Convergence patterns of the posterior semicircular canal and utricular inputs in single vestibular neurons in cats

The convergence of the posterior semicircular canal (PC) and utricular (UT) inputs in single vestibular nuclei neurons was studied intracellularly in decerebrate cats. A total of 160 vestibular neurons were orthodromically activated by selective stimulation of the PC and the UT nerve and classified according to whether or not they were antidromically activated from the spinal cord and oculomotor nuclei into vestibulospinal (VS), vestibulooculospinal (VOS), vestibuloocular (VO), and unidentified vestibular neurons. Fifty-three (33%) of 160 vestibular neurons received convergent inputs from both the PC and UT nerves. Seventy-nine (49%) vestibular neurons responded to PC inputs alone, and 28 (18%) neurons received inputs only from the UT nerve. Of 53 convergent neurons, 8 (15%) were monosynaptically excited from both nerves. Thirty-five (66%) received monosynaptic excitatory inputs from the PC nerve and polysynaptic excitatory or inhibitory inputs from the UT nerve, or vice versa. Approximately one-third of VS and VOS neurons received convergent inputs. A majority of the VS neurons descended to the spinal cord through the lateral vestibulospinal tract, while almost all the VOS neurons descended to the spinal cord through the medial vestibulospinal tract. The convergent neurons were found in all vestibular nuclei but more in the lateral nucleus and descending nucleus. The VS neurons were more numerous than VO neurons or VOS neurons.     

Properties of utricular-activated vestibular neurons that project to the contralateral vestibular nuclei in the cat

The properties of utricular (UT)-activated vestibular neurons that send axons to the contralateral vestibular nuclei (commissural neurons) were investigated intracellularly or extracellularly in decerebrate cats. A total of 27 vestibular neurons were orthodromically activated by stimulation of UT nerves and antidromically activated by stimulation of the contralateral vestibular nuclei. All neurons tested were classified as vestibulospinal (VS), vestibulooculospinal (VOS), vestibuloocular (VO), and unidentified vestibular neurons (V) after antidromic stimulation of the spinal cord and oculomotor/trochlear nuclei. Most UT-activated commissural neurons (20/27) received monosynaptic inputs. Twelve of 27 commissural neurons were located in the medial vestibular nucleus, 5 were in the lateral vestibular nucleus, 10 were in the descending vestibular nucleus, and no commissural neurons were recorded in the superior vestibular nucleus. Seven of 27 neurons were commissural VS neurons, 9 of 27 were commissural VOS neurons, and 11 of 27 were commissural V neurons. No commissural VO neurons were found. All VOS neurons and 3 VS neurons issued descending axons via the medial vestibulospinal tract. We also studied convergent inputs from the posterior semicircular canal (PC) nerve onto UT-activated commissural neurons. Five of 27 UT-activated commissural neurons received converging inputs from the PC nerves. Electronic Publication     

Convergence of posterior semicircular canal and saccular inputs in single vestibular nuclei neurons in cats

Convergence between posterior canal (PC) and saccular (SAC) inputs in single vestibular nuclei neurons was investigated in decerebrated cats. Postsynaptic potentials were recorded intracellularly after selective stimulation of the SAC and PC nerves. Stimulation of either the SAC or PC nerve orthodromically activated 143 vestibular nuclei neurons. Of these, 61 (43%) were antidromically activated by stimulation of the C1-C2 junction, 14 (10%) were antidromically activated by stimulation of the oculomotor or trochlear nucleus, and 14 (10%) were antidromically activated by stimulation of both the oculomotor or trochlear nucleus and the spinal cord. Fifty-four (38%) neurons were not activated by stimulation of either or both. We named these neurons vestibulospinal (VS), vestibulo-ocular (VO), vestibulooculo-spinal (VOS) and vestibular (V) neurons, respectively. Both PC and SAC inputs converged in 47 vestibular nuclei neurons (26 VS, 2 VO, 6 VOS and 13 V neurons). Of these, 19 received monosynaptic excitatory inputs from both nerves. This input pattern was frequently seen in VS neurons. Approximately half of the convergent VS neurons descended to the spinal cord through the lateral vestibulospinal tract. The remaining half and all the convergent VOS neurons descended to the spinal cord through the medial vestibulospinal tract. Most of the convergent neurons were located in the lateral nucleus or descending nucleus.     

