Patterns of Canal and Otolith Afferent Input Convergence in Frog Second-Order Vestibular Neurons

2002 ◽  
Vol 88 (5) ◽  
pp. 2287-2301 ◽  
Author(s):  
H. Straka ◽  
S. Holler ◽  
F. Goto
Keyword(s):  
Semicircular Canal ◽  
Linear Acceleration ◽  
Afferent Input ◽  
Second Order ◽  
Head Movements ◽  
Otolith Organs ◽  
Otolith Organ ◽  
Horizontal Canal ◽  
Vestibular Neurons ◽  
Saccular Nerve

Second-order vestibular neurons (2°VN) were identified in the isolated frog brain by the presence of monosynaptic excitatory postsynaptic potentials (EPSPs) after separate electrical stimulation of individual vestibular nerve branches. Combinations of one macular and the three semicircular canal nerve branches or combinations of two macular nerve branches were stimulated separately in different sets of experiments. Monosynaptic EPSPs evoked from the utricle or from the lagena converged with monosynaptic EPSPs from one of the three semicircular canal organs in ∼30% of 2°VN. Utricular afferent signals converged predominantly with horizontal canal afferent signals (74%), and lagenar afferent signals converged with anterior vertical (63%) or posterior vertical (37%) but not with horizontal canal afferent signals. This convergence pattern correlates with the coactivation of particular combinations of canal and otolith organs during natural head movements. A convergence of afferent saccular and canal signals was restricted to very few 2°VN (3%). In contrast to the considerable number of 2°VN that received an afferent input from the utricle or the lagena as well as from one of the three canal nerves (∼30%), smaller numbers of 2°VN (14% of each type of 2°otolith or 2°canal neuron) received an afferent input from only one particular otolith organ or from only one particular semicircular canal organ. Even fewer 2°VN received an afferent input from more than one semicircular canal or from more than one otolith nerve (∼7% each). Among 2°VN with afferent inputs from more than one otolith nerve, an afferent saccular nerve input was particularly rare (4–5%). The restricted convergence of afferent saccular inputs with other afferent otolith or canal inputs as well as the termination pattern of saccular afferent fibers are compatible with a substrate vibration sensitivity of this otolith organ in frog. The ascending and/or descending projections of identified 2°VN were determined by the presence of antidromic spikes. 2°VN mediating afferent utricular and/or semicircular canal nerve signals had ascending and/or descending axons. 2°VN mediating afferent lagenar or saccular nerve signals had descending but no ascending axons. The latter result is consistent with the absence of short-latency macular signals on extraocular motoneurons during vertical linear acceleration. Comparison of data from frog and cat demonstrated the presence of a similar organization pattern of maculo- and canal-ocular reflexes in both species.

scholarly journals Concepts and Physiological Aspects of the Otolith Organ in Relation to Electrical Stimulation

2019 ◽  
Vol 25 (Suppl. 1-2) ◽  
pp. 25-34 ◽  
Author(s):  
Ian S. Curthoys
Keyword(s):  
Electrical Stimulation ◽  
Semicircular Canal ◽  
Vestibular Nucleus ◽  
Angular Acceleration ◽  
Linear Acceleration ◽  
Afferent Input ◽  
Cell Polarization ◽  
Otolith Organs ◽  
The One ◽  
Stimulation Of

Background: This paper discusses some of the concepts and major physiological issues in developing a means of electrically stimulating the otolithic system, with the final goal being the electrical stimulation of the otoliths in human patients. It contrasts the challenges of electrical stimulation of the otolith organs as compared to stimulation of the semicircular canals. Electrical stimulation may consist of trains of short-duration pulses (e.g., 0.1 ms duration at 400 Hz) by selective electrodes on otolith maculae or otolithic afferents, or unselective maintained DC stimulation by large surface electrodes on the mastoids – surface galvanic stimulation. Summary: Recent anatomical and physiological results are summarized in order to introduce some of the unique issues in electrical stimulation of the otoliths. The first challenge is that each otolithic macula contains receptors with opposite polarization (opposing preferred directions of stimulation), unlike the uniform polarization of receptors in each semicircular canal crista. The puzzle is that in response to the one linear acceleration in the one macula, some otolithic afferents have an increased activation whereas others have decreased activation. Key Messages: At the vestibular nucleus this opposite receptor hair cell polarization and consequent opposite afferent input allow enhanced response to the one linear acceleration, via a “push-pull” neural mechanism in a manner analogous to the enhancement of semicircular canal responses to angular acceleration. Within each otolithic macula there is not just one uniform otolithic neural input to the brain – there are very distinctly different channels of otolithic neural inputs transferring the neural data to the brainstem. As a simplification these channels are characterized as the sustained and transient systems. Afferents in each system have different responses to stimulus onset and maintained stimulation and likely different projections, and most importantly different thresholds for activation by electrical stimulation and different adaptation rates to maintained stimulation. The implications of these differences are considered.

