Order Vestibular Neurons Research Articles

Intrinsic Neuronal Excitability: A Role in Homeostasis and Disease

Intrinsic Neuronal Excitability: A Role in Homeostasis and Disease

Signal processing in first- and second-order vestibular neurons

This symposium was held in Anaheim California, on February 8, 2010, at the 33rd annual Midwinter Meeting of the Association for Research in Otolaryngology (ARO). The meeting program and abstracts are published online (http://aro.org/abstracts/abstracts.html). Organized by Jay Goldberg and Kenna Peusner, the symposium was directed toward clinicians who want to bridge the gap between basic science and treating patients for vestibular disorders, vestibular neuroscientists using structural and functional approaches to understand the labyrinth and its central pathways at the system, cellular, and molecular levels, and auditory neuroscientists intrigued by the similarities and differences in signal processing in the two systems. This special issue contains those presentations on signal processing in second-order vestibular neurons and their connections. The articles underwent peer-review for this special issue. We would like to thank the Journal of Vestibular Research for the production of this special issue devoted to the symposium. The vestibular system demonstrates a remarkable plasticity in response to changing environmental demands [9] and to recover function after pathologies affecting the peripheral vestibular receptors on one side [16]. Second-order vestibular neurons are characterized by a high degree of plasticity in their connections with first-order vestibular neurons and nonlabyrinthine inputs (for review, see [20]). As demonstrated in this symposium, recent research has been directed toward defining synaptic transmission and ionic conductances involved in signal processing from the vestibular periphery to the first brain centers located in the vestibular nuclei. The experiments utilize multiple structural and functional approaches performed on intact animals, isolated vestibular circuits in culture, or brain slice preparations. The article by Beraneck and Straka entitled “Vestibular Signal Processing by Separate Sets of Neuronal Filters” reviews recent research on detecting static head position and head motion by the peripheral vestibular receptors and the activation of specific receptor areas by high or low frequency movements during locomotion. Vestibular nerve afferents convey the different dynamics of head motion in a wide range of frequencies to second–order vestibular neurons, which are equipped dynamically to process the signals [18]. From the firing patterns generated by second-order vestibular nuclei neurons, the authors propose that there are two different populations of vestibular nuclei neurons that process high or low frequency signals within two separate pathways [19]. Tonic-firing vestibular nuclei neurons process low frequency signals, and are well-suited for synaptic integration, whereas phasic-firing vestibular nuclei neurons process high frequency signals and are designed to detect events. This dual system may underlie the ability of the brain to distinguish between tilt and linear translation, or self-induced motion and passive body movements (for review, see [1]). Finally, differences in the dynamic properties between frog and mammalian vestibular nuclei neurons are discussed in relation to species-specific locomotor patterns.

末梢前庭器から前庭神経核へ―最近の知見―５．末梢前庭から前庭神経核への投射

Using intracellular staining with horseradish peroxidase (HRP), Sato et al. (1989) demonstrated the course and termination in the vestibular nuclei of electrophysiologically identified single axons originating from the three semicircular canals. All semicircular canal-activated afferents terminated on all vestibular nuclei. The morphology of physiologically identified otolith-activated afferents (Imagawa et al. 1995, 1998) and 2nd order vestibular neurons (Meng et al. 2002) was investigated by similar methodology with HRP. The ascending branches of otolith axons give off collaterals with boutons in the caudal part of the superior nucleus. The descending branches coursed caudally through the lateral part of the descending nucleus, and gave off collaterals with boutons in the lateral, descending and medial vestibular nuclei. In summary, our data now complete the catalogue of the morphology of individual primary neurons innervating vestibular end organs, i.e. the three canals and the two otolith orngas. As a whole, canal and otolith afferents basically project to the same vestibular nuclei, although there are noticeable quantitative differences. Otolith projections to areas outside the vestibu-lar nuclei where ipsilateral abducens nucleus and reticular formation are present are quite different (Uchino et al. 1994, 1996).The morphology of vestibular neurons was studied by similar methodology with HRP (See Wilson and Melvill Jones 1979). The otolith-activated 2nd order vestibular neurons were pyramidal, elongated and ovoidal in shape. Most of the labeled cells were medium to large. There was no apparent correlation between morphology and the different types of otolith- and canal-activated vestibular neurons. Thus, it seems likely that the functional type of vestibular neurons cannot be presumed on the basis of their morphology alone.

