M. Imagawa

Properties of utricular nerve-activated vestibulospinal neurons in cats

The axonal pathway, conduction velocities, and locations of the cell bodies of utricular nerve-activated vestibulospinal neurons were studied in decerebrated or anesthetized cats using the collision test of orthodromic and antidromic spikes. For orthodromic stimulation, bipolar tungsten electrodes were placed on the utricular nerve and the other vestibular nerve branches were transected. Monopolar tungsten electrodes were positioned on both sides of the upper cervical segments (C2–4), caudal end of the cervical enlargement (C7-T1), and from the lower thoracic to the upper lumbar segments (T12-L3) and were used for antidromic stimulation of the spinal cord. Another monopolar electrode was also placed in the oculomotor nucleus to study whether utricular nerve-activated vestibulospinal neurons have ascending branches to the oculomotor nucleus. Of the 173 vestibular neurons orthodromically activated by the stimulation of the utricular nerve, 46 were second-order vestibulospinal neurons and 5 were third-order neurons. The majority of the utricular nerve-activated vestibulospinal neurons were located in the rostral part of the descending vestibular nucleus and the caudal part of the ventral lateral nucleus. Seventy-three percent of the utricular nerve-activated vestibulospinal neurons descended through the ipsilateral lateral vestibulospinal tract. Approximately 80% of these neurons reached the cervicothoracic junction, but a few reached the upper lumbar spinal cord. Twenty-seven percent of the utricular nerve-activated vestibulospinal neurons descended through the medial vestibulospinal tract or the contralateral vestibulospinal tracts. Those axons terminated mainly in the upper cervical segments. Almost none of the utricular nerve-activated vestibular neurons had ascending branches to the oculomotor nucleus.

Axonal projections of utricular afferents to the vestibular nuclei and the abducens nucleus in cats

Axonal projections of utricular (UT) afferents in cats were examined by three approaches: recordings of field potentials, labelling of UT nerve fibres by localized infusion of horseradish peroxidase (HRP) and intraaxonal infusion of HRP into a single UT afferent. UT afferents project principally into the rostral part of the descending nucleus and the ventral part of the lateral nucleus. Projection into the superior and the medial nuclei and the ipsilateral abducens nucleus were also observed.

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

Abstract. 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), vestibulo-oculo-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.

Commissural effects in the otolith system.

Abstract. 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.

Cross-striolar and commissural inhibition in the otolith system.

Abstract: Neural connections from the saccular and utricular nerves to the ipsilateral vestibular neurons and the commissural effects were studied by using intracellular recordings of excitatory (E) and inhibitory (I) postsynaptic potentials (PSPs) in vestibular neurons of cats after focal stimulation of the saccular and the utricular maculae. Neural circuits from the maculae to vestibular neurons, termed crossstriolar inhibition, may provide a mechanism for increasing the sensitivity to linear acceleration and tilt of the head. It was examined whether secondary vestibular neurons activated by an ipsilateral otolith organ received a commissural inhibition from a contralateral otolith organ that occupied the same geometric plane. Results suggest that utricular‐activated vestibular neurons receiving commissural inhibition may provide a mechanism for increasing the sensitivity to horizontal linear acceleration and tilt of the head. The commissural inhibition of the saccular system was much weaker than that of the utricular system.

Morphology of single afferents of the saccular macula in cats

The morphology of single saccular afferents was studied by the intracellular horseradish peroxidase (HRP) method. Four neurons were sufficiently stained to allow reconstruction of their axonal arborizations. The main axon of these neurons bifurcated into an ascending and a descending branch at the level of the lateral nucleus. The ascending branches of two axons gave off collaterals with boutons in the caudal part of the superior nucleus, while the other two ascending branches lacked such terminations. By contrast, characteristics of the descending axonal arborization patterns of all the four neurons were substantially the same. The descending branches coursed caudally through the lateral part of the descending nucleus, and gave off up to 14 collaterals with boutons that extended throughout this nucleus. These collaterals also reached the ventral part of the lateral nucleus, the lateral border of the medial nucleus, and group f. A few axon collaterals ramified even outside the border of the vestibular nuclei into the spinal trigeminal nucleus and the reticular formation surrounding it. Axon collaterals from the stem axon also terminated in the interstitial nucleus of the vestibular nerve. There was a noticeable absence of any projection to the y group.

Second-order vestibular neuron morphology of the extra-MLF anterior canal pathway in the cat

Second-order vestibular neurons form the central links of the vestibulo-oculomotor three-neuron arcs that mediate compensatory eye movements. Most of the axons that provide for vertical vestibulo-ocular reflexes ascend in the medial longitudinal fasciculus (MLF) toward target neurons in the oculomotor and trochlear nuclei. We have now determined the morphology of individual excitatory second-order neurons of the anterior semicircular canal system that course outside the MLF to the oculomotor nucleus. The data were obtained by the intracellular horseradish peroxidase method. Cell somata of the extra-MLF anterior canal neurons were located in the superior vestibular nucleus. The main axon ascended through the deep reticular formation beneath the brachium conjunctivum to the rostral extent of the nucleus reticularis tegmenti pontis, where it crossed the midline. The main axon continued its trajectory to the caudal edge of the red nucleus from where it coursed back toward the oculomotor nucleus. Within the oculomotor nucleus, collaterals reached superior rectus and inferior oblique motoneurons. Some axon branches recrossed the midline within the oculomotor nucleus and reached the superior rectus motoneuron subdivision on that side. Since these neurons did not give off a collateral toward the spinal cord, they were classified as being of the vestibulo-oculomotor type and are thought to be involved exclusively in eye movement control. The signal content and spatial tuning characteristics of this anterior canal vestibulo-oculomotor neuron class remain to be determined.

