Peripheral innervation patterns of vestibular nerve afferents in the bullfrog utriculus

1994 ◽  
Vol 342 (2) ◽  
pp. 279-298 ◽  
Author(s):  
R. A. Baird ◽  
N. R. Schuff
Keyword(s):  
Vestibular Nerve ◽  
Peripheral Innervation ◽  
Innervation Patterns ◽  
Vestibular Nerve Afferents

The vestibular nerve of the chinchilla. V. Relation between afferent discharge properties and peripheral innervation patterns in the utricular macula

1990 ◽  
Vol 63 (4) ◽  
pp. 791-804 ◽  
Author(s):  
J. M. Goldberg ◽  
G. Desmadryl ◽  
R. A. Baird ◽  
C. Fernandez
Keyword(s):  
Lucifer Yellow ◽  
Small Diameter ◽  
Sampling Bias ◽  
Vestibular Nerve ◽  
Strongly Correlated ◽  
Utricular Macula ◽  
Peripheral Innervation ◽  
Physiological Properties ◽  
Innervation Patterns ◽  
Discharge Patterns

1. The relation between the discharge properties of utricular afferents and their peripheral innervation patterns was studied in the chinchilla by the use of intra-axonal labeling techniques. Fifty-three physiologically characterized units were injected with horseradish peroxidase (HRP) or lucifer yellow CH (LY) and their labeled processes were traced to the utricular macula. For most labeled neurons, the discharge regularity, background discharge, and sensitivity to externally applied galvanic currents were determined, as were the gain (g2 Hz) and phase (phi 2 Hz) of the response to 2-Hz sinusoidal linear forces. Terminal fields were reconstructed and fibers were classified as calyx (n = 13) or dimorphic units (n = 40). No bouton units were recovered. Calyx units were confined to the striola. Dimorphic units were located in the striola (n = 8), the juxtastriola (n = 7), or the peripheral extrastriola (n = 25). 2. To determine whether the intra-axonal sample was representative, the physiological properties of labeled utricular units were compared with those of a larger sample of extracellularly recorded units. A comparison was also made between the morphology of intra-axonally labeled units and those labeled by the extracellular injection of HRP into the vestibular nerve. Most of the discrepancies between the intra-axonal and either extracellular sample can be explained by assuming that small-diameter fibers are underrepresented in the former sample. Dimorphic fibers labeled intra-axonally had more bouton endings and larger terminal trees than did those labeled extracellularly. The latter differences may reflect a sampling bias in the extracellular material. 3. Calyx units were irregularly discharging. The discharge regularity of dimorphic units was related to their macular locations. Only 1/8 dimorphic units in the striola was regularly discharging. The ratio increases to 3/7 in the juxtastriola and to 23/25 in the peripheral extrastriola. Among dimorphic units, there is a tendency for irregularly discharging afferents to have fewer bouton endings. The trend is far from perfect because it is possible to pick a subsample of dimorphic units that have similar numbers of boutons and, yet, have discharge patterns that range from regular to irregular. 4. Published morphological polarization maps can be used to predict the excitatory tilt directions of a unit from its macular location. Predictions were confirmed in 39/41 labeled afferents. 5. The galvanic sensitivity (beta *) of an afferent, irrespective of its peripheral innervation pattern or its epithelial location, was strongly correlated with a normalized coefficient of variation (CV*).(ABSTRACT TRUNCATED AT 400 WORDS)

The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals

1988 ◽  
Vol 60 (1) ◽  
pp. 182-203 ◽  
Author(s):  
R. A. Baird ◽  
G. Desmadryl ◽  
C. Fernandez ◽  
J. M. Goldberg
Keyword(s):  
Lucifer Yellow ◽  
Discharge Rate ◽  
Small Diameter ◽  
Semicircular Canals ◽  
Preceding Paper ◽  
Vestibular Nerve ◽  
Response Properties ◽  
Peripheral Innervation ◽  
Innervation Patterns ◽  
The One