The differential response of astrocytes within the vestibular and cochlear nuclei following unilateral labyrinthectomy or vestibular afferent activity blockade by transtympanic tetrodotoxin injection in the rat

In this study, we investigated whether changes in the vestibular neuronal activity per se influence the pattern of astrocytes morphology, glial fibrillary acidic protein (GFAP) expression and ultimately their activation within the vestibular nuclei after unilateral transtympanic tetrodotoxin (TTX) injections and after unilateral inner ear lesion. The rationale was that, theoretically the noninvasive pharmacological functional blockade of peripheral vestibular inputs with TTX, allowed us to dissociate the signals exclusively related to the shutdown of the resting activity of the first-order vestibular neurons and from neuronal signals associated with trans-ganglionic changes in first order vestibular neurons induced by unilateral labyrinthectomy (UL). Since the cochlea was removed during the surgical procedure, we also studied the astrocytic reaction within the deafferented cochlear nuclei. No significant changes in the distribution or relative levels of GFAP mRNA expression, relative levels of GFAP protein or immunoreactivity for GFAP were found in the ipsilateral vestibular nuclei at any post-TTX injection times studied. In addition, no sign of microglia activation was observed. In contrast, a robust increase of the distribution and relative levels of GFAP mRNA expression, protein levels and immunoreactivity was observed in the deafferented vestibular and cochlear nuclei beginning at 1 day after inner ear lesion. GFAP mRNA expression and immunoreactivity in the cochlear nucleus was qualitatively stronger than in the ipsilateral vestibular nuclei. The results suggest that astrocyte activation in the vestibular nuclei is not related to drastic changes of vestibular nuclei neuronal activity per se. Early trans-ganglionic changes due to vestibular nerve dendrites lesion provoked by the mechanical destruction of vestibular receptors, most probably induced the glial reaction. Its functional role in the vestibular compensation process remains to be elucidated.

Development of the ear and of connections between the ear and the brain: is there a role for gravity?

This paper outlines the development of the gravistatic sensory system of the ear. First, evidence is presented that a genetic program, for which major transcription factors have already been identified using gene expression studies and targeted mutagenesis, governs the initial development of this system. Second, the formation of sensory neurons and their connections to the brain is described as revealed by tracing studies and genetic manipulations. It is concluded that the initial development of the connections of sensory neurons with mechanosensory transducers of the ear (the hair cells) and the targets in the brainstem (vestibular nuclei) is also dependent on fairly rigid genetic programs. During late embryonic and early postnatal development, however, sensory input appears to be used to fine-tune connections of these sensory neurons with the hair cells in the ear as well as with second order vestibular neurons in the brainstem. This phase is proposed to be critical for a proper calibration of the gravistatic information processing in the brain.

Central and Peripheral Components of Short Latency Vestibular Responses in the Chicken

Far-field recordings of short latency vestibular responses to pulsed cranial translation are composed of a series of positive and negative peaks occurring within 10 ms following stimulus onset. In the bird, these vestibular evoked potentials (VsEPs) can be recorded noninvasively and have been shown in the chicken and quail to depend strictly upon the activation of the vestibular component of the eighth nerve. The utility of the VsEP in the study of vestibular systems is dependent upon a clear understanding of the neural sources of response components. The primary aim of the current research in the chicken was to critically test the hypotheses that 1) responses are generated by both peripheral and central neurons and 2) peaks P1 and N1 originate from first order vestibular neurons, whereas later waves primarily depend on activity in higher order neurons. The principal strategy used here was to surgically isolate the eighth nerve as it enters the brainstem. Interruption of primary afferents of the eighth nerve in the brainstem substantially reduced or eliminated peaks beyond P2, whereas P1 and N1 were generally spared. Surgical sections that spared vestibular pathways had little effect on responses. The degree of change in response components beyond N1 was correlated with the extent of damage to central vestibular relays. These findings support the conclusion that responses are produced by both peripheral and central elements of the vestibular system. Further, response peaks later than N1 appear to be dependent upon central relays, whereas P1 and N1 reflect activity of the peripheral nerve. These findings clarify the roles of peripheral and central neurons in the generation of vestibular evoked potentials and provide the basis for a more useful and detailed interpretation of data from vestibular response testing.

