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

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.

2008 ◽  
Vol 99 (4) ◽  
pp. 1758-1769 ◽  
Author(s):  
Stefan Biesdorf ◽  
David Malinvaud ◽  
Ingrid Reichenberger ◽  
Sandra Pfanzelt ◽  
Hans Straka

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.


2013 ◽  
Vol 110 (8) ◽  
pp. 1822-1836 ◽  
Author(s):  
Shawn D. Newlands ◽  
Min Wei

After vestibular labyrinth injury, behavioral measures of vestibular function partially recover through the process of vestibular compensation. The present study was performed to improve our understanding of the physiology of macaque vestibular nucleus neurons in the compensated state (>6 wk) after unilateral labyrinthectomy (UL). The responses of neurons to sinusoidal yaw rotation at a series of frequencies (0.1–2.0 Hz) and peak velocities (7.5–210°/s) were examined to determine how the behavior of these cells differed from those in animals with intact labyrinths. The sensitivity of neurons responding to ipsilateral rotation (type I) did not differ between the intact and injured sides after UL, although this sensitivity was lower bilaterally after lesion than before lesion. The sensitivity of neurons that increase firing with contralateral rotation (type II) was higher ipsilateral to the UL than before lesion or in the nucleus contralateral to the UL. UL did not increase asymmetry in the responses of individual type I or II neurons to ipsilateral vs. contralateral rotation, nor does it change the power law relationship between neuronal firing and level of stimulation. Increased sensitivities of contralesional type I neurons to the remaining vestibular nerve input and increased efficacy of inhibitory vestibular commissures projecting to the ipsilesional vestibular nucleus appear to be responsible for recovery of dynamic function of central vestibular neurons in compensated animals. The portion of type I neurons on the ipsilesional side is reduced in compensated animals, which likely accounts for the asymmetries in vestibular reflexes and perception that characterize vestibular function after UL.


2009 ◽  
Vol 102 (3) ◽  
pp. 1388-1397 ◽  
Author(s):  
Shawn D. Newlands ◽  
Nan Lin ◽  
Min Wei

Vestibular afferents display linear responses over a range of amplitudes and frequencies, but comparable data for central vestibular neurons are lacking. To examine the effect of stimulus frequency and magnitude on the response sensitivity and linearity of non-eye movement central vestibular neurons, we recorded from the vestibular nuclei in awake rhesus macaques during sinusoidal yaw rotation at frequencies between 0.1 and 2 Hz and between 7.5 and 210°/s peak velocity. The dynamics of the neurons' responses across frequencies, while holding peak velocity constant, was consistent with previous studies. However, as the peak velocity was varied, while holding the frequency constant, neurons demonstrated lower sensitivities with increasing peak velocity, even at the lowest peak velocities tested. With increasing peak velocity, the proportion of neurons that silenced during a portion of the response increased. However, the decrease in sensitivity of these neurons with higher peak velocities of rotation was not due to increased silencing during the inhibitory portion of the cycle. Rather the neurons displayed peak firing rates that did not increase in proportion to head velocity as the peak velocity of rotation increased. These data suggest that, unlike vestibular afferents, the central vestibular neurons without eye movement sensitivity examined in this study do not follow linear systems principles even at low velocities.


1998 ◽  
Vol 80 (5) ◽  
pp. 2352-2367 ◽  
Author(s):  
Laurence Ris ◽  
Emile Godaux

