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.
Highlights
ANTISERA Choline acetyltransferase Cholinergic motoneurons were detected with a polyclonal choline acetyltransferase (ChAT) antibody raised in goat (AB144P, Chemicon) against the whole enzyme isolated from human placenta, which is identical to the brain enzyme (Bruce et al, 1985; Table 1)
At the level of the inferior colliculus (IC), the trochlear nucleus (nIV) is clearly outlined as a round nucleus embedded in the fibers of the medial longitudinal fasciclus (MLF) (Figures 1A,B; corresponds to plate 32 in Olszewski and Baxter’s work, 2nd edition, 1982, and 3rd edition by Büttner-Ennever and Horn, 2014)
OCULOMOTOR SUBGROUPS INVOLVED IN UPGAZE Motoneurons of superior rectus and inferior oblique muscles As in monkey, only selected subgroups within oculomotor nucleus (nIII) receive a strong input from CR-positive afferents (Zeeh et al, 2013); in human these include the central caudal nucleus (CCN), the CEN group, and nucleus of Perlia (NP)
Summary
Eye movements are essential for vision, because they direct the fovea to a visual target, and stabilize gaze during locomotion to Abbreviations: nIII, oculomotor nucleus; nIV, trochlear nucleus; nVI, abducens nucleus; CCN, central caudal nucleus; CEN, central group; ChAT, choline acetyltransferase; CMRF, central mesencephalic reticular formation; CR, calretinin; DL, dorsolateral group; DM, dorsomedial group; DR, dorsal raphe nucleus; EAP, extravidin-peroxidase; EW, Edinger–Westphal nucleus; EWcp, centrally projecting Edinger–Westphal nucleus; EWpg, Edinger–Westphal nucleus containing preganglionic neurons; GABA, gamma-aminobutyric acid; GAD, glutamate decarboxylase; GlyR, glycine receptor; IC, inferior colliculus; INC, interstitial nucleus of Cajal; IO, inferior oblique muscle; IPN, interpeduncular nucleus; IR, inferior rectus muscle; LP, levator palpebrae muscle; LR, lateral rectus muscle; MGB, medial geniculate body; MIF, multiply-innervated non-twitch muscle fibers; ML, medial lemniscus; MLF, medial longitudinal fasciclus; MR, medial rectus muscle; NIII, oculomotor nerve; NP, nucleus of Perlia; NP-NF, non-phosphorylated neurofilaments; PAG, periaqueductal gray; PB, phosphate buffer; PN, pontine nuclei; RIMLF, rostral interstitial nucleus of the medial longitudinal fasciculus; RN, red nucleus; SC, superior colliculus; SCP, superior cerebellar peduncle; SE of mean, standard error of the mean; SIF, singly-innervated twitch muscle fibers; SNc, substantia nigra pars compacta; SNr, substantia nigra pars reticulata; SO, superior oblique muscle; SOA, supraoculomotor area; SR, superior rectus muscle; UCN, urocortin; VEN, ventral group.compensate for head and body movements (Leigh and Zee, 2006; Horn and Leigh, 2011). The motor and premotor pathways for several eye movement types, e.g., saccades and the vestibulo-ocular reflex, are well studied in monkey, and they form the basis for assessing the homologous brain structures in humans, for example, in clinical cases of eye movement disorders (Horn and Leigh, 2011; Kennard, 2011). In order to analyze the clinical-anatomical studies involving horizontal and vertical, up- or downward eye movements, the knowledge of the localization of the motoneurons of individual extraocular muscles in human is essential. In non-human primates, the oculomotor nucleus (nIII) and trochlear nucleus (nIV) lie in the mesencephalic tegmentum at the ventral border of the periaquaeductal gray beneath the Frontiers in Neuroanatomy www.frontiersin.org
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