Saccular Nerve Research Articles

Convergence of the horizontal semicircular canal and otolith afferents on cat single vestibular neurons.

We studied the convergence of two afferent pairs of single vestibular neurons by selective stimulation of the horizontal semicircular canal (HC) and saccular (SAC) nerves, and the HC and utricular (UT) nerves in decerebrate cats. All recorded neurons were classified as vestibulospinal (VS), vestibulo-oculospinal (VOS) or vestibulo-ocular (VO), by antidromic stimulation from the oculomotor/trochlear nuclei and the spinal cord: neurons that could not be activated from any test sites were classified as vestibular (V) neurons. Of a total of 125 neurons activated by stimulation of the HC/SAC nerves, 21(17%) received convergent inputs. Twelve of 21 neurons received monosynaptic excitatory inputs from both nerves. About half (9/21, 43%) of the convergent neurons were classified as VS neurons, the majority of which descended through the ipsilateral lateral vestibulospinal tract (i-LVST). The HC/SAC convergent neurons were located in the rostral part of the descending, the medial and the caudal-ventral part of the lateral vestibular nucleus. In 80 neurons studied by stimulation of the HC/UT nerves, both inputs converged in 12 (15%) neurons, more than half of which were VS neurons. Eight of 12 convergent neurons received excitatory inputs followed by inhibition from both the HC and UT nerves. A few convergent neurons (3/12) projected to the oculomotor/trochlear nucleus. Half of the convergent and non-convergent VS neurons descended to the spinal cord through the i-LVST, and the only one VOS convergent neuron via the medial vestibulospinal tract. Most of the convergent neurons were located in the lateral, the rostral part of the descending and medial vestibular nucleus. The percentages of HC/SAC and HC/UT convergence were half those of the posterior semicircular canal (PC), PC/SAC (33%) and PC/UT (33%) convergence, respectively. The convergent neurons receiving the HC and otolith inputs may contribute at least partly to the vestibulocollic reflex.

Postoperative Vestibular-evoked Myogenic Potentials in Cases with Vestibular Schwannomas

Although still the subject of discussion, vestibular-evoked myogenic potentials (VEMPs) have been considered to reflect the function of the saccular and, more recently, the cochlear tracts. To accurately determine the precise afferent pathway carrying VEMPs, we studied the outcomes of VEMPs and other examinations in patients with unilateral vestibular schwannomas. Eleven patients with unilateral vestibular schwannomas resected using a middle cranial fossa approach were included in the study. Patients underwent pure-tone threshold audiometry, caloric tests and analysis of auditory brainstem responses (ABRs) and VEMPs pre- and postoperatively. The results were compared with those obtained in patients with intact superior or inferior vestibular and cochlear nerves. Among the 11 patients studied, 4 retained their VEMPs postoperatively. Three of the 10 patients with inferior vestibular schwannomas exhibited normal VEMPs, preserved hearing levels (20 dB HL) and anatomically intact superior vestibular nerves. In all of these cases, ABRs more closely correlated with VEMPs than with caloric responses. In one of the cases with inferior vestibular schwannomas, VEMPs were preserved postoperatively and VEMP latencies were shortened, which indicates the preoperative presence of a conduction block in either the cochlear or superior vestibular nerve. VEMPs may be conducted in both the superior vestibular and cochlear nerves, as well as in the inferior vestibular nerve. Thus, evaluation of saccular nerve function should be performed carefully, especially in cases where hearing is preserved. It appears that cochlear conduction may proceed along two pathways, one direct and the other via the brainstem, but this remains to be verified.

Efferent innervation in the goldfish saccule examined by acetylcholinesterase histochemistry

In contrast to the abundance of information available regarding the anatomy and physiology of afferents within the goldfish saccule, the efferent system of this auditory endorgan has been scarcely studied morphologically. In this study, acetylcholinesterase histochemistry with diaminobenzidine enhancement was used to describe the morphology of efferents. Under light microscopy, labeled fibers appeared in the distal portion of the saccular nerve, penetrated the basement membrane and formed a horizontal mesh-like plexus near the base of hair cells. Many vertical branchlets with terminal swellings protruded upward toward hair cells from the plexus. Under electron microscopy, dense extracellular labeling was present around efferent terminals, which often formed clusters on hair cells. Labeling was also present around unmyelinated fibers of passage within the sensory epithelium and the distal saccular nerve. These fibers contained coarse microtubules and small vesicles, and often ran in a bundle with other similar fibers. Based on their position within the epithelium, histochemistry and ultrastructural characteristics, these fibers were concluded to be efferents. These fibers became myelinated and unlabeled in the proximal saccular nerve. These results suggest that acetylcholinesterase can be a marker of entire distal unmyelinated portions of efferent fibers and demonstrated abundant efferent innervation in the goldfish saccule.

