Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey. I. An electrophysiological analysis

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)

1987 ◽  
Vol 58 (4) ◽  
pp. 719-738 ◽  
Author(s):  
S. M. Highstein ◽  
J. M. Goldberg ◽  
A. K. Moschovakis ◽  
C. Fernandez

1. Intracellular recordings were made from secondary neurons in the vestibular nuclei of barbiturate-anesthetized squirrel monkeys. Monosynaptic excitatory postsynaptic potentials (EPSPs) evoked by stimulation of the ipsilateral vestibular nerve (Vi) were measured. An electrophysiological paradigm, described in the preceding paper (26), was used to determine the proportion of irregularly (I) and regularly (R) discharging Vi afferents making direct connections with individual secondary neurons. The results were expressed as a % I index, an estimate for each neuron of the percentage of the total Vi monosynaptic input that was derived from I afferents. The secondary neurons were also classified as I, R, or M cells, depending on whether they received their direct Vi inputs predominantly from I or R afferents or else from a mixture (M) of both kinds of Vi fibers. The neurons were located in the superior vestibular nucleus (SVN) or in the rostral parts of the medical or lateral (LVN) vestibular nuclei. 2. Antidromic activation or reconstruction of axonal trajectories after intrasomatic injection of horseradish peroxidase (HRP) was used to identify three classes of secondary neurons in terms of their output pathways: 1) cerebellar-projecting (Fl) cells innervating the flocculus (n = 26); 2) rostrally projecting (Oc) cells whose axons ascended toward the oculomotor (IIIrd) nucleus (n = 27); and 3) caudally projecting (Sp) cells with axons descending toward the spinal cord (n = 13). Two additional neurons, out of 21 tested, could be antidromically activated both from the level of the IIIrd nucleus and from the spinal cord. 3. The Vi inputs to the various classes of relay neurons differed. As a class, Oc neurons received the most regular inputs. Sp neurons had more irregular inputs. Fl neurons were heterogeneous with similar numbers of R, M, and I neurons. The mean values (+/- SD) of the % I index for the Oc, Fl, and Sp neurons were 34.7 +/- 24.7, 51.9 +/- 30.4, and 61.8 +/- 18.0%, respectively. Only the Oc neurons had a % I index that was similar to the proportion of I afferents (34%) in the vestibular nerve (cf. Ref. 26). 4. The commissural inputs from the contralateral vestibular nerve (Vc) also differed for the three projection classes. Commissural inhibition was most common in Fl cells: 22/25 (88%) of the neurons had Vc inhibitory postsynaptic potentials (IPSPs) and 1/25 (4%) had a Vc EPSP. In contrast, Vc inputs were only observed in approximately half the Oc and Sp neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


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)


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.


1976 ◽  
Vol 39 (2) ◽  
pp. 301-310 ◽  
Author(s):  
V. J. Wilson ◽  
M. Maeda ◽  
J. I. Franck ◽  
H. Shimazu

In five decerebrate cats and in two under N2O-O2 anesthesia, a bipolar electrode array was inserted into a granular layer in the rostral flocculus. At this location MF field potentials were evoked by stimulation of the ipsilateral vestibular nerve and of the C2 dorsal root ganglion. Stimulation through the array was used to fire brain stem neurons antidromically. The activity of these neurons was recorded extracellularly with glass microelectrodes. Stimulation of the C2 dorsal root ganglion evoked in the caudal lateral brain stem a field potential caused by the arrival of impulses in primary afferent fibers. Cells projecting to the flocculus also responded to the stimulus, usually monosynaptically. These neurons were fired by stimulation of the area of the atlantoaxial joint. They did not respond to stimulation of the contralateral C2 dorsal root ganglion, and responded only rarely to stimulation of the dorsal rami of the C2 and C3 spinal nerves. Stimulation of the vestibular nerve was ineffective. Another group of cells projecting to the flocculus was fired at short latency by stimulation of the ipsilateral vestibular nerve. These neurons were usually inhibited by stimulation of the contralateral vestibular nerve. They were not affected by stimulation of any neck afferents. The location of many recording locations was identified by means of fast green dye marks. Most neurons relaying neck activity were in group x of Brodal and Pompeiano (4), a few were in the external cuneate nucleus, and one was in the descending vestibular nucleus. Neurons relaying labyrinthine activity were in the descending vestibular nucleus; one was found in the medial nucleus, in which tracks were made only rarely. There are two parallel pathways relaying neck and labyrinthine activity to the flocculus. While they are separate at the level of the brain stem, they converge in the same rostral areas of the flocculus. The neck afferent information may be required for proper performance of the flocculus in eye-movement control.


