Excitatory and Inhibitory Vestibular Pathways to the Extraocular Motor Nuclei in Goldfish

1997 ◽  
Vol 77 (5) ◽  
pp. 2765-2779 ◽  
Author(s):  
Werner Graf ◽  
Robert Spencer ◽  
Harriet Baker ◽  
Robert Baker

Graf, Werner, Robert Spencer, Harriet Baker, and Robert Baker. Excitatory and inhibitory vestibular pathways to the extraocular motor nuclei in goldfish. J. Neurophysiol. 77: 2765–2779, 1997. Electrophysiological, ultrastructural, and immunohistochemical techniques were utilized to describe the excitatory and inhibitory vestibular innervation of extraocular motor nuclei in the goldfish. In antidromically activated oculomotor motoneurons, electrical stimulation of the intact contralateral vestibular nerve produced short-latency, variable amplitude electrotonic excitatory postsynaptic potentials (EPSPs) at 0.5–0.7 ms followed by chemical EPSPs at 1.0–1.3 ms. Stimulation of the ipsilateral vestibular nerve produced small amplitude membrane hyperpolarizations at a latency of 1.3–1.7 ms in which equilibrium potentials were slightly more negative than resting potentials. The inhibitory postsynaptic potentials (IPSPs) reversed with large amplitudes after the injection of chloride ions suggesting a proximal soma-dendritic location of terminals exhibiting high efficacy inhibitory synaptic conductances. In antidromically identified abducens motoneurons and putative internuclear neurons, electrical stimulation of the contralateral vestibular nerve produced large-amplitude, short-latency electrotonic EPSPs at 0.5 ms followed by chemical depolarizations at 1.2–1.3 ms. Stimulation of the ipsilateral vestibular nerve evoked IPSPs at 1.4 ms that were reversed after injection of current and/or chloride ions. γ-Aminobutyric acid (GABA) antibodies labeled inhibitory neurons in vestibular subdivisions with axons projecting into the ipsilateral medial longitudinal fasciculus (MLF). Putative GABAergic terminals surrounded oculomotor, but not abducens, motoneurons retrogradely labeled with horseradish peroxidase. Hence the spatial distribution of GABAergic neurons and terminals appears highly similar in the vestibuloocular system of goldfish and mammals. Electron microscopy of motoneurons in the oculomotor and abducens nucleus showed axosomatic and axodendritic synaptic endings containing spheroidal synaptic vesicles establishing chemical, presumed excitatory, synaptic contacts with asymmetric pre- and/or postsynaptic membrane specializations. The majority of contacts with spheroidal vesicles displayed gap junctions in which the chemical and electrotonic synapses were either en face to dissimilar or adjacent to one another on the same soma/dendritic profiles. Another separate set of axosomatic synaptic endings, presumed to be inhibitory, contained pleiomorphic synaptic vesicles with symmetric pre- and/or postsynaptic membrane specializations that never included gap junctions. Excitatory and inhibitory synaptic contacts appeared equal in number but were more sparsely distributed along the soma-dendritic profiles of oculomotor as compared with abducens motoneurons. Collectively these data provide evidence for both disynaptic vestibular inhibition and excitation in all subdivisions of the extraocular motor nuclei suggesting the basic vestibulooculomotor blueprint to be conserved among vertebrates. We propose that unique vestibular neurons, transmitters, pathways, and synaptic arborizations are homologous structural traits that have been essentially preserved throughout vertebrate phylogeny by a shared developmental plan.

2001 ◽  
Vol 86 (3) ◽  
pp. 1376-1388 ◽  
Author(s):  
Werner Graf ◽  
Robert Spencer ◽  
Harriet Baker ◽  
Robert Baker

