Second-Order Vestibular Neurons Form Separate Populations With Different Membrane and Discharge Properties

2004 ◽  
Vol 92 (2) ◽  
pp. 845-861 ◽  
Author(s):  
H. Straka ◽  
M. Beraneck ◽  
M. Rohregger ◽  
L. E. Moore ◽  
P.-P. Vidal ◽  
...  
Keyword(s):  
Electrical Stimulation ◽  
Second Order ◽  
Membrane Properties ◽  
Discharge Pattern ◽  
Response Dynamics ◽  
Vestibular Neurons ◽  
Positive Current ◽  
Current Steps ◽  
Passive Membrane Properties ◽  
Stimulation Of

Membrane and discharge properties were determined in second-order vestibular neurons (2°VN) in the isolated brain of grass frogs. 2°VN were identified by monosynaptic excitatory postsynaptic potentials after separate electrical stimulation of the utricular nerve, the lagenar nerve, or individual semicircular canal nerves. 2°VN were classified as vestibulo-ocular or -spinal neurons by the presence of antidromic spikes evoked by electrical stimulation of the spinal cord or the oculomotor nuclei. Differences in passive membrane properties, spike shape, and discharge pattern in response to current steps and ramp-like currents allowed a differentiation of frog 2°VN into two separate, nonoverlapping types of vestibular neurons. A larger subgroup of 2°VN (78%) was characterized by brief, high-frequency bursts of up to five spikes and the absence of a subsequent continuous discharge in response to positive current steps. In contrast, the smaller subgroup of 2°VN (22%) exhibited a continuous discharge with moderate adaptation in response to positive current steps. The differences in the evoked spike discharge pattern were paralleled by differences in passive membrane properties and spike shapes. Despite these differences in membrane properties, both types, i.e., phasic and tonic 2°VN, occupied similar anatomical locations and displayed similar afferent and efferent connectivities. Differences in response dynamics of the two types of 2°VN match those of their pre- and postsynaptic neurons. The existence of distinct populations of 2°VN that differ in response dynamics but not in the spatial organization of their afferent inputs and efferent connectivity to motor targets suggests that frog 2°VN form one part of parallel vestibulomotor pathways.

scholarly journals Canal-Specific Excitation and Inhibition of Frog Second-Order Vestibular Neurons

1997 ◽  
Vol 78 (3) ◽  
pp. 1363-1372 ◽  
Author(s):  
H. Straka ◽  
S. Biesdorf ◽  
N. Dieringer
Keyword(s):  
Electrical Stimulation ◽  
Semicircular Canal ◽  
Second Order ◽  
Projection Neurons ◽  
Postsynaptic Potentials ◽  
Vestibular Neurons ◽  
Inhibitory Postsynaptic Potentials ◽  
Monosynaptic Epsp ◽  
Stimulation Of ◽  
Monosynaptic Excitation

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.

Vestibuloocular Reflex of the Adult Flatfish. III. A Species-Specific Reciprocal Pattern of Excitation and Inhibition

2001 ◽  
Vol 86 (3) ◽  
pp. 1376-1388 ◽  
Author(s):  
Werner Graf ◽  
Robert Spencer ◽  
Harriet Baker ◽  
Robert Baker
Keyword(s):  
Electrical Stimulation ◽  
Synaptic Vesicles ◽  
Second Order ◽  
Vestibuloocular Reflex ◽  
Horizontal Canal ◽  
Postsynaptic Potentials ◽  
Synaptic Contacts ◽  
Vestibular Neurons ◽  
Species Specific ◽  
Stimulation Of

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.

Differential Inhibitory Control of Semicircular Canal Nerve Afferent-Evoked Inputs in Second-Order Vestibular Neurons by Glycinergic and GABAergic Circuits

2008 ◽  
Vol 99 (4) ◽  
pp. 1758-1769 ◽  
Author(s):  
Stefan Biesdorf ◽  
David Malinvaud ◽  
Ingrid Reichenberger ◽  
Sandra Pfanzelt ◽  
Hans Straka
Keyword(s):  
Inhibitory Control ◽  
Semicircular Canal ◽  
Vestibular Nucleus ◽  
Second Order ◽  
Membrane Properties ◽  
Synaptic Organization ◽  
Nerve Branch ◽  
Postsynaptic Potentials ◽  
Vestibular Neurons ◽  
Intrinsic Signal