Ris, Laurence and Emile Godaux. Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. J. Neurophysiol. 80: 2352–2367, 1998. In the guinea pig, a unilateral labyrinthectomy is followed by an initial depression and a subsequent restoration of the spontaneous activity in the neurons of the ipsilateral vestibular nuclei. In two previous works, we have established the time course of these changes in the alert guinea pig using electrical stimulation as a search stimulus to select the analyzed neurons. The latter criterion was important to capture the many ipsilateral neurons that are silent at rest during the immediate postlabyrinthectomy stage. Because it is known that a pathway originating from the vestibular nuclei on one side crosses the midline and functionally inhibits the activity of the vestibular nuclei on the other side, we investigated in the first part of this study the spiking behavior of the neurons in the vestibular nuclei contralateral to the labyrinthectomy using the same procedure as that used for the ipsilateral neurons. The spiking behavior of 976 neurons was studied during 4-h recording sessions in intact animals and 1 h, 1 day, 2 days, or 1 wk postlabyrinthectomy. Neurons selected according to the electrical activation criterion were classified further as type I (their firing rate increased during ipsilateral rotation), type II (their firing rate increased during contralateral rotation), or unresponsive. The resting activity of type I neurons, which was 38.1 ± 20.9 spikes/s (mean ± SD) in the control state, increased statistically significantly 1 h after the lesion (53.3 ± 29.1 spikes/s) and remained at this level 1 wk later (56.0 ± 20.3 spikes/s). The sensitivity of type I units, which was 0.80 ± 0.46 spikes/s per deg/s in the control population, decreased to 0.49 ± 0.26 spikes/s per deg/s 1 h after the lesion and remained at this level 1 wk later (0.50 ± 0.39 spikes/s per deg/s). When all monosynaptically activated neurons (type I, type II, unresponsive) were pooled, the sensitivity to horizontal rotation fell from 0.58 ± 0.51 spikes/s per deg/s in the control state to 0.15 ± 0.25 spikes/s per deg/s 1 h after the lesion and to 0.20 ± 0.32 spikes/s per deg/s 1 wk later. The major findings of the first part of this study in the alert guinea pig are thus in accord with those of Curthoys et al. and Smith and Curthoys in anesthetized guinea pigs. In the second part of this work, we studied the spiking behavior of the neurons in the vestibular nuclei after bilateral labyrinthectomy. After unilateral labyrinthectomy, the resting discharge of the ipsilateral monosynaptically activated vestibular neurons fell from 36.9 ± 21 spikes/s (basal activity) to 6.7 ± 17.0 spikes/s 1 h after the lesion and then recovered, reaching 17.4 ± 18.9 and 40.8 ± 23.7 spikes/s 1 day and 1 wk after the lesion, respectively. These observations raise the two following questions. What are the relative contributions of the loss of the excitatory influence from the ipsilateral labyrinth (destroyed) and of the persistence of the inhibitory influence from the contralateral labyrinth (intact) in the labyrinthectomy-induced depression of activity? And are the left-right asymmetries caused by a unilateral labyrinthectomy the driving force for restoration of activity? Here, we addressed these two questions by studying the spiking behavior of 473 second-order vestibular neurons in the alert guinea pig after a bilateral labyrinthectomy. In the acute stage, 1 h after bilateral labyrinthectomy, the resting discharge of the second-order vestibular neurons was 16.2 ± 22.4 spikes/s. From comparison with the results obtained in the acute stage after a unilateral labyrinthectomy, we inferred that the ipsilateral excitatory influence was between two and three times more powerful than the contralateral inhibitory influence. After bilateral labyrinthectomy as well as after unilateral labyrinthectomy, the resting activity of the second-order vestibular neurons returned to normal, reaching 20.8 ± 23.1 spikes/s 1 day after the lesion and 38.6 ± 21.1 spikes/s 1 wk after the lesion. From this fact, we concluded that the left-right asymmetries caused by a unilateral labyrinthectomy were not the error signals inducing the restoration of activity.