In juvenile flatfish the vestibuloocular reflex (VOR) circuitry that underlies compensatory eye movements adapts to a 90° relative displacement of vestibular and oculomotor reference frames during metamorphosis. VOR pathways are rearranged to allow horizontal canal-activated second-order vestibular neurons in adult flatfish to control extraocular motoneurons innervating vertical eye muscles. This study describes the anatomy and physiology of identified flatfish-specific excitatory and inhibitory vestibular pathways. In antidromically identified oculomotor and trochlear motoneurons, excitatory postsynaptic potentials (EPSPs) were elicited after electrical stimulation of the horizontal canal nerve expected to provide excitatory input. Electrotonic depolarizations (0.8–0.9 ms) preceded small amplitude (<0.5 mV) chemical EPSPs at 1.2–1.6 ms with much larger EPSPs (>1 mV) recorded around 2.5 ms. Stimulation of the opposite horizontal canal nerve produced inhibitory postsynaptic potentials (IPSPs) at a disynaptic latency of 1.6–1.8 ms that were depolarizing at membrane resting potentials around −60 mV. Injection of chloride ions increased IPSP amplitude, and current-clamp analysis showed the IPSP equilibrium potential to be near the membrane resting potential. Repeated electrical stimulation of either the excitatory or inhibitory horizontal canal vestibular nerve greatly increased the amplitude of the respective synaptic responses. These observations suggest that the large terminal arborizations of each VOR neuron imposes an electrotonic load requiring multiple action potentials to maximize synaptic efficacy. GABA antibodies labeled axons in the medial longitudinal fasciculus (MLF) some of which were hypothesized to originate from horizontal canal-activated inhibitory vestibular neurons. GABAergic terminal arborizations were distributed largely on the somata and proximal dendrites of oculomotor and trochlear motoneurons. These findings suggest that the species-specific horizontal canal inhibitory pathway exhibits similar electrophysiological and synaptic transmitter profiles as the anterior and posterior canal inhibitory projections to oculomotor and trochlear motoneurons. Electron microscopy showed axosomatic and axodendritic synaptic endings containing spheroidal synaptic vesicles to establish chemical excitatory synaptic contacts characterized by asymmetrical pre/postsynaptic membrane specializations as well as gap junctional contacts consistent with electrotonic coupling. Another type of axosomatic synaptic ending contained pleiomorphic synaptic vesicles forming chemical, presumed inhibitory, synaptic contacts on motoneurons that never included gap junctions. Altogether these data provide electrophysiological, immunohistochemical, and ultrastructural evidence for reciprocal excitatory/inhibitory organization of the novel vestibulooculomotor projections in adult flatfish. The appearance of unique second-order vestibular neurons linking the horizontal canal to vertical oculomotor neurons suggests that reciprocal excitation and inhibition are a fundamental, developmentally linked trait of compensatory eye movement circuits in vertebrates.


2000 ◽  
Vol 203 (3) ◽  
pp. 435-445
Author(s):  
M. Wildman

The position of the coxal segment of the locust hind leg relative to the thorax is monitored by a variety of proprioceptors, including three chordotonal organs and a myochordotonal organ. The sensory neurons of two of these proprioceptors, the posterior joint chordotonal organ (pjCO) and the myochordotonal organ (MCO), have axons in the purely sensory metathoracic nerve 2C (N2C). The connections made by these afferents with metathoracic motor neurons innervating thoraco-coxal and wing muscles were investigated by electrical stimulation of N2C and by matching postsynaptic potentials in motor neurons with afferent spikes in N2C. Stretch applied to the anterior rotator muscle of the coxa (M121), with which the MCO is associated, evoked sensory spikes in N2C. Some of the MCO afferent neurons make direct excitatory chemical synaptic connections with motor neurons innervating the thoraco-coxal muscles M121, M126 and M125. Parallel polysynaptic pathways via unidentified interneurons also exist between MCO afferents and these motor neurons. Connections with the common inhibitor 1 neuron and motor neurons innervating the thoraco-coxal muscles M123/4 and wing muscles M113 and M127 are polysynaptic. Afferents of the pjCO also make polysynaptic connections with motor neurons innervating thoraco-coxal and wing muscles, but no evidence for monosynaptic pathways was found.


2001 ◽  
Vol 86 (5) ◽  
pp. 2583-2596 ◽  
Author(s):  
M.-J. Bourque ◽  
A. Kolta

Numerous evidence suggests that interneurons located in the lateral tegmentum at the level of the trigeminal motor nucleus contribute importantly to the circuitry involved in mastication. However, the question of whether these neurons participate actively to genesis of the rhythmic motor pattern or simply relay it to trigeminal motoneurons remains open. To answer this question, intracellular recordings were performed in an in vitro slice preparation comprising interneurons of the peritrigeminal area (PeriV) surrounding the trigeminal motor nucleus (NVmt) and the parvocellular reticular formation ventral and caudal to it (PCRt). Intracellular and extracellular injections of anterograde tracers were also used to examine the local connections established by these neurons. In 97% of recordings, electrical stimulation of adjacent areas evoked a postsynaptic potential (PSP). These PSPs were primarily excitatory, but inhibitory and biphasic responses were also induced. Most occurred at latencies longer than those required for monosynaptic transmission and were considered to involve oligosynaptic pathways. Both the anatomical and physiological findings show that all divisions of PeriV and PCRt are extensively interconnected. Most responses followed high-frequency stimulation (50 Hz) and showed little variability in latency indicating that the network reliably distributes inputs across all areas. In all neurons but one, excitatory postsynaptic potentials (EPSPs) or inhibitory postsynaptic potentials (IPSPs) were also elicited by stimulation of NVmt, suggesting the existence of excitatory and inhibitory interneurons within the motor nucleus. In a number of cases, these PSPs were reproduced by local injection of glutamate in lieu of the electrical stimulation. All EPSPs induced by stimulation of PeriV, PCRt, or NVmt were sensitive to ionotropic glutamate receptor antagonists 6-cyano-7-dinitroquinoxaline and d,l-2-amino-5-phosphonovaleric acid, while IPSPs were blocked by bicuculline and strychnine, antagonists of GABAA and glycine receptors. Examination of PeriV and PCRt intrinsic properties indicate that they form a fairly uniform network. Three types of neurons were identified on the basis of their firing adaptation properties. These types were not associated with particular regions. Only 5% of all neurons showed bursting behavior. Our results do not support the hypothesis that neurons of PeriV and PCRt participate actively to rhythm generation, but suggest instead that they are driven by rhythmical synaptic inputs. The organization of the network allows for rapid distribution of this rhythmic input across premotoneuron groups.