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

The convergence between the anterior semicircular canal (AC) and utricular (UT) inputs, as well as the convergence between the AC and saccular (SAC) inputs in single vestibular neurons of decerebrated cats were investigated. Postsynaptic potentials were recorded intracellularly after selective stimulation of each pair of vestibular nerves AC/UT or AC/SAC. Neurons were recorded from the central parts of the vestibular nuclei, where the otolith afferents mainly terminate. Of a total of 105 neurons that were activated after stimulation of the AC and UT nerves, 42 received convergent inputs. Thirty-eight of these neurons received excitatory inputs from both afferents. Convergent neurons were further classified into vestibulospinal (n=28) and vestibulooculospinal (n=6) neurons by antidromic activation from the border between the C1 and C2 spinal cord and the oculomotor or trochlear nucleus. Eight neurons that were not antidromically activated from either site were classified as vestibular neurons. Forty three percent of the convergent vestibulospinal neurons and most of the convergent vestibulooculospinal neurons projected to the spinal cord through the medial vestibulospinal tract. The remaining vestibulospinal and vestibulooculospinal neurons descended through the ipsilateral lateral vestibulospinal tract. Of a total of 118 neurons that were activated after stimulation of the AC and/or SAC nerves, 51 received convergent inputs (27 vestibulospinal, 4 vestibulooculospinal, 5 vestibuloocular and 15 vestibular neurons). Forty-two of the convergent neurons received excitatory inputs from both afferents. Thirty seven percent of the convergent vestibulospinal neurons and all of the convergent vestibulooculospinal neurons projected to the spinal cord through the medial vestibulospinal tract. The remaining vestibulospinal and vestibulooculospinal neurons descended through the ipsilateral lateral vestibulospinal tract. Electronic Publication     

Properties and axonal trajectories of posterior semicircular canal nerve-activated vestibulospinal neurons

We studied the axonal projections of vestibulospinal neurons activated from the posterior semicircular canal. The axonal projection level, axonal pathway, and location of the vestibulospinal neurons originating from the PC were investigated in seven decerebrated cats. Selective electrical stimulation was applied to the PC nerve, and extracellular recordings in the vestibular nuclei were performed. The properties of the PC nerve-activated vestibulospinal neurons were then studied. To estimate the neural pathway in the spinal cord, floating electrodes were placed at the ipsilateral (i) and contralateral (c) lateral vestibulospinal tract (LVST) and medial vestibulospinal tract (MVST) at the C1/C2 junction. To elucidate the projection level, floating electrodes were placed at i-LVST and MVST at the C3, T1, and L3 segments in the spinal cord. Collision block test between orthodromic inputs from the PC nerve and antidromic inputs from the spinal cord verified the existence of the vestibulospinal neurons in the vestibular nuclei. Most (44/47) of the PC nerve-activated vestibulospinal neurons responded to orthodromic stimulation to the PC nerve with a short (<1.4 ms) latency, indicating that they were second-order vestibulospinal neurons. The rest (3/47) responded with a longer (≥1.4 ms) latency, indicating the existence of polysynaptic connections. In 36/47 PC nerve-activated vestibulospinal neurons, the axonal pathway was histologically verified to lie in the spinal cord. The axons of 17/36 vestibulospinal neurons projected to the i-LVST, whereas 14 neurons projected to the MVST, and 5 to the c-LVST. The spinal segment levels of projection of these neurons elucidated that the axons of most (15/17) of vestibulospinal neurons passing through the i-LVST reached the L3 segment level; none (0/14) of the neurons passing through the MVST extended to the L3 segment level; most (13/14) of them did not descend lower than the C3 segment level. In relation to the latency and the pathway, 33/36 PC nerve-activated vestibulospinal neurons were second-order neurons, whereas the remaining three were polysynaptic neurons. Of these, 33 second-order vestibulospinal neurons, 16 passed through the i-LVST, while 13 and 4 descended through the MVST and c-LVST, respectively. The remaining three were polysynaptic neurons. Histological analysis showed that most of the PC nerve-activated vestibulospinal neurons were located within a specific area in the medial part of the lateral vestibular nucleus and the rostral part of the descending vestibular nucleus. In conclusion, it was suggested that PC nerve-activated vestibulospinal neurons that were located within a focal area of the vestibular nuclei have strong connections with the lower segments of the spinal cord and are related to postural stability that is maintained by the short latency vestibulospinal reflex.     

