George Székely

The efferent system of cranial nerve nuclei : a comparative neuromorphological study

A number of inconsistencies and controversies are inherent in the classification of cranial nerve nuclei based on the concepts of the various head-theories. The assumption of head segmentation, which is common to these theories, serves as the basis for designating the dorsomedial nuclei as the somatomotor column, although they innervate striated muscles of a viscus and a specific sense organ. The ventrolateral nuclei are called the specific visceromotor column; they innervate striated muscles in the branchiogenous area, but many of these muscles insert on skeletal elements. A series of comparative neuromorphological studies investigating the dendritic arborization pattern and axonal trajectory in the frog, lizard, and rat suggests a much more delicate classification in which nine morphologically and functionally different neuron groups can be discerned: 1. The hypoglossal nucleus appears coincidentally with the muscular tongue in amphibia. The spindle-shaped perikaryon, the bipolar dendritic arborization, and the straight ventral trajectory of the axon are characteristic morphological features in all three animal species investigated. 2. The oculomotor, trochlear, and abducens nuclei present a remarkably conservative topography and organization in all vertebrates with a moving eye. With their oval-shaped or polygonal perikarya and radiating dendritic arborization, these neurons distinctly differ from hypoglossal neurons. The ipsilateral axons follow a straight ventral course, the contralateral axons form a dorsal loop before crossing the midline, and the crossing is not consequence of neuron migration to the contralateral side. 3. The accessory abducens nucleus is present in tetrapods except apes and human. The elongated perikaryon and the dorsoventral dendritic orientation distinctly distinguish these neurons from other cranial motoneurons, the nucleus is found in the lateral part of the reticular formation. The neurons differentiate in situ, they do not migrate from the main abducens nucleus. 4. In the submammalian trigeminal and facial nuclei, two basic neuron types can be distinguished on the basis of their morphology. The first type is larger and accumulates in the rostral part of the trigeminal nucleus. This type innervates the jaw closer muscles. The second type is found in the caudal part of the trigeminal nucleus and in the facial nucleus. These neurons innervate the muscular floor of the mouth and the facial contingent supplies the jaw opener muscle. A very characteristic feature in the axonal trajectory is an initial medial course and a hairpin turn, or dorsal loop, at the lateral aspect of the medial longitudinal fasciculus. In addition to the two types of neurons, there is a third type in the frog trigeminal nucleus. This innervates an orbital muscle.(ABSTRACT TRUNCATED AT 400 WORDS)

The Extent of the Dendritic Tree and the Number of Synapses in the Frog Motoneuron.

Frog motoneurons were intracellularly labelled with cobaltic lysine in the brachial and the lumbar segments of the spinal cord, and the material was processed for light microscopy in serial sections. With the aid of the neuron reconstruction system NEUTRACE, the dendritic tree of neurons was reconstructed and the length and surface area of dendrites measured. The surface of somata was determined with the prolate – oblate average ellipsoid calculation. Corrections were made for shrinkage and for optical distortion. The mean surface area of somata was 6710 μm2; lumbar motoneurons were slightly larger than brachial motoneurons. The mean length of the combined dendritic tree of brachial neurons was 29 408 μm and that of lumbar neurons 46 806 μm. The mean surface area was 127 335 μm2 in brachial neurons, and 168 063 μm2 in lumbar neurons. The soma – dendrite surface area ratio was 3 – 5% in most cases. Dendrites with a diameter of ≤ 1.0 μm constituted ∼ 75% of the combined dendritic length in most of the neurons. Unlike in the cat, there was no correlation between the size of stem dendrites and the extent of daughter branches. From the synaptic density estimated in earlier electron microscope investigations of frog motoneuron dendrites (Antal et al., J. Neurocytol., 15, 303–310, 1986; 21, 34–49, 1992), and from the present data, the number of synapses on the dendritic tree was calculated. The calculations indicated 26 949 synapses on the smallest and 61 519 synapses on the largest neuron if the synaptic density was multiplied by the length of the dendritic tree. If the synaptic density was multiplied by the surface area of the dendritic tree the calculation yielded 23 337 synapses for the smallest and 60 682 synapses for the largest neuron. More than 60% of the combined surface area of dendrites was >600 μm from the soma. This suggests that about two‐thirds of the synapses impinged upon distant dendrites >600 μm from the soma. The efficacy of synapses at these large distances is investigated on model neurons in the accompanying paper (Wolf et al., Eur. J. Neurosci., 4, 1013–1021, 1992).