Size-related properties of vestibular afferent fibers in the frog: Differential synaptic activation of N-methyl- d-aspartate and non- N-methyl- d-aspartate receptors

Vestibular afferent fibers exhibit a specific, cell size-related uptake of aspartate and glycine [Straka H. et al. (1995) Neuroscience 70, 685–696]. A similar, size-related coexistence of glycine and glutamate had been reported earlier for these fibers [Reichenberger I. and Dieringer N. (1994) J. comp. Neurol. 349, 603–614]. Taken together, these results suggest a size-related co-release of both amino acids and the activation of different glutamate receptors in second order vestibular neurons. To test this hypothesis we stimulated the VIIIth nerve and recorded the responses of central vestibular neurons in the isolated brainstem of frogs before and during the application of the N-methyl- d-aspartate antagonists (7-chlorokynurenic acid and d-(−)-2-amino-5-phosphonovaleric acid). The presence of either one of these antagonists provoked a dose-dependent and Mg 2+-sensitive partial block of the monosynaptic responses recorded extra- or intracellularly. This implies that afferent-evoked responses in central vestibular neurons are composed of N-methyl- d-aspartate and non- N-methyl- d-aspartate receptor-mediated components. In most of the intracellularly recorded neurons (21 out of 24) the relative amplitude of the N-methyl- d-aspartate receptor-mediated component decreased with an increase in stimulus intensity. Since electric stimulation recruits thick afferents at a lower current intensity than thin afferent fibers, our results imply a co-activation of N-methyl- d-aspartate and non- N-methyl- d-aspartate receptors by thick vestibular afferents. At a given stimulus intensity the amplitude of the N-methyl- d-aspartate receptor-mediated component differed between neurons. The results of this study extend the list of known anatomical, histochemical and physiological properties that distinguish thick from thinner vestibular afferent fibers. In spite of this detailed knowledge, however, the physiological role of thick vestibular afferents is so far unclear. The novel concept of a size-related co-activation of N-methyl- d-aspartate and non- N-methyl- d-aspartate receptors by vestibular afferent fibers establishes the basis for more specific physiological hypotheses.

C-fos Expression in the rat brain after unilateral labyrinthectomy and its relation to the uncompensated and compensated stages.

The expression of the immediate early gene c-fos has been studied in the entire brain of rats 3, 6 and 24 h after surgical unilateral labyrinthectomy. We combined in situ hybridization for c-fos messenger RNA with immunocytochemistry for Fos protein to document very early changes in c-fos expression and to identify with cellular resolution neuronal populations activated by unilateral labyrinthectomy. Three hours after unilateral labyrinthectomy a bilateral increase in both c-fos messenger RNA and protein levels was seen in the superior, medial and spinal vestibular nuclei, nucleus Y, and prepositus hypoglossal nucleus. These changes were asymmetric in the medial vestibular nucleus, being most prominent in the dorsal part of the contralateral nucleus (where second order vestibular neurons are located) and in the ventral part of the ipsilateral nucleus (where commissural neurons acting on the medial vestibular nucleus of the intact side are located). An increase in c-fos messenger RNA expression was seen bilaterally, but with an ipsilateral predominance, in the vermal and paravermal areas of the cerebellar cortex, flocculus and paraflocculus, as well as in the precerebellar lateral and paramedian reticular nuclei. c-fos messenger RNA and protein levels increased in a few regions of the contralateral inferior olive. A predominantly ipsilateral increase in c-fos expression also occurred in the caudate-putamen. A bilateral but not exactly symmetric increase in both c-fos messenger RNA and protein levels was present in several nuclei of the dorsal pontine tegmentum (parabrachial nucleus, locus coeruleus and laterodorsal tegmental nucleus), mesencephalic periaqueductal gray, and several hypothalamic, thalamic and cerebrocortical regions. No change was seen in the cerebellar nuclei, lateral vestibular nucleus and red nucleus. The increased expression of c-fos observed 3 h after unilateral labyrinthectomy, in conjunction with the sudden occurrence of postural and motor deficits, usually declined 6-24 h after the lesion, i.e. during the development of vestibular compensation. In the dorsal part of the medial vestibular nucleus, however, the pattern of c-fos expression observed 3 h after unilateral labyrinthectomy was reversed 6-24 h after the lesion: both c-fos messenger RNA and protein levels increased on the ipsilateral side, but greatly decreased on the contralateral side. In conclusion, asymmetric changes in c-fos expression occurred within 3 h after unilateral labyrinthectomy, but gradually declined or reversed 6 and 24 h after the lesion, thus being temporally related to the appearance and development of vestibular compensation.