Commissural effects in the otolith system.

We examined whether otolith-activated second- and third-order vestibular nucleus neurons received commissural inhibition from the contralateral otolithic macula oriented in the same geometric plane. For this purpose we performed intracellular recording in vestibular nucleus neurons after stimulation of the ipsi- and contralateral utricular and saccular nerves. More than half (41/72) of the utricular-activated second-order vestibular nucleus neurons received commissural inhibition from the contralateral utricular nerve. The remaining neurons (31/72) showed no visible response to contralateral utricular nerve stimulation. About half (17/36) of utricular-activated third-order neurons also received commissural inhibition from the contralateral utricular nerve. Approximately 10% (7/67) of saccular-activated second-order vestibular neurons received polysynaptic commissural inhibition, whereas 16% (11/67) received commissural facilitation. The majority (49/67) of saccular second-order vestibular neurons, and almost all (22/23) third-order neurons, showed no visible response to stimulation of the contralateral saccular nerve. The present findings suggest that many utricular-activated vestibular nucleus neurons receive commissural inhibition, which may provide a mechanism for increasing the sensitivity of vestibular neurons to horizontal linear acceleration and lateral tilt of the head. Commissural inhibition in the saccular system was less prominent than in the utricular system.

Otolith and semicircular canal inputs to single vestibular neurons in cats.

Researchers studied the convergence of the vertical posterior semicircular canal (PC), saccular nerves (SAC), utricular nerves (UT), and horizontal semicircular canal nerves (HC) on single vestibular neurons. The vestibular neurons were categorized by their innervating targets. Vestibular neurons were classified as vestibulospinal proper neurons (VS), vestibulo-ocular proper neurons (VO), vestibulo-oculo-spinal neurons sending axon collaterals to the extraocular motoneuron pools and spinal cord (VOS), and vestibular nucleus neurons without axons to the oculomotor nuclei or the spinal cord (V). Results indicate that the percentage of convergence of VS neurons was higher that that of neurons sending axons to the oculomotor nuclei (VO and VOS). They conclude that the convergence of canal and otolith inputs likely contributes mainly to vestibulospinal reflexes by sending inputs to the neck and other muscles during head inclination, which creates the combined stimuli of angular and linear acceleration.

Postoperative Vestibular-evoked Myogenic Potentials in Cases with Vestibular Schwannomas

Although still the subject of discussion, vestibular-evoked myogenic potentials (VEMPs) have been considered to reflect the function of the saccular and, more recently, the cochlear tracts. To accurately determine the precise afferent pathway carrying VEMPs, we studied the outcomes of VEMPs and other examinations in patients with unilateral vestibular schwannomas. Eleven patients with unilateral vestibular schwannomas resected using a middle cranial fossa approach were included in the study. Patients underwent pure-tone threshold audiometry, caloric tests and analysis of auditory brainstem responses (ABRs) and VEMPs pre- and postoperatively. The results were compared with those obtained in patients with intact superior or inferior vestibular and cochlear nerves. Among the 11 patients studied, 4 retained their VEMPs postoperatively. Three of the 10 patients with inferior vestibular schwannomas exhibited normal VEMPs, preserved hearing levels (20 dB HL) and anatomically intact superior vestibular nerves. In all of these cases, ABRs more closely correlated with VEMPs than with caloric responses. In one of the cases with inferior vestibular schwannomas, VEMPs were preserved postoperatively and VEMP latencies were shortened, which indicates the preoperative presence of a conduction block in either the cochlear or superior vestibular nerve. VEMPs may be conducted in both the superior vestibular and cochlear nerves, as well as in the inferior vestibular nerve. Thus, evaluation of saccular nerve function should be performed carefully, especially in cases where hearing is preserved. It appears that cochlear conduction may proceed along two pathways, one direct and the other via the brainstem, but this remains to be verified.