2020 ◽  
Vol 28 (3) ◽  
pp. 35-50
Author(s):  
Oleg S. Sotnikov ◽  
Svetlana S. Sergeeva ◽  
Tat'yana I. Vasyagina

After the creation of a method for obtaining inter-neuronal gap junctions in a nervous system devoid of glia, it is expedient to reproduce gap neuronal-glial contacts on a model that also contains hybrid neuronal-glial gap junctions, which, as you know, are functionally fundamentally different from inter-neuronal contacts. The experiments were carried out on the truncus sympathicus ganglia of laboratory rats using pessimal electrical stimulation and transmission electron microscopy. Electrical activation of ganglia with a frequency of up to 100 Hz revealed local and widespread variants of various neuronal-glial connections (contacts, bridges), fringed with peri-membrane filamentous proteins. They had a blurred veil that masked two-layer neuro-membranes. Some of the contacts resembled slit or dense 5-layer structures without a visible inter-neuronal slit, but with an extreme decrease in the thickness of the contact slit. The main result of the experiments was the formation, in addition to slotted, multiple septate (ladder) contacts. Relatively independent aggregates of the electron-dense substance of the septa were located inside the intercellular gaps, crossing both adjacent membranes, and, possibly, permeate of them. Near-membrane, poorly outlined pyramid-like protein cones associated with both cell membranes were also formed. Such membranes appeared to be dotted-dashed, that is, not continuous. A significant number of septic contact membranes had endocytic invaginations (invaginations) facing neuroplasm with pyramid-like marginal projections. All reactive altered structures that have arisen de novo are considered by the authors as developed under the influence of frequency electrical stimulation of denaturation and aggregation of intrinsic and perimembrane proteins.


2000 ◽  
Vol 83 (6) ◽  
pp. 3209-3216 ◽  
Author(s):  
Jean-François Perrier ◽  
Boris Lamotte D'Incamps ◽  
Nezha Kouchtir-Devanne ◽  
Léna Jami ◽  
Daniel Zytnicki

The postsynaptic potentials elicited in peroneal motoneurons by either mechanical stimulation of cutaneous areas innervated by the superficial peroneal nerve (SP) or repetitive electrical stimulation of SP were compared in anesthetized cats. After denervation of the foot sparing only the territory of SP terminal branches, reproducible mechanical stimulations were applied by pressure on the plantar surface of the toes via a plastic disk attached to a servo-length device, causing a mild compression of toes. This stimulus evoked small but consistent postsynaptic potentials in every peroneal motoneuron. Weak stimuli elicited only excitatory postsynaptic potentials (EPSPs), whereas increase in stimulation strength allowed distinction of three patterns of response. In about one half of the sample, mechanical stimulation or trains of 20/s electric pulses at strengths up to six times the threshold of the most excitable fibers in the nerve evoked only EPSPs. Responses to electrical stimulation appeared with 3–7 ms central latencies, suggesting oligosynaptic pathways. In another, smaller fraction of the sample, inhibitory postsynaptic potentials (IPSPs) appeared with an increase of stimulation strength, and the last fraction showed a mixed pattern of excitation and inhibition. In 24 of 32 motoneurons where electrical and mechanical effects could be compared, the responses were similar, and in 6 others, they changed from pure excitation on mechanical stimulation to mixed on electrical stimulation. With both kinds of stimulation, stronger stimulations were required to evoke inhibitory postsynaptic potentials (IPSPs), which appeared at longer central latencies than EPSPs, indicating longer interneuronal pathways. The similarity of responses to mechanical and electrical stimulation in a majority of peroneal motoneurons suggests that the effects of commonly used electrical stimulation are good predictors of the responses of peroneal motoneurons to natural skin stimulation. The different types of responses to cutaneous afferents from SP territory reflect a complex connectivity allowing modulations of cutaneous reflex responses in various postures and gaits.