Distribution of hyaluronan in the central nervous system of the frog

The qualitative and quantitative distribution pattern of hyaluronan (HA), a component of the extracellular matrix (ECM), was studied in the frog central nervous system by using a highly specific HA probe and digital image analysis. HA reaction was observed in both the white and the gray matter, showing a very intense staining around the perikarya and dendrites in the perineuronal net (PN). In the telencephalon, strong reaction was found in different parts of the olfactory system, in the pallium, and in the amygdala. In the diencephalon, intensive staining was found in the nucleus of Bellonci, the dorsal habenula, the lateral and central thalamic nuclei, and the subependymal zone of the third ventricle. In the mesencephalon, layers of optic tectum displayed different intensities, with the strongest reaction in layers B, D, F, 3, and 5. Other structures of the mesencephalon showed regional differences. The PN was especially intensively stained around the perikarya of the toral nuclei, the oculomotor and trochlear nuclei, and the basal optic nucleus. In the rhombencephalon, the granular layer of cerebellum, the vestibulocochlear nuclei, the superior olive, the spinal tract of the trigeminal nerve, and parts of the reticular formation showed the most intense reaction in the PN. In the spinal cord, considerable HA staining was found in the white matter and around the perikarya of motoneurons. The present study is the first description of the HA‐positive areas of frog brain and spinal cord demonstrating the heterogeneity of HA distribution in the frog central nervous system. J. Comp. Neurol. 496:819–831, 2006.

Organization of the ambiguus nucleus in the frog (Rana esculenta)

The common root of the glossopharyngeal, vagal, and accessory nerves and the individual branches of the vagus complex were labeled with cobalt, and the organization of the ambiguus nucleus was studied. The cell column labeled through the common root extended from the upper part of the medulla to the rostral spinal cord over a distance of about 3,500 μm. The labeling of individual branches revealed four subdivisions. 1) The pharyngomotor subdivision occupied the rostral 800 μm of the cell column. It gave origin to the innervation of the pharyngeal muscles. 2) The visceromotor subdivision, consisting of small and medium‐sized cells labeled by way of the visceral branches of the vagus, was found in the rostrocaudal extent of the medulla. 3) The laryngomotor subdivision extended in the obex region over a distance of more than 1,000 μm. It supplied the sphincter muscles of the larynx. The dilator laryngeal muscle was represented in the rostral part of the visceromotor subdivision. 4) The accessory nerve subdivision was located in the lower medulla and the rostral spinal cord.

Simulation of the Effect of Synapses: the Significance of the Dendritic Diameter in Impulse Propagation

The effectiveness of synapses at various sites of the dendritic tree was studied using a segmental cable model with a program developed by Hines (Int. J. Biomed. Comput., 24, 55–68, 1989). The model rendered possible a high‐fidelity simulation of the dendritic geometry of a frog motoneuron described in the accompanying paper (Birinyi et al., Eur. J. Neurosci., 1003–1012, 1992). The model was used in the passive membrane mode and the synaptic activity was simulated with current injections into large and small diameter dendrites at proximal and distal locations. Synaptic efficiency was defined by the charge transfer ratio expressed as the proportion of the injected current which appeared at the soma. The charge transfer ratio was determined with uniform and non‐uniform distribution of specific membrane resistance over the soma–dendrite surface while the diameter of selected dendrite segments changed. The best charge transfer ratio was found with the largest dendrite membrane resistance, and the maximum efficiency of synaptic activity appeared at the original size of the dendrite segment stimulated. The amount of current that flowed in the proximal and distal directions from the segment stimulated depended on the diameter of that segment. The increase in diameter of proximal dendrites increased synaptic efficiency on distal dendrites, whereas the reverse caused a decline in synaptic efficiency on proximal dendrites. In addition to the diameter of dendrites, the arborization pattern also played a significant role in this mechanism. It is concluded that the cellulipetal increase in dendrite diameter greatly increases synaptic efficiency.