Properties of utricular and saccular nerve-activated vestibulocerebellar neurons in cats.

Properties of otolith inputs to vestibulocerebellar neurons were investigated in 14 adult cats. In the vestibular nuclei, we recorded single-unit activities that responded orthodromically after stimulation of the utricular and/or saccular nerves and antidromically after stimulation of the cerebellum (uvula-nodulus and anterior vermis). Descending axonal projections to the spinal cord were also examined by antidromic stimulation of the caudal end of the C1 segment. Forty-seven otolith-activated neurons that projected to the uvula-nodulus were recorded. Thirteen (28%) of the 47 neurons received convergent inputs from the utriculus and sacculus. The remaining 34 (72%) vestibular neurons were non-convergent neurons: 18 (38%) received utricular input alone, and 16 (34%) received saccular input alone. Most (35/47) vestibulocerebellar neurons were located in the descending vestibular nucleus and only one of these projected to the spinal cord. Seven of the 47 vestibulocerebellar neurons were located in the lateral vestibular nucleus and most of these neurons projected to the spinal cord. The remaining neurons were located in group X (two neurons) and the superior vestibular nucleus (three neurons). In a different series of experiments, 37 otolith-activated vestibular neurons were tested to determine whether they projected to the uvula-nodulus and/or the anterior vermis. Nineteen of the 37 neurons projected to the anterior vermis, 13/37 projected to the uvula-nodulus, and 5/37 projected to both. The utricular and/or saccular nerve-activated vestibulocerebellar neurons projected to not only the uvulanodulus, but also to the anterior vermis. In summary, the results of this study showed that vestibular neurons receiving inputs from the utriculus and/or sacculus projected to the cerebellar cortex. This indirect otolith-cerebellar pathway terminated both in the anterior lobe and in the uvula/nodulus.

Saccular and utricular influences on sympathetic nerve activities in cats.

We studied the effects of stimulation of the utricular and saccular nerves on sympathetic nerve activity in decerebrated cats. Bipolar electrodes were fixed in place on the utricular and/or saccular nerve under visual observation; the other branches of the vestibular nerve were transected. Baroreceptors and vagus nerves were inactivated bilaterally so that inputs from baroreceptors and other visceral receptors did not influence the sympathetic nerve outflow. Postganglionic sympathetic nerve activity was recorded from the renal branch of the sympathetic nerve, which is known to be more sensitive to vestibular stimuli than other types of sympathetic fibers. With stimulation of either the saccular or utricular nerve at low stimulus intensity, a prominent inhibition followed by a rebound excitation was evoked on spontaneous renal nerve discharges. The latency of the inhibition ranged from 65 to 130 ms, and the duration of inhibitory responses was about 90-150 ms. An increase in stimulus intensity in both the saccular and utricular nerves induced inhibitory effects preceded by short-term excitation. The latency of this excitation, which was superimposed on the initial phase of the inhibitory responses, ranged from 55 to 90 ms.

Pressure and pressure-gradient sensitivity of the tadpole medulla

The dorsal medulla of anuran tadpoles undergoes significant anatomical reorganization over metamorphic development. To examine how functional properties alter in response to anatomical changes, we recorded single and multiple unit activity in the medulla of bullfrog tadpoles to a sinusoidal-oscillating dipole source that traversed the length of the animal’s body. This dipole stimulus has been used previously to distinguish between pressure-sensitive auditory responses in the saccular nerve of the goldfish and pressure-gradient lateral line responses in the lateral line nerves of goldfish and other teleost fish. Recording sites in the developing dorsal lateral nucleus showed pressure-type responses to dipole stimulation near the animal’s head and lung. Evidence for the role of the bronchial columella and the air-filled lungs acting as a sound pressure transducer in mediating these responses was equivocal. Recording sites in the lateral line nucleus and surrounding neuropil showed pressure-gradient-type responses to stimulation near identified lines of superficial neuromasts on the body or tail. These data show that dipole stimulation is effective in eliciting responses from the medulla, and can be used to elucidate changes in function as the lateral line system degenerates and an auditory system adapted to hearing airborne sounds develops.

Sacculo-ocular reflex connectivity in cats.

