Nucleus prepositus
Introduction
The nucleus prepositus hypoglossi consists of a column of neurons in the medulla that occupies the vacancy in the somatic efferent column between the hypoglossal nucleus and the abducens nucleus. Its proximity to the hypoglossal nucleus gave it its name (prepositus hypoglossi, PH), but there is abundant anatomical and physiological evidence that the nucleus is functionally better related to the abducens motor nucleus that abuts it rostrally, so it is usually referred to simply as the prepositus nucleus. The first compelling reason for including the PH in the oculomotor system was the finding that many of the cells in the PH project directly to the extraoculomotor nuclei (Graybiel and Hartwieg, 1974; Maciewicz et al., 1977), and synapse with motor neurons that innervate the extraocular muscles; particularly, the medial and lateral rectus muscles (Alley et al., 1975; Delgado-Garcia et al., 1989; Ozaki and Okamura, 1989; Labandeira-Garcia et al., 1990; Escudero et al., 1992; Graf et al., 2002). Other anatomical studies, which will be reviewed below, have shown that the PH is connected not only to the extraocular motor nuclei, but also to most of the areas of the brainstem and cerebellum that are thought to be involved in controlling eye movements. These anatomical observations, in conjunction with the findings that many neurons in the PH have spiking activity that is related to eye movements (Baker et al., 1976; Gresty and Baker, 1976; Lopez-Barneo et al., 1982; Delgado-Garcia et al., 1989; Escudero et al., 1992; McFarland and Fuchs, 1992; Cullen et al., 1993; Sylvestre et al., 2003) and that lesions of the PH produce oculomotor control deficits (Godaux et al., 1993; Mettens et al., 1994; Büttner and Grundei, 1995; Kaneko (1997), Kaneko (1999)), make the PH an important part of the brainstem circuitry involved in controlling eye movements. In this chapter, the cytological and histochemical characteristics of the PH and our present knowledge of its afferent and efferent connections will be discussed.
Section snippets
Cytoarchitecture and chemoarchitecture of the primate prepositus nucleus
The details of the cytoarchitecture of the PH vary from species to species, particularly in regard to the relationship of the nucleus to small satellite cell groups such as Roller's nucleus, the nucleus intercalatus of Staderini, the nucleus supragenualis nervi facialis, and cell groups associated with the medial longitudinal fasciculus (MLF) (Brodal (1983), Brodal & Brodal (1983)). However, the major cytological features of the PH appear to be present in all mammals. The PH is a relatively
Morphological characteristics of PH neurons
The anatomical characteristics of individual neurons in the PH vary considerably. The dendritic and axonal morphology of neurons in different regions of the cat PH has been studied with the intracellular injection of single neurons in vivo (McCrea and Baker, 1985b). In that study, three different types of soma-dendritic architecture were observed: (1) “multidendritic” cells in the PHm; (2) small cells in the PHs; and (3) medium-sized “principal” cells in the rostral, central region of the PH.
Neurotransmitters of the PH
A variety of transmitters are found in neuronal somata and terminals in the PH: Amino acid transmitters, such as GABA, glycine (GLY), and glutamate (GLU), monoamines, such as serotonin (5-hydroxy tryptophan, 5-HT), peptides, which include vasopressin and corticotrophin-releasing factor (CRF), and nitric oxide (NO). In some cases, specific neurotransmitters are associated with specific efferent pathways from the prepositus. For example, the pathway from the PH to the contralateral abducens
Afferent projections to the PH
The PH receives inputs from a wide variety of areas in the brain (Belknap and McCrea, 1988; McCrea et al., 1989; Iwasaki et al., 1999). Afferents arise from regions as far caudal as the spinal cord and as far rostral as the prefrontal cortex. The nucleus receives inputs from cells in diverse sensory nuclei such as the nucleus of the optic tract, the vestibular nuclei, the caudal spinal trigeminal nucleus, and the central cervical nucleus; from cells in the extraocular motor nuclei and the
Efferent projections of the PH
The PH has widespread projections to many areas of the cerebellum and brainstem. The targets of these projections are summarized in Fig. 10, Fig. 11.
The role of the PH in the control of gaze
The afferent and efferent projections of the prepositus nucleus clearly make it an important part of the brainstem network that is involved in controlling gaze. Figure 12 summarizes the major afferent and efferent connections of the PH with other regions of the brain that are involved in gaze control. The nucleus receives strong inputs from regions of the brainstem reticular formation that are provide premotor commands to oculomotor and cervical motoneurons that change the direction of gaze. It
References (161)
- et al.