Morphology of vertical canal related second order vestibular neurons in the cat.

The morphology of vertical canal related second order vestibular neurons in the cat was studied with the intracellular horseradish peroxidase method. Neurons were identified by their monosynaptic potentials following electrical stimulation via bipolar electrodes implanted into individual semicircular canal ampullae. Anterior and posterior canal neurons projected primarily to contralateral or ipsilateral motoneuron pools (excitatory and inhibitory pathways, respectively). The axons of contralaterally projecting neurons crossed the midline at the level of the abducens nucleus and bifurcated into an ascending and a descending main branch which travelled in the medial longitudinal fasciculus (MLF). Two types of anterior canal neurons were observed, one with unilateral and one with bilateral oculomotor projection sites. For both neuron classes, the major termination sites were in the contralateral superior rectus and inferior oblique subdivisions of the oculomotor nucleus. In neurons which terminated bilaterally, major collaterals recrossed the midline within the oculomotor nucleus to reach the ipsilateral superior rectus motoneuron pool. Other, less extensive, termination sites of both neuron classes were in the contralateral vestibular nuclear complex, the facial nucleus, the medullary and pontine reticular formation, midline areas within and neighboring the raphé nuclei, and the trochlear nucleus. The ascending main axons continued further rostrally to reach the interstitial nucleus of Cajal and areas around the fasciculus retroflexus. The descending branches proceeded further caudal in the medial vestibulo-spinal tract but were not followed to their spinal target areas. In addition to two previously described posterior canal related neuron types (Graf et al. 1983), we found neurons with bilateral oculomotor terminals and a spinal collateral. Typical for posterior canal neurons, the major termination sites were in the trochlear nucleus (superior oblique motoneurons) and in the inferior rectus subdivision of the oculomotor nucleus. Axon collaterals recrossed the midline to reach ipsilateral inferior rectus motoneurons. The axons of ipsilaterally projecting neurons ascended through the reticular formation to join the MLF caudal to the trochlear nucleus. The main target sites of anterior canal related neurons were in the trochlear nucleus and the inferior rectus subdivision of the oculomotor nucleus. Minor collaterals reached the pontine reticular formation and areas in between the fiber bundles of the ipsilateral MLF.(ABSTRACT TRUNCATED AT 400 WORDS)

Evidence for an alteration in brainstem cholinergic pathways following unilateral labyrinthectomy in the frog

Following VIIIth nerve stimulation, field potentials recorded in the contralateral vestibular nuclei of isolated medullae are larger in amplitude and more sensitive to atropine in chronically hemilabyrinthectomized frogs than those of controls. The atropine-sensitive component occurs at a latency which precludes involvement of the monosynaptic commissural projection between second order vestibular neurons. Therefore, in addition to this commissural projection, the contributions of more indirect pathways have to be considered in an attempt to understand the neuronal basis of behavioral improvement following vestibular lesions.

Vestibular mechanisms related to vertical and torsional eye movements.