Spatial coordination by descending vestibular signals

Spatial response properties of medial (MVST) and lateral (LVST) vestibulospinal tract neurons were studied in alert and decerebrate cats during sinusoidal angular rotations of the whole body in the horizontal and many vertical planes. Of 220 vestibulospinal neurons with activity modulated during 0.5-Hz sinusoidal rotations, 200 neurons exhibited response gains that varied as a cosine function of stimulus orientation and phases that were near head velocity for rotation planes far from the minimum response plane. A maximum activation direction vector (MAD), which represents the axis and direction of rotation that maximally excites the neuron, was calculated for these neurons. Spatial properties of secondary MVST neurons in alert and decerebrate animals were similar. The responses of 88 of 134 neurons (66%) could be accounted for by input from one semicircular canal pair. Of these, 84 had responses consistent with excitation from the ipsilateral canal of the pair (13 horizontal, 27 anterior, 44 posterior) and 4 with excitation from the contralateral horizontal canal. The responses of the remaining 46 (34%) neurons suggested convergent inputs. The activity of 38 of these was significantly modulated by both horizontal and vertical rotations. Twelve neurons (9%) had responses that were consistent with input from both vertical canal pairs, including 9 cells with MADs near the roll axis. Thirty-two secondary MVST neurons (24%) had type II yaw and/or roll responses. The spatial response properties of 18 secondary LVST neurons, all studied in decerebrate animals, were different from those of secondary MVST neurons. Sixteen neurons (89%) had type II yaw and/or roll responses, and 12 (67%) appeared to receive convergent canal pair input. Convergent input was more common on higher-order vestibulospinal neurons than on secondary neurons. These results suggest that MVST and LVST neurons and previously reported vestibulo-ocular neurons transmit functionally different signals. LVST neurons, particularly those with MADs close to the roll axis, may be involved in the vestibular-limb reflex. The combination of vertical and ipsilateral horizontal canal input on many secondary MVST neurons suggests a contribution to the vestibulocollic reflex. However, in contrast to most neck muscles, very few neurons had maximum vertical responses near pitch.     

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. Received: 8 July 1996 / Accepted: 21 April 1997     

Saccular and utricular inputs to single vestibular neurons in cats

Saccular and utricular organs are essential for postural stability and gaze control. Although saccular and utricular inputs are known to terminate on vestibular neurons, few previous studies have precisely elucidated the origin of these inputs. We investigated the saccular and utricular inputs to single vestibular neurons in whole vestibular nuclei of decerebrated cats. Postsynaptic potentials were recorded from vestibular neurons after electrical stimulation of the saccular and utricular nerves. Ascending and descending axonal projections were examined by stimulating the oculomotor/trochlear nuclei and the cervical segment of the spinal cord, respectively. After each experiment, locations of recorded neurons were identified. The recorded neurons (140) were classified into vestibulo-spinal (79), vestibulo-oculo-spinal (9), and vestibulo-ocular (3) neurons based on antidromic responses; 49 other vestibular neurons were unidentified. The majority of recorded neurons were mainly located in the lateral vestibular nucleus. Most of the otolith-activated vestibular nuclei neurons seemed to participate in vestibulospinal reflexes. Of the total 140 neurons recorded, approximately one third (51) received saccular and utricular inputs (convergent neurons). The properties of these 51 convergent neurons were further investigated. Most (33/51) received excitatory postsynaptic potentials (EPSPs) after saccular and utricular nerve stimulation. These results implied that most of the convergent neurons in this study additively coded mixed information for vertical and horizontal linear acceleration. Based on the latencies of convergent neurons, we found that an early integration process for vertical and horizontal linear acceleration existed at the second-order level.     