The otolith system contributes to the vestibulo-ocular reflexes (VOR) when the head moves linearly in the horizontal plane or tilts relative to gravity. The saccules are thought to detect predominantly accelerations along the gravity vector. Otolith-induced vertical eye movements following vertical linear accelerations are attributed to the saccules. However, information on the neural circuits of the sacculo-ocular system is limited, and the effects of saccular inputs on extraocular motoneurons remain unclear. In the present study, synaptic responses to saccular-nerve stimulation were recorded intracellularly from identified motoneurons of all twelve extraocular muscles. Experiments were successfully performed in eleven cats. Individual motoneurons of the twelve extraocular muscles--the bilateral superior recti (SR), inferior recti (IR), superior obliques (SO), inferior obliques (IO), lateral recti (LR), and medial recti (MR) were identified antidromically following bipolar stimulation of their respective nerves. The saccular nerve was selectively stimulated by a pair of tungsten electrodes after removing the utricular nerve and the ampullary nerves of the semicircular canals. Stimulus intensities were determined from the stimulus-response curves of vestibular N1 field potentials in order to avoid current spread. Intracellular recordings were performed from 129 extraocular motoneurons. The majority of the neurons showed no response to saccular-nerve stimulation. In 17 (30%) of 56 extraocular motoneurons related to vertical eye movements (bilateral SR and IR), depolarizing and/or hyperpolarizing postsynaptic potentials (PSPs) were observed in response to saccular-nerve stimulation. The latencies of PSPs ranged from 2.3 to 8.9 ms, indicating that the extraocular motoneurons received neither monosynaptic nor disynaptic inputs from saccular afferents. The majority of the latencies of the depolarization, including depolarization-hyperpolarization, were in the range of 2.3-3.3 ms. Latencies of hyperpolarizations were typically longer than those of depolarizations. Only one contralateral SO motoneuron of 43 recorded oblique extraocular motoneurons (bilateral SO and IO) showed a depolarization-hyperpolarization in response to saccular-nerve stimulation at a latency of 2.5 ms. None of 30 recorded horizontal extraocular motoneurons (bilateral LR and MR) responded to stimulation of the saccular nerve. The neural linkage in the sacculo-ocular system is relatively weak in comparison to the utriculo-ocular and sacculo-collic systems, suggesting that the role of the sacculo-ocular system in stabilizing eye position may be reduced when compared with utriculo-ocular and semi-circular canal-ocular reflexes.

Canal and otolith inputs to single vestibular neurons in cats.

Convergence of both afferents from the PC and saccular macula, and those from the PC and utricular macula on single vestibular neurons was noted by use of intercellular recording from vestibular neurons. Vestibular neurons were classified VO neurons (vestibulo-ocular proper neurons), VOS (Vestibulo-oculo-spinal neurons sending axon collaterals both to the extraocular motoneuron pools and to the spinal cord), VS neurons (vestibulospinal proper neurons) and V neurons (vestibular neurons without axons to the oculomotor nuclei or the spinal cord) on the basis of whether or not they responded antidromically to stimulation of the oculomotor nuclei and the spinal cord. Of the total 143 vestibular neurons recorded in the series of experiments on convergence of the PC and saccular afferents, 47 neurons (33%) were received inputs from both the PC and saccular nerves. Twenty-six of the 47 convergent neurons were identified as having the nature of VS neurons. Half (13/26) of those were activated monosynaptically from both the PC and saccular nerves. Only one saccular-activated neuron without PC inputs sent an axon to the oculomotor nuclei. In the other series of experiments on the convergence of the PC and utricular afferents, 41 (37%) of 111 vestibular neurons were proved to converge on inputs from both nerves. The majority (35/41) of the neurons received monosynaptic inputs from the PC nerve and polysynaptic EPSP-IPSP sequences from the utricular nerve, or vice versa. The ratio of PC-otolith convergent neurons among utricular-activated neurons (41/54, 76%) was higher than that among saccular activated neurons (47/88, 53%). The percentage of utricular alone neurons without PC inputs (13/111, 12%) was less than that of the saccular alone without PC inputs (41/145, 28%). In conclusion, the convergence of canal and otolith inputs likely contribute mainly to vestibulospinal reflexes including the vestibulocollic reflex, by sending inputs to the neck and other muscles during head inclination which creates the combined stimuli of angular and linear acceleration.

Saccular and utricular inputs to sternocleidomastoid motoneurons of decerebrate cats.

