Zeeh C, Messoudi A, Büttner-Ennever JA, Horn AK - Front Neuroanat (2014)

Proposed map of the motoneurons for individual extraocular muscles in human shown at four representative planes from caudal to rostral. The right half shows corresponding sections in Nissl staining to demonstrate the cytoarchitecture. The central caudal nucleus at most caudal planes contains the motoneurons of the levator palpebrae muscle (LP) (A). The medial rectus muscles (MR) is represented in two groups, the dorsolateral B- and the ventral A-group (A,B). The central group represents the motoneurons of the inferior oblique (IO) and superior rectus (SR) muscle (A,B). The nucleus of Perlia (NP) is separated from the main nucleus, but may contain SR motoneurons as well (B,C). The dorsomedial group corresponds to the inferior rectus motoneurons (IR) (A–C). The centrally projecting neurons of the Edinger–Westphal nucleus (EWcp) appear as a single lateral group on caudal levels dorsal to nIII (A), adjoined by a medial group further rostrally (B), which both merge to a single dorsal group (C). Another ventral extension of the EWcp appears on rostral levels (D). Note that the preganglionic neurons in the EWpg do not form a compact nucleus (B). Scale bar: (A–D) 500 μm.
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Figure 8: Proposed map of the motoneurons for individual extraocular muscles in human shown at four representative planes from caudal to rostral. The right half shows corresponding sections in Nissl staining to demonstrate the cytoarchitecture. The central caudal nucleus at most caudal planes contains the motoneurons of the levator palpebrae muscle (LP) (A). The medial rectus muscles (MR) is represented in two groups, the dorsolateral B- and the ventral A-group (A,B). The central group represents the motoneurons of the inferior oblique (IO) and superior rectus (SR) muscle (A,B). The nucleus of Perlia (NP) is separated from the main nucleus, but may contain SR motoneurons as well (B,C). The dorsomedial group corresponds to the inferior rectus motoneurons (IR) (A–C). The centrally projecting neurons of the Edinger–Westphal nucleus (EWcp) appear as a single lateral group on caudal levels dorsal to nIII (A), adjoined by a medial group further rostrally (B), which both merge to a single dorsal group (C). Another ventral extension of the EWcp appears on rostral levels (D). Note that the preganglionic neurons in the EWpg do not form a compact nucleus (B). Scale bar: (A–D) 500 μm.
Mentions: As in monkey, only selected subgroups within nIII receive a strong input from CR-positive afferents (Zeeh et al., 2013); in human these include the CCN, the CEN group, and NP. Combined tract-tracing and CR-immunostaining experiments in monkey have shown that the CR-positive input was confined to motoneurons participating in upgaze, e.g., SR, IO, and LP in the CCN (Fuchs et al., 1992; Zeeh et al., 2013). Furthermore, tracer injections into the IO or SR muscles in monkey revealed that these two subgroups occupy a similar portion in the central part of the caudal nIII, except for the fact that the SR motoneurons are located contralaterally and tend to lie more medially to the IO motoneurons, which project to the ipsilateral eye muscle. The dendrites of retrogradely labeled IO and SR motoneurons are intimately intermingled and are not confined to any individual cytoarchitectural borders (Spencer and Porter, 1981; Zeeh et al., 2013). Based on the similar anatomical and histochemical features of the CEN group including the selective CR input, the CEN subgroup in the human nIII is considered as the location of SR and IO motoneurons (Figure 8).

Bottom Line: The oculomotor nucleus (nIII) contains the motoneurons of medial, inferior, and superior recti (MR, IR, and SR), inferior oblique (IO), and levator palpebrae (LP) muscles.We studied the transmitter inputs to human nIII and the trochlear nucleus (nIV), which innervates the superior oblique muscle (SO), to outline individual motoneuron subgroups.This study provides a map of the individual subgroups of motoneurons in human nIII for the first time, and suggests that NP may contain upgaze motoneurons.

View Article: PubMed Central - PubMed

Affiliation: Oculomotor Group, Institute of Anatomy and Cell Biology, Department I, Ludwig-Maximilians-University of Munich Munich, Germany.

ABSTRACT
The oculomotor nucleus (nIII) contains the motoneurons of medial, inferior, and superior recti (MR, IR, and SR), inferior oblique (IO), and levator palpebrae (LP) muscles. The delineation of motoneuron subgroups for each muscle is well-known in monkey, but not in human. We studied the transmitter inputs to human nIII and the trochlear nucleus (nIV), which innervates the superior oblique muscle (SO), to outline individual motoneuron subgroups. Parallel series of sections from human brainstems were immunostained for different markers: choline acetyltransferase combined with glutamate decarboxylase (GAD), calretinin (CR) or glycine receptor. The cytoarchitecture was visualized with cresyl violet, Gallyas staining and expression of non-phosphorylated neurofilaments. Apart from nIV, seven subgroups were delineated in nIII: the central caudal nucleus (CCN), a dorsolateral (DL), dorsomedial (DM), central (CEN), and ventral (VEN) group, the nucleus of Perlia (NP) and the non-preganglionic centrally projecting Edinger-Westphal nucleus (EWcp). DL, VEN, NP, and EWcp were characterized by a strong supply of GAD-positive terminals, in contrast to DM, CEN, and nIV. CR-positive terminals and fibers were confined to CCN, CEN, and NP. Based on location and histochemistry of the motoneuron subgroups in monkey, CEN is considered as the SR and IO motoneurons, DL and VEN as the B- and A-group of MR motoneurons, respectively, and DM as IR motoneurons. A good correlation between monkey and man is seen for the CR input, which labels only motoneurons of eye muscles participating in upgaze (SR, IO, and LP). The CCN contained LP motoneurons, and nIV those of SO. This study provides a map of the individual subgroups of motoneurons in human nIII for the first time, and suggests that NP may contain upgaze motoneurons. Surprisingly, a strong GABAergic input to human MR motoneurons was discovered, which is not seen in monkey and may indicate a functional oculomotor specialization.

No MeSH data available.