Influence of neck afferents on vestibulospinal neurons

Summary The effects of neck afferent stimulation on vestibulospinal neurons in Deiters' nucleus and in the descending nucleus, and the interaction of cervical and vestibular input, were examined extracellularly in decerebrate, decerebellate cats. Many of the vestibulospinal neurons were identified as having axons in the lateral or medial vestibulospinal tract (LVST or MVST) and as being driven antidromically from C₃ or C₆.Half of the spontaneously active neurons were excited with a latency of 2.5–5.5 ms (early excitation) by stimulation of the contralateral C₂ ganglion. In some neurons early excitation was followed by late excitation (latency > 6 ms), which was in other neurons the only effect seen. Early excitation was due to stimulation of proximal afferents because stimulation of the C₂ dorsal or ventral rami usually produced late excitation only. Early excitation was seen in LVST and MVST neurons terminating between C₃ and C₆ and in those projecting beyond C₆. Neurons with early excitation were scattered throughout Deiters' nucleus and the rostral part of the descending nucleus.In some neurons, mainly in the descending nucleus, the initial effect of contralateral C₂ ganglion stimulation was inhibition. Inhibition could be evoked by stimulation of the ganglion or dorsal rami bilaterally. The axons of all tested inhibited neurons were in the MVST.Thirty-five percent of the population studied received convergence of early excitation and short-latency input from the labyrinth, sometimes from the semicircular canals. There was also convergence between late excitation or inhibition and vestibular input.The influence of neck afferent input on vestibulospinal neurons provides one pathway for this input to the neck and limb segments of the spinal cord. This pathway may be part of the substrate of the tonic neck reflex. In addition, vestibulospinal neurons are one site of interaction between neck and vestibular reflexes.Supported by N.I.H. grant NS 02619     

The effects of stimulating the cerebellar nodulus in the cat on the responses of vestibular neurons

In a first series of experiments, recordings were obtained from cat abducens and trochlear motorneurons and from axons of secondary vestibular neurons terminating in these motor nuclei, and the effects of cerebellar nodulus stimulation on utricular- and canal-evoked responses in these neurons were studied. Ultricular activation of vestibular axons recorded in the ipsilateral VIth and contralateral IVth nuclei was probably monosynaptically inhibited by nodular stimulation provided conditioning-test intervals were in the range between 0-10 ms and the test stimuli were close to threshold intensities. Of the vestibular axons activated by stimulation of the semicircular canal nerves only those evoked by the horizontal canal stimulation and recorded in the ipsilateral VIth nucleus were weakly inhibited. When the vestibular stimuli were strong enough to produce clear field potentials in the motor nuclei and/or postsynaptic potentials in motorneurons, nodular stimulation had practically no effect on their amplitudes. It is concluded that inhibition of vestibuloocular transmission is weak as compared to floccular inhibition studied previously. In a second series of experiments, recordings were obtained from vestibular neurons which were activated antidromically and/or transsynaptically by stimulation of the contralateral fastigial nucleus, and the effects of ipsilateral nodular stimulation on these responses were studied. It was found that nodular stimulation inhibited both antidromic as well as transsynaptic fastigial activations of vestibular neurons. Most of these vestibular neurons were located in the descending vestibular nucleus and received polysynaptic vestibular and spinal inputs. It is concluded that in addition to its weak inhibitory effect on vestibuloocular transmission the nodulus exerts a powerful inhibition on vestibular neurons transmitting vestibular and spinal inputs to cerebellar nuclei and/or cortex. It is suggested that the nodulus controls cerebellar projecting vestibular neurons which carry vestibular and spinal information to the cerebellum. The vestibular, proprioceptive and visual information which is present in the nodulus may aid the role of the nodulus in controlling body posture.     