1. A series of experiments concerning the organization of the vertical vestibuloocular reflex (VOR) of the rabbit are reviewed. 2. Unanesthetized, encéphale isolé and intact, alert rabbits have been submitted to natural stimulation of the labyrinth consisting in sinusoidal oscillations and static tilts around the longitudinal axis. The oculomotor responses have been recorded at the level of the III nucleus oculomotor neurons (OMN) and from the four vertical eye muscles. 3. The phase and gain of the OMN response at different frequencies of oscillation indicate a serial involvement of the macular ampullar labyrinthine receptors in the activation of the OMN. In the low frequency range of head movements, macular receptors alone can provide adequate ocular compensation. By raising the frequency of head movements, the threshold value of acceleration for recruiting second order vestibular neurons related to semicircular canals is reached and the vertical VOR is controlled predominantly by the ampullar receptors of the vertical canals. 4. These results have been confirmed and extended in the alert, intact rabbit. By orienting the animal in different positions with respect to the axis of oscillation it has been possible to activate selectively one or the other pair of complementary vertical canals. The EMG responses recorded from the vertical eye muscle exhibited different magnitudes in the different orientations, while the phase curve remained the same. 5. The static otolith-ocular reflex has also been investigated by tilting the alert animals oriented in the same way. The pattern of the EMG responses elicited by the pure macular input coincides with that obtained during dynamic stimulation. The existence of separate functional macular regions specifically connected with the different eye muscles and a close convergent action of the two types of labyrinthine receptors in ocular compensation, are suggested.

Eye movement related activity and morphology of second order vestibular neurons terminating in the cat abducens nucleus.

Intracellular records were obtained from axons of second order vestibular neurons in, and around, the left abducens nucleus in alert cats implanted with stimulating electrodes on both vestibular nerves and the left VIth nerve. Twelve secondary vestibular neurons were identified by their increase in firing rate with horizontal head rotation to the left and/or increasing eye position to the right. Following HRP injection, somatic location, axonal trajectory and termination sites were determined. Each of the above cells collateralized extensively in the abducens nucleus in a fashion consistent with their being either inhibitory (n = 7; left) or excitatory (n = 6; right) vestibular neurons in the disynaptic horizontal vestibulo-ocular reflex pathway. These vestibular neurons also arborized extensively in other posterior brainstem eye-movement related areas as well as sending an axon to the spinal cord.

Responses to step and repeated impulse accelerations in second order vestibular neurons of the cat

The characteristics of response of 98 vestibular nuclei neurons were investigated in the barbiturate anesthetized cat. All type I and type II neurons (tonic and kinetic) responded to stimulation of the horizontal canals with step and impulse accelerations. Seventy-seven (79 per cent) neurons of all types demonstrated adaptation, while the remaining 21 (21 per cent) neurons showed either reverse adaptation or no adaptation. When the interval between impulses with impulse accelerations reached a critical minimum, the averaged response was remarkably like the response to step acceleration, including the rate of adaptation. A previously undescribed response decline to repetitive impulse acceleration was seen, which, while sharing some characteristics with habituation, appears to be more closely related to adaptation. Furthermore, the data suggest that adaptation seen at the vestibular nuclear level is more likely a central phenomenon rather than a peripheral one.

Response characteristics of semicircular canal and otolith systems in cat. I. Dynamic responses of primary vestibular fibers.

1. The activity of cat semicircular canal and otolith afferents was studied during yaw and roll rotations, respectively, to examine their dynamic behavior. 2. A sinusoidal analysis of the canal afferent activities showed that their dynamic characteristics are similar to those of second order vestibular neurons, except for a two to three-fold lower absolute gain. This agrees with earlier studies using angular acceleration steps. 3. Both divisions of the eighth nerve were sampled so as to examine afferents from both the utriculus and sacculus. Within the range of inputs used (+/- 25 degrees lateral tilt), the presumed sacular afferents (inferior division) showed either a gamma- or beta-response. However, the gain of their response was generally much less than for the afferents of the superior division (mostly utricular). This behavior is to be expected on the basis of receptor orientations and the components of gravity acting upon the macular receptors. 4. In response to ramp changes in angular position, some otolith units showed a phasic-tonic response pattern, i.e., an overshoot followed by an adaptation to a new steady state level of activity. The majority of units showed predominantly tonic responses proportional to displacement. 5. During sinusoidal rotations the predominantly tonic units showed small phase leads of 0 to 15 degrees at 0.025 Hz which remained constant or decreased to 0 to -15 degrees at 1.0 Hz. The gains were flat or increased by up to 2 fold. The phasic-tonic units showed greater phase leads, 10 to 50 degrees, and gains which increased from 2 to 8 fold. 6. This behavior of otolith afferents suggests that they can provide information about both the magnitude and the rate of change of linear acceleration stimuli.

