[Post-embryonic differentiation of a cutaneous electro-receptor]. / Sur la différenciation postembryonnaire d'un électrorécepteur cutané.

In order to decrease the rate of postembryonic development of electroreceptor organs, excisions of epidermis and deafferentations were carried out in the gymnotid fish Eigenmannia virescens. Twenty-five days later, the epidermis showed electroreceptor organs without innervation. Some of these at the beginning of their development consisted of masses of identical cells, whereas others showed presumed sensory cells whose cytoplasm contained rudimentary synaptic structures. The epidermis also showed differentiated tuberous organs with a low number of sensory cells. In all these organs, radioactive thymidine was fixed in the nuclei of the platform accessory cells. Thirty-five-40 days after surgery, tuberous organs were identical to the functional organs, and thymidine was detected in the nuclei of the cavity accessory cells. These results show that the gymnotid electroreceptor organs can develop before any nervous contact occurs, and suggest that they might originate from epidermal cells.

Oculomotor system of the weakly electric fish Gnathonemus petersii.

The peripheral and central aspects of the extraocular system were studied in the weakly electric fish Gnathonemus petersii. All six extraocular muscles show a similar composition of large and small fibers grouped characteristically in the proximal and distal regions respectively. The exit of the three extraocular nerves from the brain is similar to that in other vertebrates. However, the intracephalic and intracranial course of the trochlear nerve is unusual, partly because of the extraordinary hypertrophy of the cerebellum. The three nerves course rostrally on the ventral brain surface; the trochlear nerve penetrates the orbital cavity separately from the two other nerves. The fiber-diameter spectrum of each extraocular nerve is bimodal; unmyelinated fibers were not observed in any of the nerves. The location of the extraocular motor nuclei was established by retrograde axonal transport of HRP or cobaltic-lysine complex. The oculomotor nucleus is situated ventral to the posterior pole of the magnocellular mesencephalic nucleus and the trochlear nucleus is found caudal and dorsal to this. The abducens nucleus is situated at the level of the octavolateral efferent nucleus and consists of a single group of cells on each side of the ventral tegmentum. The oculomotor nucleus of G. petersii shows a somatotopic organization. The superior rectus muscle receives a contralateral innervation whereas the inferior rectus and oblique muscles and the internal rectus muscles receive an ipsilateral innervation. The superior oblique muscle is innervated by contralateral trochlear motoneurons and the external rectus by ipsilateral abducens motoneurons. The majority of extraocular motoneurons have piriform perikarya and long beaded dendrites that extend laterally in the oculomotor and abducens nuclei and rostrally in the trochlear nucleus. The terminal dendritic portions of trochlear motoneurons widely overlap with oculomotor dendrites and perikarya. In all three nuclei the axon originates opposite to the main dendrite. Collaterals of the hairpin-bend abducens axons could be identified in a few cases. The oculomotor system of G. petersii appears basically similar to that of other teleosts; the differences observed concern mainly the structure of the abducens nucleus, the intracranial and intracephalic course of the trochlear nerve, and the relatively small number of axons in each nerve.

High substance P-like immunoreactivity (SPLI) in the olfactory and electrosensory cells of gymnotid fish.

Substance P has been proposed as a candidate neurotransmitter or neuromodulator in the nociceptive system. Using a light microscopial immunohistochemical peroxidase-anti-peroxidase technique we have detected high substance P-like immunoreactivity (SPLI) in several types of sensory organs of 4 species of gymnotiform teleost fish: olfactory epithelium, vestibular, lateral line and electrosensory organs. The olfactory nerve and its endings within the olfactory bulb and the telencephalon were also strongly labelled. At these sites no SPLI was revealed in other teleosts (Carassius auratus, Gnathonemus petersii). The findings suggest that substance P may be involved in neurotransmission or neuromodulation in these specific sensory systems of these species.

Morphology and physiology of the brainstem nuclei controlling the electric organ discharge in mormyrid fish.

The motoneurons to the mormyrid electric organ are driven from the medullary relay nucleus. This nucleus is in turn innervated by an adjacent cell group, nucleus C. The goals of this study were to characterize the morphology and physiology of neurons in these two nuclei, and to test the hypothesis that nucleus C is the command nucleus responsible for initiating the electric organ discharge. Medullary relay neurons and nucleus C neurons were recorded intracellularly and labeled with horseradish peroxidase. Medullary relay neurons have a richly branched dendritic arborization, confined mainly to the nucleus itself, and somatosomatic, dendrosomatic, and presynaptic dendro-axonal gap junctions have been observed. Medullary relay neuron axons descend to the spinal cord without branching. Nucleus C dendrites extend far into the ventral reticular formation. Axons of nucleus C neurons have one branch that ramifies densely within the medullary relay nucleus, forming large club endings on the medullary relay neuron soma. Two additional branches project bilaterally toward the bulbar command associated nuclei. Both medullary relay neurons and nucleus C neurons fire a double action potential that precedes each electric organ discharge. Activity in nucleus C precedes that in the medullary relay nucleus by 100-300 microseconds. Postsynaptic activity is recorded in nucleus C neurons but not in medullary relay neurons. Hyperpolarization of a single nucleus C neuron can lower the frequency of the electric organ discharge. Both morphological and physiological data indicate that nucleus C is an integrating center where the electric organ command is initiated.