Spatial properties of second-order vestibulo-ocular relay neurons in the alert cat

Second-order vestibular nucleus neurons which were antidromically activated from the region of the oculomotor nucleus (second-order vestibuloocular relay neurons) were studied in alert cats during whole-body rotations in many horizontal and vertical planes. Sinusoidal rotation elicited sinusoidal modulation of firing rates except during rotation in a clearly defined null plane. Response gain (spike/s/deg/s) varied as a cosine function of the orientation of the cat with respect to a horizontal rotation axis, and phases were near that of head velocity, suggesting linear summation of canal inputs. A maximum activation direction (MAD) was calculated for each cell to represent the axis of rotation in three-dimensional space for which the cell responded maximally. Second-order vestibuloocular neurons divided into 3 non-overlapping populations of MADs, indicating primary canal input from either anterior, posterior or horizontal semicircular canal (AC, PC, HC cells). 80/84 neurons received primary canal input from ipsilateral vertical canals. Of these, at least 6 received input from more than one vertical canal, suggested by MAD azimuths which were sufficiently misaligned with their primary canal. In addition, 21/80 received convergent input from a horizontal canal, with about equal number of type I and type II yaw responses. 4/84 neurons were HC cells; all of them received convergent input from at least one vertical canal. Activity of many vertical second-order vestibuloocular neurons was also related to vertical and/or horizontal eye position. All AC and PC cells that had vertical eye position sensitivity had upward and downward on-directions, respectively. A number of PC cells had MADs centered around the MAD of the superior oblique muscle, and 2/3 AC cells recorded in the superior vestibular nucleus had MADs near that of the inferior oblique. Thus, signals with spatial properties appropriate to activate oblique eye muscles are present at the second-order vestibular neuron level. In contrast, none of the second-order vestibuloocular neurons had MADs near those of the superior or inferior rectus muscles. Signals appropriate to activate these eye muscles might be produced by combining signals from ipsilateral and contralateral AC neurons (for superior rectus) or PC neurons (for inferior rectus). Alternatively, less direct pathways such as those involving third or higher order vestibular or interstitial nucleus of Cajal neurons might play a crucial role in the spatial transformations between semicircular canals and vertical rectus eye muscles.     

Cerebellar control of the vestibulospinal tract cells in rabbit

Summary The organization of the cerebellar, vestibular and spinal inputs to the lateral and medial vestibulospinal tract (LVST and MVST) cells was studied in anaesthetized rabbits. Synaptic actions of these inputs were determined by recording postsynaptic potentials intracellularly and also unit spike discharges extracellularly from a number of LVST and MVST cells. As reported previously in cats, inhibition was evoked very frequently from the vermal cortex of the cerebellar anterior lobe and less frequently from that of the posterior lobe. However, no such inhibition was derived from the flocculus. The cerebellar inhibition was exerted upon both LVST and MVST cells, whether they received monosynaptic activation from the primary vestibular afferents (second-order) or not and whether they conducted impulses fast or slowly. However, the inhibition was frequently absent in slow second-order MVST cells. The vast majority of LVST and MVST cells received an excitatory input from the spinocerebellar afferents ascending the funiculus posterolateralis. This input was particularly prominent from the upper cervical cord. The spinal excitation thus obtained occurred in close connection with the cerebellar inhibition. Hence, it appears that the cerebellar vermis receives the spinal signals that drive LVST and MVST cells and in turn sends out inhibitory signals to adjust the reflex activity in these cells.     