1984 ◽  
Vol 51 (6) ◽  
pp. 1236-1256 ◽  
Author(s):  
J. M. Goldberg ◽  
C. E. Smith ◽  
C. Fernandez

Most vestibular nerve afferents can be classified as regularly or irregularly discharging. Two factors are theoretically identified as being potentially responsible for differences in discharge regularity. The first, ascribable to synaptic noise, is the variance (sigma v2) characterizing the transmembrane voltage fluctuations of the axon's spike trigger site, i.e., the place where impulses normally arise. The second factor is the slope (dmuv/dt) of the trigger site's postspike recovery function. Were (dmuv/dt) a major determinant of discharge regularity, the theory predicts that the more irregular the discharge of a unit, the greater should be its sensitivity to externally applied galvanic currents and the faster should be the postspike recovery of its electrical excitability. The predictions would not hold if differences in the discharge regularity between units largely reflected variations in sigma v. To test these predictions, the responses of vestibular nerve afferents to externally applied galvanic currents were studied in the barbiturate-anesthetized squirrel monkey. Current steps of 5-s duration and short (50 microsecond) shocks were delivered by way of the perilymphatic space of the vestibule. Results were similar regardless of which end organ an afferent innervated. The regularity of discharge of each unit was expressed by a normalized coefficient of variation (CV*). The galvanic sensitivity (beta p) of a unit, measured from its response to current steps, was linearly related to discharge regularity (CV*), there being approximately 20-fold variations in both variables across the afferent population. Various geometric factors--including fiber diameter, position of individual axons within the various nerve branches, and the configuration of unmyelinated processes within the sensory epithelium--are unlikely to have made a major contribution to the positive relation between beta P and CV*. The postspike recovery of electrical excitability was measured as response thresholds to shocks, synchronized to follow naturally occurring impulses at several different delays. Recovery in irregular units was more rapid than in regular units. Evidence is presented that externally applied currents acted at the spike trigger site rather than elsewhere in the sensory transduction process. We argue that the irregular discharge of some vestibular afferents offers no functional advantage in the encoding and transmission of sensory information. Rather, the irregularity of discharge is better viewed as a consequence of the enhanced sensitivity of these units to depolarizing influences, including afferent and efferent synaptic inputs.


2007 ◽  
Vol 98 (6) ◽  
pp. 3197-3205 ◽  
Author(s):  
Aizhen Yang ◽  
Timothy E. Hullar

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.


2009 ◽  
Vol 101 (4) ◽  
pp. 1921-1931 ◽  
Author(s):  
Vladyslav V. Vyazovskiy ◽  
Ugo Faraguna ◽  
Chiara Cirelli ◽  
Giulio Tononi

In humans, non-rapid eye movement (NREM) sleep slow waves occur not only spontaneously but can also be induced by transcranial magnetic stimulation. Here we investigated whether slow waves can also be induced by intracortical electrical stimulation during sleep in rats. Intracortical local field potential (LFP) recordings were obtained from several cortical locations while the frontal or the parietal area was stimulated intracortically with brief (0.1 ms) electrical pulses. Recordings were performed in early sleep (1st 2–3 h after light onset) and late sleep (6–8 h after light onset). The stimuli reliably triggered LFP potentials that were visually indistinguishable from naturally occurring slow waves. The induced slow waves shared the following features with spontaneous slow waves: they were followed by spindling activity in the same frequency range (∼15 Hz) as spontaneously occurring sleep spindles; they propagated through the neocortex from the area of the stimulation; and compared with late sleep, waves triggered during early sleep were larger, had steeper slopes and fewer multipeaks. Peristimulus background spontaneous activity had a profound influence on the amplitude of the induced slow waves: they were virtually absent if the stimulus was delivered immediately after the spontaneous slow wave. These results show that in the rat a volley of electrical activity that is sufficiently strong to excite and recruit a large cortical neuronal population is capable of inducing slow waves during natural sleep.


2018 ◽  
Vol 119 (1) ◽  
pp. 73-83 ◽  
Author(s):  
Shawn D. Newlands ◽  
Ben Abbatematteo ◽  
Min Wei ◽  
Laurel H. Carney ◽  
Hongge Luan

Roughly half of all vestibular nucleus neurons without eye movement sensitivity respond to both angular rotation and linear acceleration. Linear acceleration signals arise from otolith organs, and rotation signals arise from semicircular canals. In the vestibular nerve, these signals are carried by different afferents. Vestibular nucleus neurons represent the first point of convergence for these distinct sensory signals. This study systematically evaluated how rotational and translational signals interact in single neurons in the vestibular nuclei: multisensory integration at the first opportunity for convergence between these two independent vestibular sensory signals. Single-unit recordings were made from the vestibular nuclei of awake macaques during yaw rotation, translation in the horizontal plane, and combinations of rotation and translation at different frequencies. The overall response magnitude of the combined translation and rotation was generally less than the sum of the magnitudes in responses to the stimuli applied independently. However, we found that under conditions in which the peaks of the rotational and translational responses were coincident these signals were approximately additive. With presentation of rotation and translation at different frequencies, rotation was attenuated more than translation, regardless of which was at a higher frequency. These data suggest a nonlinear interaction between these two sensory modalities in the vestibular nuclei, in which coincident peak responses are proportionally stronger than other, off-peak interactions. These results are similar to those reported for other forms of multisensory integration, such as audio-visual integration in the superior colliculus. NEW & NOTEWORTHY This is the first study to systematically explore the interaction of rotational and translational signals in the vestibular nuclei through independent manipulation. The results of this study demonstrate nonlinear integration leading to maximum response amplitude when the timing and direction of peak rotational and translational responses are coincident.