1. The relation between the response properties of semicircular canal afferents and their peripheral innervation patterns was studied by the use of intra-axonal labeling techniques. Fifty physiologically characterized units were injected with horseradish peroxidase (HRP) or Lucifer yellow CH (LY) and their processes were traced to the crista. The resting discharge, discharge regularity, and responses to both externally applied galvanic currents and sinusoidal head rotations were determined for most neurons. Terminal fields were reconstructed and, as in the preceding paper, the fibers were classified as calyx, bouton, or dimorphic units. 2. To determine if the intra-axonal sample was representative, the physiological properties of the labeled units were compared with those of a sample of extracellularly recorded units. A comparison was also made between the morphology of the intra-axonal units and those labeled by extracellular injection of HRP into the vestibular nerve Most of the discrepancies between the intra-axonal and the two extracellular samples can be explained by assuming that small-diameter fibers are underrepresented in the former sample. 3. A normalized coefficient of variation (CV*), independent of discharge rate, was used to classify units as regular, intermediate, or irregular. The CV* ranged from 0.020 to 0.60. Regular units (CV* less than or equal to 0.10) outnumbered irregular units (CV* greater than or equal to 0.20) by an approximately 3:1 ratio and had higher resting discharges. 4. Calyx units were invariably irregular. The one recovered bouton unit was regular. The discharge regularity of dimorphic units was related to their epithelial location, with those found in the periphery of the crista having a more regular discharge than those located more centrally. Dimorphic units, even those with quite similar morphology, can differ in their discharge regularity. Calyx and dimorphic units, which differ in their morphology, can both be irregular. These observations imply that discharge regularity is not determined by the branching pattern of a fiber or the number and types of hair cells it contacts. 5. The galvanic sensitivity (beta*) of an afferent, irrespective of its peripheral innervation pattern, was strongly correlated with CV*. This is consistent with the notion that discharge regularity and galvanic sensitivity are causally related, both being determined by postspike recovery mechanisms of the afferent nerve terminal.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey. II. Correlation with output pathways of secondary neurons

1987 ◽  
Vol 58 (4) ◽  
pp. 719-738 ◽  
Author(s):  
S. M. Highstein ◽  
J. M. Goldberg ◽  
A. K. Moschovakis ◽  
C. Fernandez
Keyword(s):  
Spinal Cord ◽  
Vestibular Nucleus ◽  
Preceding Paper ◽  
Vestibular Nuclei ◽  
Vestibular Nerve ◽  
Antidromic Activation ◽  
Mean Values ◽  
Postsynaptic Potentials ◽  
The Mean ◽  
Vestibular Nerve Afferents

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)

scholarly journals Response of Vestibular Nerve Afferents Innervating Utricle and Saccule During Passive and Active Translations

2009 ◽  
Vol 101 (1) ◽  
pp. 141-149 ◽  
Author(s):  
Mohsen Jamali ◽  
Soroush G. Sadeghi ◽  
Kathleen E. Cullen
Keyword(s):  
Efference Copy ◽  
Vestibular Nerve ◽  
Whole Body ◽  
Response Dynamics ◽  
Efferent System ◽  
Perceptual Stability ◽  
Vestibular Nerve Afferents ◽  
Otolith System ◽  
Head Translation ◽  
Passive Movements

The distinction between sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. In this study, we investigated whether linear translations are encoded similarly during active and passive translations by the otolith system. Vestibular nerve afferents innervating the saccule or utricle were recorded in alert macaques. Single unit responses were compared during passive whole body, passive head-on-body, and active head-on-body translations (vertical, fore-aft, or lateral) to assess the relative influence of neck proprioceptive and efference copy-related signals on translational coding. The response dynamics of utricular and saccular afferents were comparable and similarly encoded head translation during passive whole body versus head-on-body translations. Furthermore, when monkeys produced active head-on-body translations with comparable dynamics, the responses of both regular and irregular afferents remained comparable to those recorded during passive movements. Our findings refute the proposal that neck proprioceptive and/or efference copy inputs coded by the efferent system function to modulate the responses of the otolith afferents during active movements. We conclude that the vestibular periphery provides faithful information about linear movements of the head in the space coordinates, regardless of whether they are self- or externally generated.

scholarly journals Efferent Inputs Are Required for Normal Function of Vestibular Nerve Afferents

2019 ◽  
Vol 39 (35) ◽  
pp. 6922-6935 ◽  
Author(s):  
Vishal Raghu ◽  
Richard Salvi ◽  
Soroush G. Sadeghi
Keyword(s):  
Normal Function ◽  
Vestibular Nerve ◽  
Vestibular Nerve Afferents

The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in the horizontal and superior semicircular canals