Excitatory and Inhibitory Inputs From Saccular Afferents to Single Vestibular Neurons in the Cat

1997 ◽  
Vol 78 (4) ◽  
pp. 2186-2192 ◽  
Author(s):  
Y. Uchino ◽  
H. Sato ◽  
H. Suwa
Keyword(s):  
Hair Cells ◽  
Semicircular Canal ◽  
Response Pattern ◽  
Linear Acceleration ◽  
High Sensitivity ◽  
Vestibular Neurons ◽  
Dorsal Edge ◽  
Stimulus Current ◽  
Saccular Nerve ◽  
Stimulation Of

Uchino, Y., H. Sato, and H. Suwa. Excitatory and inhibitory inputs from saccular afferents to single vestibular neurons in the cat. J. Neurophysiol. 78: 2186–2192, 1997. Connections from saccular afferents to vestibular neurons were studied by means of intracellular recordings of excitatory (E) and inhibitory (I) postsynaptic potentials (PSPs) in vestibular neurons after focal stimulation of the saccular macula in decerebrated cats. Focal stimulation was given to the saccular macula in two ways, in which the polarity of stimulus current via a pair of electrodes was changed. In group A, one of the electrodes was inserted into the ventral and the other into the dorsal edge of the saccular macula. The focal stimulation was across the striola so that the reversal of morphological polarization in hair cells was bridged by the pulse stimulus. In 22/36 vestibular neurons tested, the stimulation of the saccular macula evoked monosynaptic (≤1.2 ms) EPSPs, including EPSP-IPSP sequences, with one polarity of stimulation, and disynaptic (≥1.5 ms) IPSPs when the polarity of the stimulus current was changed. In 14/36 neurons, the response pattern was the same regardless of the stimulus polarity; EPSPs (12/36) or IPSPs (2/36). In group B, a pair of electrodes was inserted into the dorsal edge of the saccular macula, so that the striola was not bridged by the current stimulus. In all of the vestibular neurons tested, the response pattern was always the same regardless of the polarity: mono- (22/31) and disynaptic (3/31) EPSPs or disynaptic IPSPs (6/31). In addition, the saccular nerve was stimulated after removing the macula in some cats ( group C). The stimulation of the saccular nerve evoked EPSPs in 62 vestibular neurons (including EPSP-IPSP sequences in 31 neurons) and IPSPs in 19 vestibular neurons. Convergence between the saccular nerve and other vestibular nerves was studied by the intracellular recording of PSPs. Fifty-six percent (18/32) of the saccular-activated neurons had excitatory and/or inhibitory potentials evoked after stimulation of the utricular nerve and the horizontal and anterior semicircular canal nerves, and 44% (19/43) of the neurons received inputs from the posterior semicircular canal nerve. The results support the hypothesis that saccular afferents from one population of hair cells activate vestibular neurons monosynaptically and that afferents from another population of hair cells located on the opposite side of the striola appear to project to the same vestibular neurons disynaptically via inhibitory interneurons. Neural circuits from saccular afferents to vestibular neurons, which we term cross-striolar inhibition, thus may provide a mechanism for increasing the sensitivity to vertical linear acceleration. The circuit described is provided not only with high sensitivity but also with input noise-resistant characteristics.