Response characteristics of semicircular canal and otolith systems in cat. II. Responses of trochlear motoneurons

1. The electrical activity of single trochlear motoneurons (TMns) and axons of second order vestibular neurons presumably terminating on these motoneurons were studied during natural stimulation of semicircular canals and otolith organs in cats anesthetized with Ketamine. 2. Null point analysis showed that TMns received an excitatory canal input from the contralateral posterior canal, and labyrinthine lesion experiments suggested that the functionally synergistic, ipsilateral anterior canal provides an inhibitory input. A small number of motoneurons showed orthogonal canal convergence. 3. In addition to the canal projections most TMns received an otolithic input. Firing rate was proportional to lateral head tilt and was of the beta type. Most units also responded to pitch with an increase and decrease in firing rate on nose-up and nose-down positioning, respectively. Lesion experiments indicated that the otolith responses are the results of reciprocal innervation of TMns by contralateral (excitatory) and ipsilateral (inhibitory) otolith projections. 4. During sinusoidal rotation in yaw (canal only stimulation) the mean phase lag re acceleration of the response of TMns increased from 60 degrees at 0.025 Hz to 126 degrees at 1.0 Hz. In roll (canal plus otolith stimulation) the phase lag of TMn responses measured 180 degrees and 130 degrees at 0.025 and 1.0 Hz, respectively. Phase-lags measured in Vi and Vc axons were less by ca. 15 degrees. 5. The otolith contribution to TMn responses in roll was calculated by vectorial subtraction of the yaw from the roll responses: A phase lag of 10 (0.025 Hz) to 90 degrees (0.5 Hz) re. displacement was noted and gain was constant over the same range. Similar lag dynamics were revealed in TMns when studied during ramp displacement of the head. 6. The possible functional role of central canal-otolith convergence and the differences between the response of primary vestibular afferents and secondary vestibular neurons and TMns will be discussed.

Response of first order vestibular neurons to lidocaine hydrochloride.

Changes in behavior and electrical activity of primary vestibular neurons were observed following injection of lidocaine hydrochloride into the middle ear of cats. After injection the cats exhibited head and ocular nystagmus, head and neck deviation and pupillary changes. Mean preinjection resting discharge rate for first order vestibular neurons was 46.0 spikes/sec. Two hours after lidocaine application the resting rate decreased to a mean of 22.2 spikes/sec and then recovered to 43.0 spikes/sec four hours, and 47.4 spikes/sec six hours after the experimental treatment. The increment sensitivity (increased rate of firing) of horizontal canal neurons to constant angular acceleration for the control period was 2.0 extra spikes/sec/deg/sec2; two hours after the application, 70% of the recorded neurons were unresponsive to angular acceleration or tilt. The sensitivity after four hours was 1.0 spikes/sec/deg/sec2 and 2.1 spikes/sec/deg/sec2 at six hours. The distinct depression of sensitivity by lidocaine at four hours compared to normal mean resting rate at this time suggests these functions may be governed by two modes of action in the receptor or first order afferents.