The neuronal organization of horizontal semicircular canalactivated inhibitory vestibulocollic neurons in the cat

Summary1.The somatic location and axonal projections of inhibitory vestibular nucleus neurons activated by the horizontal semicircular canal nerve (HCN) were studied in anesthetized cats. Cats were anesthetized with ketamine hydrochloride and pentobarbital sodium. 2.Intracellular recordings were obtained from 11 neck extensor motoneurons which were identified by antidromic activation from the dosai rami (DR) in the C1 segment. Stimulation of the ipsilateral (i-) HCN and the ipsilateral abducens (AB) nucleus evoked IPSPs in the motoneurons. These IPSPs were fully or partially occluded when they were evoked simultaneously. 3. Intracellular recordings were obtained from 8 AB motoneurons. Stimulation of the i-HCN and the i-C1DR motoneuron pool evoked IPSPs in the AB motoneurons. These IPSPs were also partially occluded when they were evoked simultaneously, which implied that some HCN-activated neurons inhibit both i-AB motoneurons and ipsilateral neck motoneurons. 4. Unit activity was extracellularly recorded from 30 vestibular neurons that were activated monosynaptically by i-HCN stimulation. Their axonal projections were determined by stimulating the i-AB nucleus and the i-C1DR motoneuron pool. Eight neurons were activated by both stimuli, and were termed vestibulooculo-collic (VOC) neurons. Their axonal branching was examined by means of local stimulation in and around the i-AB nucleus and the i-C1DR motoneuron pool. Eighteen neurons were antidromically activated from the i-C1DR motoneuron pool but not from the i-AB nucleus. These were termed vestibulo-collic (VC) neurons. Four neurons were activated from the i-AB nucleus but not from the ventral funiculus in the C1 segment, and were termed vestibulo-ocular (VO) neurons. The HCN-activated inhibitory neurons were mostly localized in the rostroventral part of the medial vestibular nucleus. 5. Horseradish peroxidase (HRP) was injected iontophoretically into descending axons of 2 HCN-activated inhibitory VOC neurons which were identified by stimulation of the i-HCN and the i-AB nucleus. Axon collaterals were ramified from a stem axon in the ventral funiculus, and entered the gray matter and spread in the laminae VIII and IX. Terminal boutons were distributed over the medial and the ventromedial parts of the vental horn in the C1 segment.

Lower lumbar branching of caudal medullary expiratory neurons of the cat

Extracellular spike activities of medullary expiratory (E) neurons in the caudal ventral respiratory group were recorded in cats anesthetized with sodium pentobarbital. The majority of E neurons extended their axons in the lower lumbar or the sacral segments and distributed collaterals in L5-L7. These results suggest that E neurons are involved not only in respiratory activities but also in the respiratory modulated motor activities of the lower lumbar segments.

Convergence of ipsilateral semicircular canal inputs onto single vestibular nucleus neurons in cats.

Convergent inputs from the ipsilateral semicircular canal nerves onto single vestibular nucleus neurons were investigated in decerebrate cats using intracellular recording after selective stimulation of each ampullar nerve. One hundred and seventy-four neurons were activated by stimulating the anterior semicircular (AC) and/or posterior semicircular canal (PC) nerves. These neurons were also antidromically stimulated and classified according to the pattern of their collateral projections to the oculomotor complex and the spinal cord. Four types were found: vestibulo-ocular (VO), vestibulospinal (VS), vestibulo-oculospinal (VOS), and vestibular (V) neurons, the latter of which were not activated by stimulation of either the oculomotor complex or the spinal cord. Of 174 AC- and/or PC-activated vestibular nucleus neurons, 32 (18%) received convergent inputs from both nerves. These convergent neurons included 11 VS, 6 VOS, and 15 V neurons. We found no VO neurons with convergent input. The vast majority (82%) of AC/PC-activated VS and VOS convergent neurons received excitatory inputs from both nerves, 12% received reciprocal inputs (i.e., excitatory from one and inhibitory from the other), and the remaining neurons received inhibitory inputs from both nerves. By stimulating the horizontal semicircular (HC) and/or PC nerves, 183 neurons were activated. Of these, 44 (24%) received convergent inputs from both nerves. These convergent neurons included 19 VS, 5 VOS, 2 VO, and 18 V neurons. Approximately one-half (46%) of HC/PC-activated VS and VOS convergent neurons received excitatory inputs from both nerves and 42% received reciprocal inputs, and the remaining neurons received inhibitory inputs from both nerves. In both nerve pairs, the percentage of VS neurons was higher (AC/PC, 34%; HC/PC, 43%) than that of VOS or VO neurons. Approximately half of these convergent neurons were located in the lateral nucleus. These results suggest that, during mixed angular head accelerations, the vestibulocollic reflex may be partly accomplished by VS and VOS convergent neurons.