Afferents to the vestibulo-cerebellum and the origin of the visual climbing fibers in the rabbit
Brain Res.
(1975) - et al.
Nystagmus induced by pharmacological inactivation of the brainstem ocular motor integrator in monkey
Vision Res.
(1999) - et al.
Afferent regulation of the locus coeruleus neurons: anatomy, physiology and pharmacology
Prog. Brain Res.
(1991) - et al.
Is the prepositus hypoglossi nucleus the source of another vestibulo-ocular pathway?
Brain Res.
(1975) - et al.
Neuronal activity in the prepositus hypoglossi nucleus correlated with vertical and horizontal eye movement in the cat
Brain Res.
(1976) - et al.
Organization of vestibular nucleus projections to the caudal dorsal cap of kooy in rabbits
Neuroscience
(1994) - et al.
Zonal organization of flocculo-vestibular connections in rats
Neuroscience
(2000) - et al.
Responses of cat prepositus hypoglossi neurons to horizontal angular acceleration
Neuroscience
(1977) - et al.
Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey
Brain Res.
(1983) - et al.
Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat
Brain Res. Bull.
(1990)
Possible excitatory and inhibitory feedback to the superior colliculus: a combined retrograde and immunocytochemical study in the prepositus hypoglossi nucleus of the guinea pig
Neurosci. Res.
Sight and insight—on the physiological role of nitric oxide in the visual system
Trends Neurosci.
A neurophysiological study of prepositus hypoglossi neurons projecting to oculomotor and preoculomotor nuclei in the alert cat
Neuroscience
Potent inhibitory input to locus coeruleus from the nucleus prepositus hypoglossi
Brain Res. Bull.
Brain stem projections to lobule VII of the posterior vermis in the squirrel monkey: as demonstrated by the retrograde axonal transport of tritiated horseradish peroxidase
Brain Res.
An autoradiographic analysis of the tecto-olivary projection in primates
Brain Res.
Vestibular integrators in the oculomotor system
Neurosci. Res.
Connections of the caudal cerebellar interpositus complex in a new world monkey (Cebus apella)
Brain Res. Bull.
Regulation of noradrenergic coerulean neuronal firing mediated by 5-HT2 receptors: involvement of the prepositus hypoglossal nucleus
Neuropharmacology
Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer techniques
Brain Res.
GABA and non-GABA immunostained neurones in the nucleus prepositus and the periparabigeminal area projecting to the guinea pig superior colliculus
Neurosci. Lett.
Anatomical interconnections of the pedunculopontine tegmental nucleus and the nucleus prepositus hypoglossi in the cat
Brain Res.
Differential projections to the superior collicular layers from the perihypoglossal nuclei in the cat
Brain Res.
Distribution and cerebellar projections of cholinergic and corticotropin-releasing factor-containing neurons in the caudal vestibular nuclear complex and adjacent brainstem structures
Neuroscience
Axonal branches and terminations in the cat abducens nucleus of secondary vestibular neurons in the horizontal canal system
Neurosci. Lett.
Neural connections of the pontine reticular formation, which connects reciprocally with the nucleus prepositus hypoglossi in the rat
Neuroscience
Cholinergic innervation and receptors in the cerebellum
Prog. Brain Res.
Pretectofugal fibers from the nucleus of the optic tract in monkeys
Brain Res.
Afferent projections to the thalamus from the perihypoglossal nuclei
Brain Res.
Efferent connections from the external cuneate nucleus to the medulla oblongata in the gerbil
Brain Res.
Responses of prepositus hypoglossi neurons to optokinetic and vestibular stimulations in the rat
Brain Res.
The frontal eye field projects to the nucleus prepositus hypoglossi in the monkey
Neurosci. Lett.
Prearcuate cortex in the Cebus monkey has cortical and subcortical connections like the macaque frontal eye field and projects to fastigial-recipient oculomotor-related brainstem nuclei
Brain Res. Bull.
The origin of brainstem afferents of the paramedian pontine reticular formation in the cat
Brain Res.
The dorsal tegmental nucleus: an axoplasmic transport study
Brain Res.
Afferent projections to the rat locus coeruleus demonstrated by retrograde and anterograde tracing with cholera-toxin B subunit and Phaseolus vulgaris leucoagglutinin
Neuroscience
Vestibular and medullary brain stem afferents to the abducens nucleus in the cat
Brain Res.