1997 ◽  
Vol 78 (3) ◽  
pp. 1363-1372 ◽  
Author(s):  
H. Straka ◽  
S. Biesdorf ◽  
N. Dieringer

Straka, H., S. Biesdorf, and N. Dieringer. Canal-specific excitation and inhibition of frog second-order vestibular neurons. J. Neurophysiol. 78: 1363–1372, 1997. Second-order vestibular neurons (2°VNs) were identified in the in vitro frog brain by their monosynaptic excitation following electrical stimulation of the ipsilateral VIIIth nerve. Ipsilateral disynaptic inhibitory postsynaptic potentials were revealed by bath application of the glycine antagonist strychnine or of the γ-aminobutyric acid-A (GABAA) antagonist bicuculline. Ipsilateral disynaptic excitatory postsynaptic potentials (EPSPs) were analyzed as well. The functional organization of convergent monosynaptic and disynaptic excitatory and inhibitory inputs onto 2°VNs was studied by separate electrical stimulation of individual semicircular canal nerves on the ipsilateral side. Most 2°VNs (88%) received a monosynaptic EPSP exclusively from one of the three semicircular canal nerves; fewer 2°VNs (10%) were monosynaptically excited from two semicircular canal nerves; and even fewer 2°VNs (2%) were monosynaptically excited from each of the three semicircular canal nerves. Disynaptic EPSPs were present in the majority of 2°VNs (68%) and originated from the same (homonymous) semicircular canal nerve that activated a monosynaptic EPSP in a given neuron (22%), from one or both of the other two (heteronymous) canal nerves (18%), or from all three canal nerves (28%). Homonymous activation of disynaptic EPSPs prevailed (74%) among those 2°VNs that exhibited disynaptic EPSPs. Disynaptic inhibitory postsynaptic potentials (IPSPs) were mediated in 90% of the tested 2°VNs by glycine, in 76% by GABA, and in 62% by GABA as well as by glycine. These IPSPs were activated almost exclusively from the same semicircular canal nerve that evoked the monosynaptic EPSP in a given 2°VN. Our results demonstrate a canal-specific, modular organization of vestibular nerve afferent fiber inputs onto 2°VNs that consists of a monosynaptic excitation from one semicircular canal nerve followed by disynaptic excitatory and inhibitory inputs originating from the homonymous canal nerve. Excitatory and inhibitory second-order (2°) vestibular interneurons are envisaged to form side loops that mediate spatially similar but dynamically different signals to 2° vestibular projection neurons. These feedforward side loops are suited to adjust the dynamic response properties of 2° vestibular projection neurons by facilitating or disfacilitating phasic and tonic input components.


1957 ◽  
Vol 3 (4) ◽  
pp. 611-614 ◽  
Author(s):  
Eduardo De Robertis ◽  
Alberto Vaz Ferreira

The nerve endings of the adrenal medulla of the rabbit were studied under the electron microscope in the normal condition and after prolonged electrical stimulation of the splanchnic nerve. With a stimulus of 100 pulses per second for 10 minutes, there is an increase in the number of synaptic vesicles in the nerve ending. The mean number is of 82.6 vesicles per square micron in the normal and of 132.7 per square micron in the stimulated glands. With a stimulus of 400 pulses per second for 10 minutes, there is a considerable depletion of synaptic vesicles and other changes occur in the nerve endings. The mean number of vesicles is of 29.2 per square micron. These results are interpreted as indicative of an increased activity of the ending in one case, and as a diminished activity and fatigue of the synaptic junction in the other.


1999 ◽  
Vol 16 (5) ◽  
pp. 889-893 ◽  
Author(s):  
STEPHEN A. GEORGE ◽  
GANG-YI WU ◽  
WEN-CHANG LI ◽  
SHU-RONG WANG

We analyzed postsynaptic potentials and dye-labeled morphology of tectal neurons responding to electrical stimulation of the optic nerve and of the nucleus isthmi in a reptile, Gekko gekko, in order to compare with previously reported interactions between the optic tectum and the nucleus isthmi in amphibians and birds. The results indicate that isthmic stimulation exerts inhibitory and excitatory actions on tectal cells, similar to dual isthmotectal actions in amphibians. It appears that dual actions of the isthmotectal pathway in amphibians and reptiles are shared by two subdivisions of the nucleus isthmi in birds. The morphology of tectal cells responding to isthmic stimulation is generally similar to that of tectoisthmic projecting neurons, but they differ particularly in that some tectoisthmic cells bear numerous varicosities whereas cells receiving isthmic afferents do not. Thus, it is likely that at least some tectoisthmic cells may not be in the population of tectal cells that can be affected by isthmic stimulation. Forty-four percent of injections resulted in dye-coupled labeling, suggesting extensive electrical connections between tectal cells in reptiles.


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