The mormyrid brainstem--II. The medullary electromotor relay nucleus: an ultrastructural horseradish peroxidase study.

The medullary relay nucleus of the mormyrid weakly electric fish Gnathonemus petersii is a stage in the command pathway for the electric organ discharge. It receives input from the presumed command or pacemaker nucleus and projects to the electromotoneurons in the spinal cord. Its fine structure and synaptology were investigated by electron microscopy. The origin of the terminals contacting the cell membrane of the neurons of this nucleus was determined by horseradish peroxidase (HRP) injections into different brain structures, namely into the bulbar command- and mesencephalic command-associated nuclei. Twenty-five to thirty large cells of about 45 micron in diameter constitute the medullary electromotor relay. Each cell has a kidney-shaped, lobulated nucleus, a large myelinated axon with a short initial segment and several long, richly arborizing primary dendrites. Many, if not all, cells are interconnected with large somatosomatic or dendrosomatic, dendrodendritic and dendroaxonic gap junctions. These junctions often occur in serial or triadic arrangements. The relay cells receive large club endings as well as small boutons. The club endings are found mainly on the soma and primary dendrites and are morphologically mixed synapses. The boutons are characterized by synapses which are only chemical and are distributed all over the cell membrane, but with a definitely higher frequency on secondary dendrites and more distal parts of dendritic processes. Horseradish peroxidase injections into the mesencephalic command-associated nucleus reveal a large number of labelled boutons on the secondary dendrites of the relay cells. Injections into the bulbar command-associated nucleus label the same type of boutons as mesencephalic injections, but also label club endings on relay cell soma and primary dendrites. The results support the conclusion made on the basis of previous light microscopical observations that boutons originate from the bulbar command-associated nucleus, whereas the club endings issue from the presumed pacemaker nucleus (nucleus c). The club endings of the bifurcating axons of this nucleus are labelled by retro- and anterograde transport of horseradish peroxidase; the bifurcating axons project simultaneously to the bulbar command-associated nucleus and the medullary relay nucleus.

The mormyrid rhombencephalon: I. Light and EM investigations on the structure and connections of the lateral line lobe nucleus with HRP labelling.

The rhombencephalic posterior lateral line lobe nucleus (nLLL) and its connections were investigated in the mormyrid fish Gnathonemus petersii, at light and electron microscopical levels using HRP tracing. The nLLL, constituted on each side of about 1500 large, round shaped, adendritic cells, is located in the intermediate cell and fibre layer exclusively, in the ventrolateral zone of the posterior lateral line lobe. The cells show a complex synaptology: boutons with chemical synapses cover the largest part of the soma and the long initial segment of the axons. In addition each nLLL cell bears generally two club endings which form gap junctions with the postsynaptic membrane. On the unmyelinated portion of the club ending, a particular synaptic complex (= serial synaptic connections) was observed; large endings, bearing boutons with chemical synapses, contact the club ending with gap junctions. HRP injection into either lateral line nerve showed that the club endings represent the peripheral input of the nLLL. This input is exclusively ipsilateral; the anterior and posterior lateral line nerve projection does not seem to overlay at this level. Retrograde labelling of nLLL cells after HRP injection into the anterior mesencephalic exterolateral nucleus (nELa) confirms the electrophysiological results according to which the nLLL projects directly and bilaterally to the nELa. This rhombo-mesencephalic connection is established through club endings of the nLLL axons which form gap junctions with the large cells of the nELa. About two thirds of the nLLL axons form a crossed and one third an uncrossed bundle within the lateral lemniscal pathway. Anterograde transport in the axon collaterals shows that some of the nLLL cells project simultaneously to the ipsi- and to the contralateral nELa permitting this system a high degree of electrosensory information processing.

Synaptic structure of the lateral line lobe nucleus in mormyrid fish.

Electron microscopical observations reveal a complex synaptic structure (Fig. 1) in the nucleus of the lateral line lobe (nLLL). Different types of axosomatic and axoaxonic synapses are demonstrated to be in contact with the large cells. The results furnish morphological evidence for electrotonic transmission (by way of club endings with gap junctions) at this level of the electrosensory pathway of mormyrid fish. A new ultrastructural finding is the existence of presynaptic gap junctions on the unmyelinated surface area of the club endings.

An electrotonically coupled pathway in the central nervous system of some teleost fish, Gymnotidae and Mormyridae.

Morphological and physiological results indicate that the magnocellular mesencephalic nucleus (MMN) is characteristic of all species of weakly electric fish, so far investigated. The potentials recorded from this nucleus are due to the fish's own electric organ discharge (EOD). After abolition of the EOD by curare the mesencephalic potential is suppressed, but it can still be obtained by artificial electric stimulation. After injection of curare the medullary pacemaker activity responsible for the EOD remains undisturbed. The results, therefore, let us exclude the hypothesis that the mesencephalic response is evoked by recurrent pacemaker activity. The very short delay (1 msec) of the mesencephalic potential is explained by the existence of a rapid conduction electrosensory pathway where the peripheral, rhombencephalic and mesencephalic elements are electrotonically coupled. This kind of transmission provides a constant synaptic delay and a one-to-one input-output ratio. The fish can receive, by means of this electrosensory pathway, a binary signal for each electrical event whether it comes from its own electric organ or from neighbouring fish.