Convergence pattern of uncrossed excitatory and inhibitory semicircular canal-specific inputs onto second-order vestibular neurons of frogs

2000 ◽  
Vol 135 (4) ◽  
pp. 462-473 ◽  
Author(s):  
H. Straka ◽  
N. Dieringer
Keyword(s):  
Semicircular Canal ◽  
Second Order ◽  
Vestibular Neurons

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.

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.

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 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.

Effects of ketamine on the adaptive responses of second-order vestibular neurons of the cat

1984 ◽  
Vol 5 (4) ◽  
pp. 262-265 ◽  
Author(s):  
Jai H. Ryu ◽  
Richard W. Babin ◽  
Chan Liu ◽  
Brian F. McCabe
Keyword(s):  
Second Order ◽  
Adaptive Responses ◽  
Vestibular Neurons

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.

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