Connections from the otolithic organs to sternocleidomastoid (SCM) motoneurons were studied in 20 decerebrate cats. The electrical stimulation was selective for the saccular or the utricular nerves. Postsynaptic potentials were recorded from antidromically identified SCM motoneurons; these muscles participate mainly in neck rotation and flexion. Partial transections of the brainstem at the level of the obex were performed to identify the possible pathway from the otolithic organs to the SCM motoneurons. Saccular or utricular nerve stimulation mainly evoked inhibitory postsynaptic potentials (IPSPs) in the ipsilateral SCM motoneurons. Some of the sacculus-induced IPSPs were preceded by small-amplitude excitatory PSPs (EPSPs). The latencies of the PSPs ranged from 1.8 to 3.1 ms after saccular nerve stimulation and from 1.7 to 2.8 ms after utricular nerve stimulation, indicating that most of the ipsilateral connections were disynaptic. In the contralateral SCM motoneurons, saccular nerve stimulation had no or faint effects, whereas utricular nerve stimulation evoked EPSPs in about two-thirds of neurons, and no visible PSPs in about one-third of neurons. The latencies of the EPSPs ranged from 1.5 to 2.0 ms, indicating the disynaptic connection. Thus, the results suggest a difference between the two otolithic innervating patterns of SCM motoneurons. After transection of the medial vestibulospinal tract (MVST), saccular nerve stimulation did not evoke IPSPs at all in ipsilateral SCM motoneurons, but some (11/40) neurons showed small-amplitude EPSPs. Most (24/33) of the utricular-activated IPSPs disappeared after transection, whereas the other 9 neurons still indicated IPSPs. In the contralateral SCM motoneurons, no utricular-activated EPSPs were recorded after transection. These MVST transection results suggest that most of the otolith-SCM pathways are located in the MVST at the obex level. However, the results also suggest the possibility that other otolith-SCM pathways exist at the obex level.

In vitro and in vivo responses of saccular and caudal nucleus neurons in the grassfrog (Rana temporaria).

We present results from in vitro and in vivo studies of response properties of neurons in the saccular and caudal nuclei in the frog. In the in vitro studies the saccular nerve of the isolated brain was stimulated with electrical pulses. In the in vivo experiments, the neurons were stimulated by dorso-ventral vibrations of the intact animal. We identified six response types: (1) primary-like cells with short latencies and follow repetition rates up to 100 Hz; (2) phasic cells responding only to the first pulse in a train; (3) bursting cells firing several spikes in response to any stimulation; (4) late responders with very long latencies; (5) integrator cells showing facilitated responses, and (6) inhibitory cells inhibited by saccular nerve stimulation. The cells have comparable sensitivity and frequency characteristics to the primary fibres (BF 10-80 Hz, thresholds from 0.01 cm/s2) and enable a sophisticated analysis of vibrational stimuli.

Projections of primary afferents from regions of the saccule in toadfish ( Opsanus tau)

The hair cell orientation patterns present on the saccules of fishes may be important for encoding the direction of a sound source. This study was conducted to determine whether primary afferent projections to the medulla are organized by the best directions for the hair cells they innervate. The toadfish saccule has hair cells oriented primarily in the vertical plane: both the rostral and the caudal saccule have hair cell orientations sweeping from 0° to 45°, and the middle saccule has hair cells oriented at 90°. Fluorescent dextran amines were used singly and in combination to label regions of the saccular nerve innervating rostral, middle, and caudal saccule. The projections of those afferents were examined in detail in the anterior and descending octaval nuclei, which are auditory nuclei in this species. There was no evidence of topographic projections based on location along the length of the saccule or based on hair cell orientation. There was some evidence that parallel inputs are present from each region of the saccule examined, which may be based on the 180° opposition of hair cells found throughout the saccule; however, afferents from the rostral, middle, and caudal saccule appear to have overlapping projections to the anterior and descending octaval nuclei. These data suggest that in toadfish, calculations of the direction of the sound source may begin in either of these primary auditory nuclei by comparing afferent input from along the saccule.

Effect of temperature on electrical resonance in leopard frog saccular hair cells.