Axon collaterals of anterior semicircular canal-activated vestibular neurons and their coactivation of extraocular and neck motoneurons in the cat

We studied the ascending and descending axonal trajectories of excitatory vestibular neurons related to the anterior semicircular canal, by means of local stimulation and spike-triggered signal averaging techniques in anesthetized cats. More than 200 vestibular neurons related to the ampullary nerve of the anterior semicircular canal (ACN) were identified as vestibulo-ocular neurons by antidromic stimulation of the contralateral inferior oblique (IO) muscle motoneuron pool. In the descending, medial and ventral lateral nuclei, about 60% of these vestibulo-ocular neurons were also activated antidromically by upper cervical spinal cord stimulation (vestibulo-ocular-collic (cervical) = VOC). These VOC neurons produced unitary EPSPs in the majority of neck extensor motoneurons located at the C₁ segment. None of the VOC neurons had axons descending as far as the thoracic level. Most of these VOC neurons were activated monosynaptically following stimulation of the ACN. The conduction velocity of the descending axons of VOC neurons was approximately 63 m/s, which was significantly faster than that of the ascending axons. The remaining 40% of the vestibulo-ocular neurons were not activated antidromically following spinal cord stimulation at intensities of 1 mA or more (vestibulo-ocular = VO). Most of the VO neurons were activated polysynaptically by ACN stimulation. The superior vestibular nucleus contained VO neurons that were activated mono- and polysynaptically following ACN stimulation.     

Response of vestibular neurons to head rotations in vertical planes. I. Response to vestibular stimulation

1. We have studied, in decerebrate cats, the responses of neurons in the lateral and descending vestibular nuclei to whole-body rotations in vertical planes that activated vertical semicircular canal and utricular receptors. Some neurons were identified as vestibulospinal by antidromic stimulation with floating electrodes placed in C4. 2. The direction of tilt that caused maximal excitation (response vector orientation) of each neuron was determined. Neuron dynamics were then studied with sinusoidal stimuli closely aligned with the response vector orientation, in the range 0.02-1 Hz. A few cells, for which we could not identify a response vector, probably had spatial-temporal convergence. 3. On the basis of dynamics, neurons were classified as receiving their input primarily from vertical semicircular canals, primarily from the otolith organs, or from canal+otolith convergence. 4. Response vector orientations of canal-driven neurons were often near +45 degrees or -45 degrees with respect to the transverse (roll) plane, suggesting these neurons received excitatory input from the ipsilateral anterior or posterior canal, respectively. Some neurons had canal-related dynamics but vector orientations near roll, presumably because they received convergent input from the ipsilateral anterior and posterior canals. Few neurons had their vectors near pitch. 5. In the lateral vestibular nucleus, neurons with otolith organ input (pure otolith or otolith+canal) tended to have vector orientations closer to roll than to pitch. In the descending nucleus the responses were evenly divided between the roll and pitch quadrants. 6. We conclude that most of our neurons have dynamics and response vector orientations that make them good candidates to participate in vestibulospinal reflexes acting on the limbs, but not those acting on the neck.     

Electrophysiological analysis of the vestibulospinal reflex pathway of rabbit. I. Classification of tract cells

Summary In anaesthetized rabbits, the medulla was surveyed with recording microelectrodes to identify different types of vestibulospinal tract neurones. Field potentials, unitary extracellular spikes and intracellular potentials were recorded during antidromic stimulation at C₁ and C₆ segments and during orthodromic stimulation through VIIIth nerve. The lateral and medial vestibulospinal tracts (LVST and MVST) were stimulated discriminately with the method developed in Appendix. On the basis of different axonal courses and conduction velocities, three major groups were distinguished for those cells which were activated monosynaptically by the primary vestibular afferents; 1. fast conducting LVST; 2. fast conducting MVST; and 3. slowly conducting MVST. Three other groups were discriminated for those cells which received only a polysynaptic or no action from primary vestibular afferents. These were; 4. fast conducting LVST; 5. slowly conducting LVST and 6. slowly conducting MVST. All of these six types of VST cells were represented within Deiters' nucleus. Only a relatively small number of MVST cells were found in the medial vestibular nucleus.     