Ipsilateral utricular and semicircular canal interactions from electrical stimulation of individual vestibular nerve branches recorded in the descending medial longitudinal fasciculus

Interactions from electrical stimulation of individual vestibular end organ nerves recorded from second order vestibular neurons projecting caudally in the medial longitudinal fascinulus (MLF) have been investigated in unanesthetized, decerebrate decerebellate cats. Canal-canal and utricle-canal interactions were recorded using various condition-test parameters. The brain stem was sectioned to eliminate influence of the contralateral vestibular nuclei, and the condition-test experiments were repeated. The type of interaction observed (inhibition or facilitation) and the degree to which it occurred were dependent on the MLF recording site. Also, in the case of utricular interactions, these were dependent on the site of utricular stimulation. These dependencies indicate a topological arrangement from receptor cell through the second order neuronal projection pathways. Sectioning of the brain stem produced changes in the interaction patterns, indicating masking and/or balancing of the ipsilateral interactions. In interactions between the anterior and posterior canals, instances of no apparent interactions occuring before sectioning converted to inhibition after sectioning. This indicates that some facilitative interaction occurs involving feedback from the contralateral vestibular nuclei, and this facilitation masks or balances ipsilateral inhibition. In interactions between the anterior and horizontal canals, contralateral inhibitory influence masks ipsilateral facilitatory interactions. Contralateral facilitatory influence again balances ipsilateral inhibition in interactions between the horizontal and posterior canals. The degree of inhibition and facilitation observed indicates that considerably more polysynaptic ipsilateral convergence on second order vestibular neurons occurs than has been demonstrated in intracellular studies. Only inhibition was observed when the anterior canal was conditioned by stimulation of the utricular nerve after sectioning. In all other pairings, mixed effects were observed. It is suggested that this is related to known functional connections of semicircular canal second order neurons with neck motoneurons. Not only is canal output affected by utricular activity, but each canal affects utricular output in a different manner.

Transfer characteristics of first and second order lateral canal vestibular neurons in gerbil

Discharge patterns of first and second order vestibular neurons responding to angular acceleration in the plane of the lateral canals were studied in gerbil. The resting discharge activity of each cell was used to characterize the neuron by measuring the coefficient of variation and coefficient of skewness of the interspike interval distributions. Sinusoidal angular oscillations ranging in frequency from 0.0125 to 5.0 Hz were delivered by a velocity controlled rate-table. A PDP-12 minicomputer system was used on-line to display period and post-stimulus histograms of discriminated single unit activity. Off-line Fourier analysis of the period histograms was used to determine the phase of cell response to sinusoidal accelerations, while the average level and amplitude were determined by a least squares fitting algorithm applied over the fraction of the stimulus period where the cell discharged. First order neurons were found to have high discharge rates (average= 61.7imp./sec) and bidirectional responses to rotation, and were of two groups called regular and irregular according to their resting discharge patterns. Second order neurons, located mainly in the medial and lateral vestibular nuclei, had low or even zero resting discharge rates (average= 17.8) resulting in more uni-directional responses and were of a single population. For frequencies less than 10 Hz, the Bode plots of the regular first order neurons are similar to that of a first order system with a time constant of about 2 sec as predicted by the torsion pendulum theory for cupula movement. The irregular first order neurons show an increasing gain above 0.5 Hz and a large phase lead relative to angular velocity above 1.0 Hz suggestive of a fractional power transfer function. The second order neurons show the phase and gain characteristics of the regular first order neurons being in phase with angular velocity above 1.0 Hz.

Planar relationships of semicircular canals in the cat.

Planar relationships of semicircular canals in the cat.

Responses of Vestibular Nuclear Neurons to Ampullar Input

The responses of single vestibular nerve fibers of a frog to horizontal angular acceleration (acceleration and velocity steps) are described and compared in this chapter with the responses obtained from the cats' second order vestibular neurons. Of the afferent fibers, the majority show frequency adaptation (65 %) to prolonged constant angular acceleration. Second order neurons, however, show no significant adaptation. The majority of both afferent fibers and second order neurons show a non-linear relation between frequency increase and angular acceleration. The lowest thresholds for frequency increase are similar in both groups. Time constants of the majority of nerve fibers are about 3 sec (range 1–10 sec). It is suggested that fibers having short time constants represent acceleration sensitive units whereas those having long time constants monitor angular velocity. Time constants of second order neurons are distinctly different for tonic (resting discharge) and kinetic (no resting discharge) type I neurons (8.1 f 1.6 sec and 3.7 f 0.8 sec, respectively). Functional implications of these two groups of neurons are discussed here. The synaptology and location of second order vestibular neurons of the semicircular canals are also described here.