Leopard frog saccular hair cells exhibit an electrical resonance in response to a depolarizing stimulus that has been proposed to contribute to the tuning properties of the frog sacculus by acting as an electrical band-pass filter. With the whole cell patch-clamp technique, we have investigated the effect of temperature on electrical resonances in isolated saccular hair cells, and we have described the effects of temperature on the currents and channel kinetics underlying electrical resonance. A hair cell's onset resonant frequency in response to a constant depolarizing current pulse increases linearly with temperature at a rate of 11 Hz/1 degrees C, exhibiting a mean Q10 of 1.7 between 15 and 35 degrees C. However, offset resonant frequencies continue to double every 10 degrees C, exhibiting a mean Q10 of 2.1. If steady-state voltage during the stimulus is held constant, all oscillatory frequencies increase with a mean Q10 of 2.1. The average level of steady-state depolarization during a +150-pA depolarizing current pulse decreases with increasing temperature (-6 mV from 15 to 25 degrees C). This temperature-dependent reduction of the steady-state membrane potential causes a shift in the voltage-dependent channel kinetics to slower rates, thus reducing the apparent Q10 for onset resonant frequencies. The peak outward tail current and net steady-state outward current, which is the sum of a voltage-dependent inward calcium current (ICa) and an outward calcium-dependent potassium current (IK(Ca)), increase with temperature, exhibiting a mean Q10 of 1.7 between 15 and 25 degrees C. The activation rate (T1/2) of the outward current exhibits a mean Q10 of 2.3 between 15 and 25 degrees C, while the deactivation rate (taurel) exhibits a mean Q10 of 2.9 over the same temperature range. These results support previous models of the molecular determination of resonant frequency, which have proposed that a combination of IK(Ca) channel kinetics and the overall magnitude of the outward current are primarily responsible for determining the resonant frequency of an isolated hair cell. The robust temperature sensitivity of the hair cell receptor potential contrasts sharply with the temperature-insensitive tuning properties of in vivo saccular nerve fiber recordings. Possible explanations for this discrepancy are discussed.

Properties of saccular nerve-activated vestibulospinal neurons in cats.

Axonal pathways, projection levels, conduction velocities, and locations of the cell bodies of saccular nerve-activated vestibulospinal neurons were studied in decerebrated cats and anesthetized cats, using a collision test of orthodromic and antidromic spikes. The saccular nerve was selectively stimulated by bipolar tungsten electrodes. Three monopolar electrodes were inserted into the left and right lateral vestibulospinal tract (LVST) and medial vestibulospinal tract (MVST) of the C1 segment, to determine the pathway of axons. Three pairs of similar electrodes were positioned bilaterally in the C3-4, T1, and L3 segments to examine projection levels. Another monopolar electrode was placed in the oculomotor nucleus to determine whether saccular nerve-activated vestibulospinal neurons have branches ascending to the oculomotor nucleus. Of 145 vestibular neurons orthodromically activated by stimulation of the saccular nerve, 46 were activated from the C1 segment antidromically. Forty-three were second-order vestibulospinal neurons and 3 were third-order vestibulospinal neurons. Four saccular nerve-activated vestibulospinal neurons were also antidromically activated from the oculomotor nucleus. Sixty-three percent of the saccular nerve-activated vestibulospinal neurons descended through the MVST; one-third of these terminated in the upper cervical segments, one-third reached the lower cervical segments and the remaining one-third reached the upper thoracic segments. Thirty percent of the saccular nerve-activated vestibulospinal neurons descended through the ipsilateral LVST; most of these reached the upper thoracic segments. Seven percent of the saccular nerve-activated vestibulospinal neurons descended through the contralateral vestibulospinal tracts terminating in the upper cervical segments. Most of the saccular nerve-activated vestibulospinal neurons originated in the caudal part of the lateral nucleus and rostral part of the descending nucleus.

Excitatory and inhibitory inputs from saccular afferents to single vestibular neurons in the cat.

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.