Axon collaterals to the extraocular motoneuron pools of inhibitory vestibuloocular neurons activated from the anterior, posterior and horizontal semicircular canals in the cat

The branching pattern of inhibitory vestibuloocular neurons and their synaptic contacts with extraocular motoneurons were studied by means of spike-triggered averaging and local stimulation techniques. Individual vestibuloocular neurons activated by stimulation of the ampullary nerve of the anterior semicircular canal (ACN) inhibited motoneurons in both the ipsilateral (i-) trochlear nucleus and i-inferior rectus motoneuron pools. Individual vestibuloocular neurons receiving input from the ampullary nerve of the posterior semicircular canal (PCN) inhibited motoneurons in both the i-inferior oblique and i-superior rectus motoneuron pools. Probably, these axonal trajectories underlie conjugate eye movement during vertical head rotation. No conclusive evidence was found to indicate that single inhibitory vestibular neurons receiving input from the horizontal semicircular canal (HCN) give off axon collaterals to the i-abducens and the contralateral medial rectus motoneurons. A separate projection of HCN-related neurons to motoneurons supplying the lateral and medial rectus muscles might be useful for convergence during horizontal head movement.     

Canal-otolith interaction in the fastigial nucleus of the alert monkey

To determine the contribution of the otoliths as well as the horizontal and vertical semicircular canals to the response of "vestibular only" neurons in the rostral fastigial nucleus of the alert monkey, we applied natural sinusoidal vestibular stimuli (0.6 Hz; +/-15 deg) around different axes. During the experiment the monkey sat erect in a primate chair with the head immobile. Semicircular canal responses were investigated during tilted yaw stimulation around an earth vertical axis. The tilt angle was varied by 30 deg and included the optimal plane for horizontal canal stimulation (15 deg nose down from the stereotactic plane). The otoliths and mainly the vertical canals made contributions during stimulation around an earth-fixed horizontal axis (vertical stimulation). Head orientation was also slowly altered (2-3 deg/s) over a range of 180 deg under both stimulus conditions (tilted yaw and vertical stimulation). Neuronal data for each paradigm were fitted by a least squares best-sine function. Computation of the hypothetical contributions made by all three pairs of semicircular canals and the otoliths to these responses showed that 74% of the 46 neurons investigated received an otolith input; in most instances it was combined with a canal input. Neurons most often received input from the horizontal and vertical canals as well as the otoliths. Only a minority of neurons received a purely otolith (13%), vertical canal (13%), or horizontal canal (4%) input. Conventional criteria (head position-related activity, spatiotemporal convergence, STC) failed to detect an otolith contribution in several such instances. Thus, canal-otolith convergence is the general rule at this central stage of vestibular information processing in the fastigial nucleus. The large variety of response types allows these neurons to participate in multiple tasks of vestibulospinal movement control.     

Spatial distribution of the vestibulospinal neurons in the frog vestibular nuclei.

In experiments on the preparation of a frog perfused brain (Rana ridibunda), intracellular potentials were recorded from neurons of the vestibular nuclei following stimulation of the vestibular nerve and the spinal cord. The vestibulospinal neurons were identified on the basis of excitatory postsynaptic potentials evoked by the stimulation of the ipsilateral vestibular nerve and antidromic activation from the stimulation of the cervical and lumbar enlargements of the spinal cord. The cells that could be activated antidromically only by cervical cord stimulation have been designated as C cells, and the cells that could also be activated antidromically as a result of lumbar stimulation have been termed L cells. The average conduction velocity determined for C neurons was 10.67 m/s and for L neurons 15.84 m/s. The ratio of C and L neurons over the vestibular nuclear complex was very similar to each other: 52% C neurons and 48% L neurons. The majority of both types of neurons were localized in the lateral vestibular nucleus (58.6%), to a lesser extent in the descending vestibular nucleus (30.7%) and very little in the medial vestibular nucleus (10.6%). In the lateral vestibular nucleus, C neurons prevailed in the caudal part of the nucleus and L neurons prevailed in the rostral part. By contrast, in the descending and medial vestibular nuclei there was a gradual increase of C and L cells quantitatively from the rostral to the caudal part. Fast and slow cells were detected among the vestibulospinal neurons. The fast neurons of L cells did not prevail greatly over the slow ones, whereas the slow neurons of C cells prevailed comparatively largely over the fast neurons. Thus, it became possible to reconstruct the spatial distribution of the identified vestibulospinal neurons. The results of spatial distribution of C and L vestibulospinal neurons in the frogs failed to conform to definite somatotopy, which is characteristic of mammalian vestibular nuclei.The results of this study have confirmed an earlier assumption that C and L neurons in the frog's vestibular nuclei as a source of vestibulospinal fibers, are scattered separately or more frequently in groups, so that they establish a 'patch-like' somatotopy and do not form a distinctly designed field as in mammals.     