1996 ◽  
Vol 76 (4) ◽  
pp. 2439-2446 ◽  
Author(s):  
N. Isu ◽  
D. B. Thomson ◽  
V. J. Wilson

1. Previous studies of vestibular effects on the upper cervical cord have concentrated on the lateral and medial vestibulospinal tracts and on the actions that they exert on neck motoneurons and other neurons in the ventral horn. It is known, however, that both the rostral and the caudal areas of the vestibular nuclei (VN) give rise to axons that are located in the dorsal and dorsolateral funiculi and that terminate in the dorsal horn. A primary goal of our experiments was to investigate the effect of VN stimulation on neurons dorsal to lamina VII. 2. In decerebrate cats with the caudal cerebellar vermis removed, we stimulated different areas of the VN with an array of electrode. The area of stimulation extended from the caudal tip of the descending nucleus to Deiters' nucleus, and was divided into rostral and caudal halves with the use of the descending nucleus as a reference. For control purposes some stimulating points were placed in the external cuneate nucleus and restiform body. 3. We tested the effects of VN stimulation on spontaneously firing neurons in the ipsilateral C2 and C3 segments. For purposes of classification the gray matter was divided into four zones corresponding approximately to laminae 1-IV, V-VI, VII, and VIII of Rexed. Overall, the activity of 39 of 84 neurons was influenced from one or more stimulating sites. For six cells there was some possibility of current spread to the external cuneate nucleus or to the underlying reticular formation. 4. VN-evoked effects could consist of facilitation, or, less often, inhibition. In the majority of facilitated neurons conditioning stimuli evoked a synchronized, short-latency, increase in firing probability. When evoked by single stimuli this facilitation was considered monosynaptic. Facilitation that was diffuse, or that was only evoked by two or more stimuli, presumably involved more complex pathways. The latency of inhibition could not be measured, but was short. 5. Stimulation of either the rostral or caudal VN had no effect on neurons in laminae I-IV. Electrodes placed rostrally had little effect on neurons in laminae V-VI, but influenced more than half the neurons in laminae VII-VIII. Conversely, electrodes placed caudally were most effective on cells in laminae V-VII, although they also influenced some neurons in lamina VIII. 6. Stimulation of the dorsal rami influenced most neurons in laminae V-VI, and about a quarter of the neurons in laminae VII-VIII. When tested, there was often convergence between vestibulospinal and peripheral inputs. 7. Our results provide physiological evidence that vestibulospinal fibers influence neurons not only in laminae VII and VIII, but also as far dorsally as lamina V. Fibers that influence neurons in laminae V and VI originate primarily in the caudal areas of the VN. As suggested previously on anatomic grounds, the projection to the dorsal laminae, which is predominantly facilitatory, often converges with afferent input and can therefore modulate its influence on spinal neurons.


2007 ◽  
Vol 97 (6) ◽  
pp. 3986-3996 ◽  
Author(s):  
Aryn H. Gittis ◽  
Sascha du Lac

Neural circuits are composed of diverse cell types, the firing properties of which reflect their intrinsic ionic currents. GABAergic and non-GABAergic neurons in the medial vestibular nuclei, identified in GIN and YFP-16 lines of transgenic mice, respectively, exhibit different firing properties in brain slices. The intrinsic ionic currents of these cell types were investigated in acutely dissociated neurons from 3- to 4-wk-old mice, where differences in spontaneous firing and action potential parameters observed in slice preparations are preserved. Both GIN and YFP-16 neurons express a combination of four major outward currents: Ca2+-dependent K+ currents ( IKCa), 1 mM TEA-sensitive delayed rectifier K+ currents ( I1TEA), 10 mM TEA-sensitive delayed rectifier K+ currents ( I10TEA), and A-type K+ currents ( IA). The balance of these currents varied across cells, with GIN neurons tending to express proportionately more IKCa and IA, and YFP-16 neurons tending to express proportionately more I1TEA and I10TEA. Correlations in charge densities suggested that several currents were coregulated. Variations in the kinetics and density of I1TEA could account for differences in repolarization rates observed both within and between cell types. These data indicate that diversity in the firing properties of GABAergic and non-GABAergic vestibular nucleus neurons arises from graded differences in the balance and kinetics of ionic currents.


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