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.

scholarly journals Differential Spatial Organization of Otolith Signals in Frog Vestibular Nuclei

2003 ◽  
Vol 90 (5) ◽  
pp. 3501-3512 ◽  
Author(s):  
Hans Straka ◽  
Stefan Holler ◽  
Fumiyuki Goto ◽  
Florian P. Kolb ◽  
Edwin Gilland
Keyword(s):  
Spatial Organization ◽  
Vestibular Nucleus ◽  
Field Potential ◽  
Vestibular Function ◽  
Vestibular Nuclei ◽  
Second Order ◽  
Vestibular Neurons ◽  
Dorsal Nucleus ◽  
Sensory Map ◽  
Saccular Nerve

Activation maps of pre- and postsynaptic field potential components evoked by separate electrical stimulation of utricular, lagenar, and saccular nerve branches in the isolated frog hindbrain were recorded within a stereotactic outline of the vestibular nuclei. Utricular and lagenar nerve-evoked activation maps overlapped strongly in the lateral and descending vestibular nuclei, whereas lagenar amplitudes were greater in the superior vestibular nucleus. In contrast, the saccular nerve-evoked activation map coincided largely with the dorsal nucleus and the adjacent dorsal part of the lateral vestibular nucleus, corroborating a major auditory and lesser vestibular function of the frog saccule. The stereotactic position of individual second-order otolith neurons matched the distribution of the corresponding otolith nerve-evoked activation maps. Furthermore, particular types of second-order utricular and lagenar neurons were clustered with particular types of second-order canal neurons in a topology that anatomically mirrored the preferred convergence pattern of afferent otolith and canal signals in second-order vestibular neurons. Similarities in the spatial organization of functionally equivalent types of second-order otolith and canal neurons between frog and other vertebrates indicated conservation of a common topographical organization principle. However, the absence of a precise afferent sensory topography combined with the presence of spatially segregated groups of particular second-order vestibular neurons suggests that the vestibular circuitry is organized as a premotor map rather than an organotypical sensory map. Moreover, the conserved segmental location of individual vestibular neuronal phenotypes shows linkage of individual components of vestibulomotor pathways with the underlying genetically specified rhombomeric framework.

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.

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.

Relationship of Semicircular Canal Size to Vestibular-Nerve Afferent Sensitivity in Mammals

2007 ◽  
Vol 98 (6) ◽  
pp. 3197-3205 ◽  
Author(s):  
Aizhen Yang ◽  
Timothy E. Hullar
Keyword(s):  
Semicircular Canal ◽  
High Frequency ◽  
High Gain ◽  
Vestibular Nerve ◽  
Radius Of Curvature ◽  
Horizontal Canal ◽  
Vestibular Nerve Afferents ◽  
The Relationship ◽  
Irregular Afferents ◽  
Anterior Canal

The relationship between semicircular canal radius of curvature and afferent sensitivity has not been experimentally determined. We characterized mouse semicircular canal afferent responses to sinusoidal head rotations to facilitate interspecies and intraspecies comparisons of canal size to sensitivity. The interspecies experiment compared the horizontal canal afferent responses among animals ranging in size from mouse to rhesus monkey. The intraspecies experiment compared afferent responses from the larger anterior canal to those from the smaller horizontal canal of mice. The responses of mouse vestibular-nerve afferents showed a low- and high-frequency phase lead and high-frequency gain enhancement. Regular horizontal-canal afferents showed a sensitivity to 0.5-Hz sinusoidal rotations of 0.10 ± 0.03 (SD) spike · s−1/deg · s−1 and high-gain irregular afferents showed a sensitivity of 0.25 ± 0.11 spike · s−1/deg · s−1. The interspecies comparison showed that the sensitivity of regular afferents was related to the radius of curvature R according to the formula Gr = 0.23R − 0.09 ( r2 = 0.86) and the sensitivity of irregular afferents was related to radius according to the formula Gi = 0.32R + 0.01 ( r2 = 0.67). The intraspecies comparison showed that regularly firing anterior canal afferents were significantly more sensitive than those from the relatively smaller horizontal canal, with Gr = 0.25R. This suggests that canal radius of curvature is closely related to afferent sensitivity both among and within species. If the relationship in humans is similar to that demonstrated here, the sensitivity of their regular vestibular-nerve afferents to 0.5-Hz rotations is likely to be about 0.67 spike · s−1/deg · s−1 and of their high-gain irregular afferents about 1.06 spikes · s−1/deg · s−1.

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