Directional response properties of saccular afferents of the toadfish, Opsanus tau

The displacement sensitivity, frequency response, and directional response properties of primary saccular afferents of toadfish (Opsanus tau) were studied in response to a simulation of acoustic particle motion for which displacement magnitudes and directions were manipulated in azimuth and elevation. Stimuli were 50, 100, and 200 Hz sinusoidal, translatory oscillations of the animal at various axes in the horizontal and midsagittal planes. Thresholds in these planes defined a cell's characteristic axis (the axis having the lowest threshold) in spherical coordinates. Recordings were made from afferents in rostral, middle, and caudal bundles of the saccular nerve. The most sensitive saccular afferents responded with a phase-locked response to displacements as small as 0.1 nm. This sensitivity rivals that of the mammalian cochlea and is probably common to the sacculi and other otolith organs of most fishes. Most afferents showed lower thresholds at 100 Hz than at 50 or 200 Hz. Eighty percent of afferents have three-dimensional directional properties that would be expected if they innervated a group of hair cells having the same directional orientation on the saccular epithelium. Of the afferents that are not perfectly directional, most appear to innervate just two groups of hair cells having different orientations. The directional characteristics of afferents are qualitatively correlated with anatomically defined patterns of hair cell orientation on the saccule. In general, azimuths of best sensitivity tend to lie parallel to the plane of the otolith and sensory epithelium. Elevations of best sensitivity correspond well with hair cell orientation patterns in different regions of the saccular epithelium. Directional hearing in the horizontal plane probably depends upon the processing of interaural differences in overall response magnitude. These response differences arise from the gross orientations of the sacculi and are represented, in part, as time differences among nonspontaneous afferents that show level-dependent phase angles of synchronization. Directional hearing in the vertical plane may be derived from the processing of across-afferent profiles of activity within each saccule. Fishes were probably the first vertebrates to solve problems in sound source localization, and we suggest that their solutions formed a model for those of their terrestrial inheritors.

Sacculocollic reflex arcs in cats.

Neuronal connections and pathways underlying sacculocollic reflexes were studied by intracellular recordings from neck extensor and flexor motoneurons in decerebrate cat. Bipolar electrodes were placed within the left saccular nerve, whereas other branches of the vestibular nerve were removed in the inner ear. To prevent spread of stimulus current to other branches of the vestibular nerve, the saccular nerve and the electrodes were covered with warm semisolid paraffin-Vaseline mixture. Saccular nerve stimulation evoked disynaptic (1.8-3.0 ms) excitatory postsynaptic potentials (EPSPs) in ipsilateral neck extensor motoneurons and di- or trisynaptic (1.8-4.0 ms) EPSPs in contralateral neck extensor motoneurons, and di- and trisynaptic (1.7-3.6 ms) inhibitory postsynaptic potentials (IPSPs) in ipsilateral neck flexor motoneurons and trisynaptic (2.7-4.0 ms) IPSPs in contralateral neck flexor motoneurons. Ipsilateral inputs were about twice as strong as contralateral ones to both extensor and flexor motoneurons. To determine the pathways mediating this connectivity, the lateral part of the spinal cord containing the ipsilateral lateral vestibulospinal tract (i-LVST) or the central part of the spinal cord containing the medial vestibulospinal tracts (MVSTs) and possibly reticulospinal fibers (RSTs) were transected at the caudal end of the C1 segment. Subsequent renewed intracellular recordings following sacculus nerve stimulation indicated that the pathway from the saccular nerve to the ipsilateral neck extensor motoneurons projects though the i-LVST, whereas the pathways to the contralateral neck extensors and to the bilateral neck flexor motoneurons descend in the MVSTs/RSTs. Our data show that sacculo-neck reflex connections display a qualitatively bilaterally symmetrical innervation pattern with excitatory connections to both neck extensor motoneuron pools, and inhibitory connections to both neck flexor motoneuron pools. This bilateral organization contrasts with the unilateral innervation scheme of the utriculus system. These results suggest a different symmetry plane along which sacculus postural reflexes are organized, thus supplementing the reference planes of the utriculus system and allowing the gravistatic system to represent all three translational spatial degrees of freedom. We furthermore suggest that the sacculocollic reflex plays an important role in maintaining the relative position of the head and the body against the vertical linear acceleration of gravity.

Long-lasting depression of mauthner cell-initiated escape response produced by inhibitory long-term potentiation

Application of horseradish peroxidase (HRP) to the proximal end of the transected saccular nerve in the goldfish results in uptake by fibers projecting to the distal half of the Mauthner (M) cell's lateral dendrite. More discrete HRP injections reveal an organized projection from the saccular nerve onto the lateral dendrite, as small groups of stained fibers terminate there in restricted regions. The possibility that this represents a tonotopic projection onto the M-cell is considered.