Quantitative morphological analysis of the motoneurons innervating muscles involved in tongue movements of the frog Rana esculenta.

We give an account of an effort to make quantitative morphological distinctions between motoneurons of the frog innervating functionally different groups of muscles involved in the movements of the tongue. The protractor, retractor, and inner muscles of the tongue were considered on the basis of their major action during the prey‐catching behavior of the frog. Motoneurons were selectively labeled with cobalt lysin through the nerves of the individual muscles, and dendritic trees of successfully labeled neurons were reconstructed. Each motoneuron was characterized by 15 quantitative morphological parameters describing the size of the soma and dendritic tree and 12 orientation variables related to the shape and orientation of the dendritic field. The variables were subjected to multivariate discriminant analysis to find correlations between form and function of these motoneurons. According to the morphological parameters, the motoneurons were classified into three functionally different groups weighted by the shape of the perikaryon, mean diameter of stem dendrites, and mean length of dendritic segments. The most important orientation variables in the separation of three groups were the ellipses describing the shape of dendritic arborization in the horizontal, frontal, and sagittal planes of the brainstem. These findings indicate that characteristic geometry of the dendritic tree may have a preference for one array of fibers over another. J. Comp. Neurol. 470:409–421, 2004.

Trigeminal motoneurons with disparate dendritic geometry innervate different muscle groups in the frog

Cobalt labelling revealed two, morphologically different types of neurons in the trigeminal motor nucleus innervating masticatory muscles and the levator bulbi muscle, respectively. As far as their neuronal morphology is concerned, levator bulbi motoneurons differed from all other motoneurons of the brainstem. They could not be found in lizards and rats; and the levator bulbi muscle was also absent in these animals. This motoneuron group is compared with the accessory abducens nucleus which innervates the retractor bulbi muscles, and is present only in animals which possess this muscle group.

An approach to the complexity of the brain.

The establishment of ordered neuronal connections is supposed to take place under the control of specific cell adhesion molecules (CAM) which guide neuroblasts and axons to their appropriate destination. The extreme complexity of the nervous system does not provide a favorable medium for the development of deterministic connections. Simons [112] theorems offer a mean to approach the high level of complexity of the nervous system. The basic tenet is that complex systems are hierarchically organized and decomposable. Such systems can arise by selective trial and error mechanisms. Subsystems in complex systems only interact in an aggregate manner, and no significant information is lost if the detail of aggregate interactions is ignored. A number of nervous activities, which qualify for these requirements, are shown. The following sources of selection are considered: internal and external feedbacks, previous experience, plasticity in simple structures, and the characteristic geometry of dendrites. The role played by CAMs and other membrane-associated molecules is discussed in the sense that they are either inductor molecules that turn on different homeobox genes, or downstream products of genes, or both. These molecules control cellular and tissular differentiation in the developing brain creating sources of selection required for the trial and error process in the organization of the nervous tissue.

Deglutition and Phonation: The Ambiguus Nucleus

The dorsal motor nucleus of the vagus is traditionally included in the efferent nuclear complex of the glossopharyngeal and vagal nerves. Since this nucleus innervates viscera and also possesses a facial component, it will be discussed in the brain stem vegetative system. Here we focus on the central innervation of the branchiogenic striated musculature in the region of the glossopharyngeal and vagal nerves.

Control of Jaw Movements and Facial Expression: The Trigeminal and Facial Nuclei

The description of these two nuclei together is motivated by their joint activity in the control of the primary mandibular joint. The secondary (mammalian) mandibular joint is controlled only by the trigeminal nerve. A part of the structural transformation which results in the secondary jaw joint is the appearance of muscles for mastication and facial expression. Concurrent with the transformation of the periphery, profound structural changes occur in the center and these changes are rather equivocally treated in the literature. We think that the joint discussion of these two motor nuclei from a functional point of view promotes the understanding of species differences in these nuclei. In this effort, we give a short overview of the evolution of the primary and secondary mandibular joints and their muscles before describing the corresponding motor centers.