Origin of descending afferents to the rostral part of dorsal cap of inferior olive which transfers contralateral optic activities to the flocculus. A horseradish peroxidase study
Brain Res.
Sources of subcortical GABAergic projections to the superior colliculus in the cat
J. Comp. Neurol.
Effects of nucleus prepositus hypoglossi lesions on visual climbing fiber activity in the rabbit flocculus
J. Neurophysiol.
Cholinergic innervation of the cerebellum of rat, rabbit, cat, and monkey as revealed by choline acetyltransferase activity and immunohistochemistry
J. Comp. Neurol.
Cholinergic projection to the dorsal cap of the inferior olive of the rat, rabbit, and monkey
J. Comp. Neurol.
Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey
J. Comp. Neurol.
A slow excitatory postsynaptic potential mediated by 5-HT2 receptors in nucleus prepositus hypoglossi
J. Neurosci.
Experimental demonstration of cerebellar connexions from the perihypoglossal nuclei (nucleus intercalatus, nucleus praepositus hypoglossal and nucleus of roller) in the cat
J. Anat.
The perihypglossal nuclei in the macaque monkey and the chimpanzee
J. Comp. Neurol.
Observations on the projection from the perihypoglossal nuclei onto the cerebellum in the macaque monkey
Arch. Ital. Biol.
Gaze-evoked nystagmus and smooth pursuit deficits: their relationship studied in 52 patients
J. Neurol.
Pathways from cell groups of the paramedian tracts to the floccular region
N. Y. Acad. Sci.
Efferent pathways of the nucleus of the optic tract in monkey and their role in eye movements
J. Comp. Neurol.
Cited by (83)
Gaze holding abnormalities as an inaugural event in multiple sclerosis - A case report
2020, Clinical Neurology and NeurosurgeryCorollary Discharge Signals in the Cerebellum
2019, Biological Psychiatry: Cognitive Neuroscience and NeuroimagingCitation Excerpt :A number of major candidates convey motor information tuned to multiple effectors and derive from sources across the brain, including cerebral cortex, via relay in the basilar pontine nuclei (13–16). Other major brainstem sources of motor information are the lateral reticular nucleus (17–21), conveying information on cervical and limb musculature; the nucleus hypoglossis prepositus and nucleus reticularis tegmenti pontis, both encoding parameters of oculomotor control (22–24); the magnocellular red nucleus (25–27), involved in limb and facial movement; the cerebellar nuclei (12,28–30), mediating control of diverse effectors; and the ventral/rostral spinocerebellar tract (31–36), reporting activity of spinal motor neurons. Each of these putative sources of motor information could contribute to Purkinje neuron signaling, most clearly in analogous motor domains as the motor CD.
Modeling gaze position-dependent opsoclonus
2019, Progress in Brain ResearchCitation Excerpt :The NPH projects directly to the three motor nuclei (IIIn, IVn, and VIn), providing the necessary tonic activity to hold the eye steady against the elastic restoring forces in the orbit. The NPH neurons use a variety of both excitatory and inhibitory neurotransmitters, including GABA, glycine (Gly), and glutamate (Glu) (McCrea and Horn, 2006). Spike-triggered averaging and autoradiography revealed that NPH neurons which project to the ipsilateral abducens nucleus gave rise to excitatory postsynaptic currents via Glu, whereas NPH neurons that project to the contralateral abducens nucleus evoked inhibitory postsynaptic currents via Gly (Escudero et al., 1992; Spencer et al., 1989).
Distinct response properties of rat prepositus hypoglossi nucleus neurons classified on the basis of firing patterns
2017, Neuroscience ResearchCitation Excerpt :In the PHN, transient burst signals that are proportional to eye velocity are transformed into sustained signals that are proportional to eye position for gaze holding; therefore, the PHN is regarded as an oculomotor neural integrator. The function of the PHN is accomplished by heterogeneous neuronal populations that display distinct electrophysiological, morphological, and chemical profiles (Delgado-Garcia et al., 2006; McCrea and Horn, 2006). Preceding in vitro studies have indicated that PHN neurons can be classified into two discrete types based on their spike shapes, a type that exhibits monophasic afterhyperpolarization (AHP) (type A) and a type that exhibits biphasic AHP (type B), although an intermediate type (type C) and an additional type that exhibits monophasic AHP and clusters of action potentials intermingled with subthreshold membrane oscillations (type D) have also been found (Idoux et al., 2006, 2008; see also, Serafin et al., 1991; Beraneck et al., 2003).