Effects of natural neck afferent stimulation on vestibulo-spinal neurons in the decerebrate cat

Summary The response patterns of antidromically identified vestibulo-spinal Deiters' neurons and other vestibular nuclear neurons to stimulation of neck receptors and horizontal semicircular canal receptors were investigated in precollicular decerebrate cats.The neck receptors were stimulated by sinusoidal oscillation (frequency 0.2 Hz and 10 ° amplitude) and trapezoidal movements of the cervical axis vertebrae in the horizontal plane, while the head was stereotaxically fixed in a prone position. The influence of horizontal semicircular canal receptors was examined by sinusoidal turntable oscillations (0.2 Hz, 10 °).Out of 151 antidromically driven Deiters' neurons, 16 units responded to neck rotation and 11 cells out of 148 Deiters' neurons were influenced by the horizontal semicircular canal receptors. Only 3 of these neurons were affected by convergent cervical and vestibular influences and revealed antagonistic response patterns. Neck-responsive units were found to be scattered throughout Deiters' nucleus, whereas semicircular-canal-influenced neurons were predominantly encountered in its rostro-ventral part.Altogether, 68 neck-responsive neurons in the vestibular nuclear complex were tested. These units showed a periodic, direction-specific modulation of the discharge rate in response to sinusoidal oscillation. Almost all responses were related to input angular velocity at 0.2 Hz with a mean gain of 1.15 imp/s per deg/s. During trapezoidal neck displacement, responsive units also exhibited tonical components in their discharge rates.These results suggest kinetic-static response characteristics of neck receptors. The cervico-vestibulo-spinal pathway may contribute to tonic neck reflexes; vestibular and neck reflexes may partially interact in Deiters' nucleus.Supported by Sonderforschungsbereich Hirnforschung und Sinnesphysiologie (SFB 70) der Deutschen Forschungsgemeinschaft     

Plane-specific brainstem commissural inhibition in frog second-order semicircular canal neurons

Commissural inputs of identified second-order semicircular canal neurons were studied by separate stimulation of each of the three canal nerves on either side in the vitro frog brains. The spatial pattern of these inputs was further investigated in those second-order canal neurons that received a monosynaptic input from only one ipsilateral canal nerve (91%). Since similar results were obtained in the presence as in the absence of the cerebellum, commissural inputs must have been relayed via fibers crossing in the brainstem. Following stimulation of individual semicircular canal nerves, commissural inputs were either inhibitory or excitatory. A commissural inhibition was evoked in the majority of the recorded neurons (79%) by stimulation of the coplanar semicircular canal nerve on the contralateral side. In the remaining neurons, a commissural excitatory input was evoked. A commissural excitation, originating from the two noncoplanar semicircular canals, predominated in most (68%) of the recorded neurons and was independent of the type of second-order canal neuron. The onset latency of the canal plane-specific commissural inhibitory potentials was di- or trisynaptic. Stimulation of the contralateral VIIIth nerve evoked excitatory commissural responses. The canal plane-specific commissural inhibition therefore might have been masked by commissural excitatory responses as in earlier studies. The similar organization of the canal plane-specific commissural inhibition in frog and cat corroborates the notion of a phylogenetically conservative, basic vestibular organization. The presence of a canal plane-unspecific commissural excitation, however, appears to be a feature that is specific to frogs. The functional implications of these similarities and differences are discussed.