2019 ◽  
Vol 122 (2) ◽  
pp. 512-524 ◽  
Author(s):  
Amelia H. Gagliuso ◽  
Emily K. Chapman ◽  
Giorgio P. Martinelli ◽  
Gay R. Holstein

Anterograde and retrograde tract tracing were combined with neurotransmitter and modulator immunolabeling to identify the chemical anatomy of vestibular nuclear neurons with direct projections to the solitary nucleus in rats. Direct, sparsely branched but highly varicose axonal projections from neurons in the caudal vestibular nuclei to the solitary nucleus were observed. The vestibular neurons giving rise to these projections were predominantly located in ipsilateral medial vestibular nucleus. The cell bodies were intensely glutamate immunofluorescent, and their axonal processes contained vesicular glutamate transporter 2, supporting the interpretation that the cells utilize glutamate for neurotransmission. The glutamate-immunofluorescent, retrogradely filled vestibular cells also contained the neuromodulator imidazoleacetic acid ribotide, which is an endogenous CNS ligand that participates in blood pressure regulation. The vestibulo-solitary neurons were encapsulated by axo-somatic GABAergic terminals, suggesting that they are under tight inhibitory control. The results establish a chemoanatomical basis for transient vestibular activation of the output pathways from the caudal and intermediate regions of the solitary nucleus. In this way, changes in static head position and movement of the head in space may directly influence heart rate, blood pressure, respiration, as well as gastrointestinal motility. This would provide one anatomical explanation for the synchronous heart rate and blood pressure responses observed after peripheral vestibular activation, as well as disorders ranging from neurogenic orthostatic hypotension, postural orthostatic tachycardia syndrome, and vasovagal syncope to the nausea and vomiting associated with motion sickness. NEW & NOTEWORTHY Vestibular neurons with direct projections to the solitary nucleus utilize glutamate for neurotransmission, modulated by imidazoleacetic acid ribotide. This is the first direct demonstration of the chemical neuroanatomy of the vestibulo-solitary pathway.


1987 ◽  
Vol 58 (4) ◽  
pp. 700-718 ◽  
Author(s):  
J. M. Goldberg ◽  
S. M. Highstein ◽  
A. K. Moschovakis ◽  
C. Fernandez

1. The electrical excitability of vestibular nerve afferents is related to their discharge regularity (23). Irregular (I) afferents are more excitable than regular (R) afferents. We explored the possibility that the differences in electrical excitability could be used to determine the profile of monosynaptic inputs from the ipsilateral vestibular nerve (Vi) to secondary neurons of the vestibular nuclei. The growth of monosynaptic Vi excitatory postsynaptic potentials (EPSPs) as shock strength is increased should reflect the kinds of afferent input that a secondary neuron receives. We were particularly interested in seeing if cells in the vestibular nuclei could be distinguished as R or I neurons depending on whether they received predominantly regular or irregular inputs. Barbiturate-anesthetized squirrel monkeys were used. 2. Recordings were made from vestibular nerve afferents. Shock strength was expressed as multiples of T, the value needed to recruit 10% of the afferents or, as determined empirically, to evoke a detectable field potential in the vestibular nuclei. Most I afferents (85/87 = 98%) were recruited below 4 X T, whereas most R afferents (197/212 = 93%) were first activated above 4 X T. The relation between latent period and electrical excitability was flat for units with thresholds in the range 1-4 X T. Latent periods increased for units with higher thresholds, especially those first activated above 8 x T. The threshold differences between I and R afferents are maximal if the shock falls at approximately half the mean interval after a naturally occurring action potential. The same results were obtained by having each unit fire to a maximal (16-32 X T) conditioning shock and then determining the threshold to a test shock presented 4 ms later. The latter stimulus configuration was used to study the Vi monosynaptic inputs to secondary neurons. The test shock was raised by successive doublings from 1 X T to the strength of the conditioning shock (16-32 X T). 3. Intracellular recordings were made from neurons located in the superior vestibular nucleus or the rostral parts of the medical or lateral vestibular nuclei. Amplitudes and latent periods of Vi EPSPs were measured from averages of several repetitions of each stimulus pair. Each EPSP was calculated by subtracting the extracellular from the intracellular averaged response. Of the 122 neurons sampled, 115 were judged to be monosynaptically related to the ipsilateral vestibular nerve because their Vi EPSPs had latent periods in the range of 0.7-1.4 ms.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 74 (5) ◽  
pp. 2087-2099 ◽  
Author(s):  
L. Ris ◽  
C. de Waele ◽  
M. Serafin ◽  
P. P. Vidal ◽  
E. Godaux