Labyrinthine nerve-evoked monosynaptic excitatory postsynaptic potentials (EPSPs) in second-order vestibular neurons (2°VN) sum with disynaptic inhibitory postsynaptic potentials (IPSPs) that originate from the thickest afferent fibers of the same nerve branch and are mediated by neurons in the ipsilateral vestibular nucleus. Pharmacological properties of the inhibition and the interaction with the afferent excitation were studied by recording monosynaptic responses of phasic and tonic 2°VN in an isolated frog brain after electrical stimulation of individual semicircular canal nerves. Specific transmitter antagonists revealed glycine and GABAA receptor-mediated IPSPs with a disynaptic onset only in phasic but not in tonic 2°VN. Compared with GABAergic IPSPs, glycinergic responses in phasic 2°VN have larger amplitudes and a longer duration and reduce early and late components of the afferent nerve-evoked subthreshold activation and spike discharge. The difference in profile of the disynaptic glycinergic and GABAergic inhibition is compatible with the larger number of glycinergic as opposed to GABAergic terminal-like structures on 2°VN. The increase in monosynaptic excitation after a block of the disynaptic inhibition in phasic 2°VN is in part mediated by a N-methyl-d-aspartate receptor-activated component. Although inhibitory inputs were superimposed on monosynaptic EPSPs in tonic 2°VN as well, the much longer latency of these IPSPs excludes a control by short-latency inhibitory feed-forward side-loops as observed in phasic 2°VN. The differential synaptic organization of the inhibitory control of labyrinthine afferent signals in phasic and tonic 2°VN is consistent with the different intrinsic signal processing modes of the two neuronal types and suggests a co-adaptation of intrinsic membrane properties and emerging network properties.

Firing Behavior of Vestibular Neurons During Active and Passive Head Movements: Vestibulo-Spinal and Other Non-Eye-Movement Related Neurons

1999 ◽  
Vol 82 (1) ◽  
pp. 416-428 ◽  
Author(s):  
Robert A. McCrea ◽  
Greg T. Gdowski ◽  
Richard Boyle ◽  
Timothy Belton
Keyword(s):  
Electrical Stimulation ◽  
Eye Movement ◽  
Head Rotation ◽  
Head Movements ◽  
Whole Body ◽  
Body Rotation ◽  
Firing Behavior ◽  
Vestibular Neurons ◽  
Gaze Saccades ◽  
Stimulation Of

The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units ( n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20–75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.

EFFECTS OF NEURAL STALK STIMULATION ON PHASIC DISCHARGE OF SUPRAOPTIC NEURONES IN BRATTLEBORO RATS DEVOID OF VASOPRESSIN

1981 ◽  
Vol 90 (2) ◽  
pp. 211-220 ◽  
Author(s):  
G. LENG ◽  
J. WIERSMA
Keyword(s):  
Electrical Stimulation ◽  
Diabetes Insipidus ◽  
Supraoptic Nucleus ◽  
Discharge Pattern ◽  
Brattleboro Rats ◽  
Long Evans ◽  
Discharge Patterns ◽  
Stimulation Of

Brattleboro rats, homozygous for diabetes insipidus, and Long–Evans rats were anaesthetized with urethane, and antidromically identified neurones were recorded from the supraoptic nucleus. Phasically firing neurones were studied during repeated electrical stimulation of the neural stalk, whereby most supraoptic neurones, but not the recorded neurone, were activated antidromically. Such stimulation consistently modified the discharge pattern of phasic neurones in Long–Evans rats, but was relatively ineffective in Brattleboro rats. These results suggest that the effects of neural stalk stimulation on discharge patterns in Long–Evans rats may be substantially mediated by the evoked release of vasopressin or neurophysin.

Topiramate is likely to act outside of the trigeminocervical complex

Cephalalgia ◽  
2013 ◽  
Vol 33 (5) ◽  
pp. 291-300 ◽  
Author(s):  
Robin J Storer ◽  
Peter J Goadsby
Keyword(s):  
Electrical Stimulation ◽  
Superior Sagittal Sinus ◽  
Significant Inhibition ◽  
Second Order ◽  
Trigeminovascular System ◽  
Extracellular Recordings ◽  
Sagittal Sinus ◽  
Sites Of Action ◽  
Laboratory Models ◽  
Stimulation Of

Background To facilitate understanding the locus and mechanism of action of antimigraine preventives, we examined the effect of topiramate on trigeminocervical activation in the cat. Methods Cats were anesthetized and physiologically monitored. Electrical stimulation of the superior sagittal sinus activated nociceptive trigeminovascular afferents. Extracellular recordings were made from neurons in the trigeminocervical complex. Results Microiontophoretically delivered topiramate, applied locally at the second order synapse of the trigeminovascular system in the trigeminocervical complex, produced significant inhibition of L-glutamate-evoked firing of neurons only at the highest microiontophoretic currents (27 ± 7% at −160 nA; p < 0.05, n = 14 cells), but did not inhibit firing of these neurons evoked by stimulation of the craniovascular afferents (2 ± 5%, p = 0.762, n = 13 cells). In contrast, systemically administered topiramate (30 mg/kg intravenously) partly inhibited this firing (32 ± 10% at 15 min; F5,35 = 3.5, p < 0.05, n = 8 cats). After this systemic administration, profound inhibition (70 ± 10%, p < 0.001, n = 7) of L-glutamate-evoked firing of cells in the trigeminocervical complex at the second order synapse of the trigeminovascular system was observed. Conclusions These data suggest that topiramate acts outside of the trigeminocervical complex in the cat. Determining the sites of action of preventive antimigraine treatments is crucial to developing laboratory models for the development of new therapeutics, and may vary between species.

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