1988 ◽  
Vol 60 (1) ◽  
pp. 167-181 ◽  
Author(s):  
C. Fernandez ◽  
R. A. Baird ◽  
J. M. Goldberg
Keyword(s):  
Hair Cells ◽  
Afferent Fiber ◽  
Central Zone ◽  
Semicircular Canals ◽  
Peripheral Zone ◽  
Sensory Epithelium ◽  
Vestibular Nerve ◽  
Fiber Types ◽  
Peripheral Innervation ◽  
Numerous Type

1. Afferent fibers supplying the horizontal and superior semicircular canals of the chinchilla were labeled by extracellular injections of horseradish peroxidase (HRP) into the vestibular nerve. The arborizations of labeled fibers within the sensory epithelium were reconstructed from serial sections of the crista. 2. The sensory epithelium of the crista can be divided into central, intermediate, and peripheral zones of approximately equal areas. The three zones can be distinguished in normal material by the density of hair cells and by the morphology of calyx endings. 3. Labeled fibers supply either the canalicular or the utricular side of the crista. Axons seldom bifurcate below the basement membrane and they begin dividing into their terminal arborizations almost immediately upon entering the sensory epithelium. The arborizations are compact, seldom extending more than 50 micron from the parent axon. 4. Both calyx and bouton endings were labeled. Calyces can be simple or complex. Simple calyces innervate individual hair cells, whereas complex calyces supply two to three adjacent hair cells. Complex calyces are commonly found only in the central zone. Simple calyces and boutons are located in all regions of the epithelium. Calyces emerge from the parent axon or one of its thick branches. Boutons, whether en passant or terminal, are always located on thin processes. 5. Fibers were classified as calyx, bouton, or dimorphic. The first type only has calyx endings, the second only has bouton endings, and the third has both kinds of endings. Dimorphic units make up some 70% of the labeled fibers, bouton units some 20%, and calyx units some 10%. The three fiber types differ in the diameters of their parent axons and in the regions of the crista they supply. Axon diameters are largest for calyx units and smallest for bouton units. Calyx units are concentrated in the central zone of the crista, whereas bouton units are largely confined to the peripheral zone. Dimorphic units are seen throughout the sensory epithelium. 6. Calyx units are almost always unbranched and end as simple calyces or, less often, as complex calyces. The terminal arbors of bouton units consist of fine processes containing 15-80 endings. Dimorphic units vary in complexity from fibers with a single calyx and a few boutons to those with one to four calyces and more than 50 boutons. 7. The results emphasize the importance of dimorphic units, which were the most numerous type of afferent fiber labeled in this study and were the only units found to innervate all regions of the sensory epithelium.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Efferent-Mediated Responses in Vestibular Nerve Afferents of the Alert Macaque

2009 ◽  
Vol 101 (2) ◽  
pp. 988-1001 ◽  
Author(s):  
Soroush G. Sadeghi ◽  
Jay M. Goldberg ◽  
Lloyd B. Minor ◽  
Kathleen E. Cullen
Keyword(s):  
Rotational Velocity ◽  
Semicircular Canals ◽  
Macaque Monkey ◽  
Nerve Fibers ◽  
Vestibular Nerve ◽  
Vestibular Afferents ◽  
Motion Responses ◽  
Unilateral Labyrinthectomy ◽  
Vestibular Nerve Afferents

The peripheral vestibular organs have long been known to receive a bilateral efferent innervation from the brain stem. However, the functional role of the efferent vestibular system has remained elusive. In this study, we investigated efferent-mediated responses in vestibular afferents of alert behaving primates (macaque monkey). We found that efferent-mediated rotational responses could be obtained from vestibular nerve fibers innervating the semicircular canals after conventional afferent responses were nulled by placing the corresponding canal plane orthogonal to the plane of motion. Responses were type III, i.e., excitatory for rotational velocity trapezoids (peak velocity, 320°/s) in both directions of rotation, consistent with those previously reported in the decerebrate chinchilla. Responses consisted of both fast and slow components and were larger in irregular (∼10 spikes/s) than in regular afferents (∼2 spikes/s). Following unilateral labyrinthectomy (UL) on the side opposite the recording site, similar responses were obtained. To confirm the vestibular source of the efferent-mediated responses, the ipsilateral horizontal and posterior canals were plugged following the UL. Responses to high-velocity rotations were drastically reduced when the superior canal (SC), the only intact canal, was in its null position, compared with when the SC was pitched 50° upward from the null position. Our findings show that vestibular afferents in alert primates show efferent-mediated responses that are related to the discharge regularity of the afferent, are of vestibular origin, and can be the result of both afferent excitation and inhibition.

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