1. Neuronal activity was investigated in the left superior vestibular nucleus (SVN), lateral vestibular nucleus (LVN), and rostral part of the medial vestibular nucleus (MVN) in the alert guinea pig after a unilateral (left) labyrinthectomy was performed. Vestibular neurons were recorded either immediately (just-postoperative group, n = 6) or 1 wk after labyrinthectomy (1-wk-postoperative group, n = 6) and compared with the activity recorded in intact animals (control group, n = 6). 2. Animals were prepared for extracellular recording of single-unit activity and for eye movement recording (scleral search coil technique). To enable stimulation of the left vestibular nerve, bipolar silver ball electrodes were chronically implanted either in contact with the bony labyrinth in the control group or close to the stump of the vestibular nerve after labyrinthectomy. Complete labyrinthectomy was performed under halothane anesthesia. 3. The criterion used to select vestibular neurons for analysis was their recruitment by an electric shock on the vestibular nerve. Of the 589 recorded neurons, 424, defined as second-order vestibular neurons, were recruited at monosynaptic latencies (0.85-1.15 ms) and 165 were recruited at polysynaptic latencies. One hundred three second-order vestibular neurons were recorded in the control group, 173 in the just-postoperative group, and 148 in the 1-wk-postoperative group. 4. The activity of the electrically recruited neurons was recorded during sinusoidal horizontal head rotation in the dark (0.3 Hz, 40 degrees/s peak velocity). The behavior of the neurons was analyzed by plotting their firing rate against head velocity. The Y-intercept of the regression line was used to express spontaneous firing rate (resting discharge), and its slope was used to express the sensitivity of the neuron-to-head velocity. 5. In the absence of statistically significant difference between the characteristics of the neuronal discharge of the second-order vestibular neurons recorded in the SVN, LVN, and rostral MVN, the data were pooled. The Resting discharge of these cells amounted to 41.0 +/- 24.7 (SD) spikes/s in the control state, fell to 7.2 +/- 13.9 spikes/s just after labyrinthectomy, and completely returned to normal values 1 wk after surgery (42.5 +/- 21.6 spikes/s). Among the monosynaptically recruited neurons, the percentage of silent units was 0% in the control group, 69% in the just-postoperative group, and 0% in the 1-wk-postoperative group. 6. By contrast, the sensitivity to head velocity of the second-order vestibular neurons, which was 0.69 +/- 0.48 (SD) spikes.s-1/deg.s-1 in the control state and which fell to 0.03 +/- 0.11 spikes.s-1/deg.s-1 just after labyrinthectomy, remained low 1 wk after injury (0.21 +/- 0.26 spikes.s-1/deg.s-1). Moreover, the slight recovery of sensitivity to head rotation was due only to units behaving as type II neurons. 7. The mean resting discharge of the polysynaptically recruited neurons (pooled from the 3 explored nuclei) was 31.6 +/- 19.3 spikes/s in the control group. It decreased to 11.6 +/- 12.1 spikes/s in the just-postoperative group and recovered to 39.8 +/- 20.2 spikes/s in the 1-wk-postoperative group. No neuron was silent at rest either in the control group or in the 1-wk-postoperative group. Just after labyrinthectomy, 35% of the neurons had a null resting activity. The mean sensitivity to head velocity of these neurons was 0.55 +/- 0.42 spikes.s-1/deg.s-1 in the control group. It decreased to 0.05 +/- 0.12 spikes.s-1/deg.s-1 in the just-postoperative group and recovered to 0.22 +/- 0.17 spikes.s-1/deg.s-1 in the 1-wk-postoperative group. 8. We conclude that, at least in the guinea pig, the restoration of the spontaneous activity of the deafferented neurons is complete 1 wk after a unilateral labyrinthectomy and thus probably plays an important role in vestibular compensation...


2002 ◽  
Vol 88 (5) ◽  
pp. 2287-2301 ◽  
Author(s):  
H. Straka ◽  
S. Holler ◽  
F. Goto

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.


1996 ◽  
Vol 199 (3) ◽  
pp. 673-681 ◽  
Author(s):  
G Hjelmstad ◽  
G Parks ◽  
D Bodznick

The dorsal granular ridge (DGR) of the elasmobranch vestibulolateral cerebellum is the source of a parallel fiber projection to the electrosensory dorsal nucleus. We report that the DGR in Raja erinacea contains a large percentage of units with activity modulated by the animal's own ventilation. These include propriosensory and electrosensory units, responding to either ventilatory movements or the resulting electroreceptive reafference, and an additional population of units in which activity is phase-locked to the ventilatory motor commands even in animals paralyzed to block all ventilatory movements. A principal function of processing in the dorsal nucleus is the elimination of ventilatory noise in second-order electrosensory neurons. The existence of these ventilatory motor corollary discharge units, along with other DGR units responsive to ventilatory movements, suggests that the parallel fiber projection is involved in the noise cancellation mechanisms.


1992 ◽  
Vol 68 (2) ◽  
pp. 471-484 ◽  
Author(s):  
R. Boyle ◽  
J. M. Goldberg ◽  
S. M. Highstein

1. A previous study measured the relative contributions made by regularly and irregularly discharging afferents to the monosynaptic vestibular nerve (Vi) input of individual secondary neurons located in and around the superior vestibular nucleus of barbiturate-anesthetized squirrel monkeys. Here, the analysis is extended to more caudal regions of the vestibular nuclei, which are a major source of both vestibuloocular and vestibulospinal pathways. As in the previous study, antidromic stimulation techniques are used to classify secondary neurons as oculomotor or spinal projecting. In addition, spinal-projecting neurons are distinguished by their descending pathways, their termination levels in the spinal cord, and their collateral projections to the IIIrd nucleus. 2. Monosynaptic excitatory postsynaptic potentials (EPSPs) were recorded intracellularly from secondary neurons as shocks of increasing strength were applied to Vi. Shocks were normalized in terms of the threshold (T) required to evoke field potentials in the vestibular nuclei. As shown previously, the relative contribution of irregular afferents to the total monosynaptic Vi input of each secondary neuron can be expressed as a %I index, the ratio (x100) of the relative sizes of the EPSPs evoked by shocks of 4 x T and 16 x T. 3. Antidromic stimulation was used to type secondary neurons as 1) medial vestibulospinal tract (MVST) cells projecting to spinal segments C1 or C6; 2) lateral vestibulospinal tract (LVST) cells projecting to C1, C6; or L1; 3) vestibulooculo-collic (VOC) cells projecting both to the IIIrd nucleus and by way of the MVST to C1 or C6; and 4) vestibuloocular (VOR) neurons projecting to the IIIrd nucleus but not to the spinal cord. Most of the neurons were located in the lateral vestibular nucleus (LV), including its dorsal (dLV) and ventral (vLV) divisions, and adjacent parts of the medial (MV) and descending nuclei (DV). Cells receiving quite different proportions of their direct inputs from regular and irregular afferents were intermingled in all regions explored. 4. LVST neurons are restricted to LV and DV and show a somatotopic organization. Those destined for the cervical and thoracic cord come from vLV, from a transition zone between vLV and DV, and to a lesser extent from dLV. Lumbar-projecting neurons are located more dorsally in dLV and more caudally in DV. MVST neurons reside in MV and in the vLV-DV transition zone.(ABSTRACT TRUNCATED AT 400 WORDS)


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