Yoshio Uchino

Axonal trajectories of posterior canal-activated secondary vestibular neurons and their coactivation of extraocular and neck flexor motoneurons in the cat.

SummaryUnit activities of 148 secondary vestibular neurons related to the posterior semicircular canal were recorded extracellularly in anesthetized cats. Axonal projections of these neurons were examined by their antidromic responses to stimulation of the excitatory target motoneurons of the contralateral (c-) inferior rectus muscle (IR) and bilateral (bi-) motoneuron pools of longus capitis muscles, neck flexors, in the C1 segment (C1LC). The neurons were classified into 4 groups according to their axonal projections. The first group of neurons, termed vestibulo-oculo-collic (VOC) neurons, sent axon collaterals both to the c-IR motoneuron pool and to the c-C1LC motoneuron pool. The majority of them (72%) were located in the descending nucleus. The second group of neurons were termed vestibuloocular (VO) neurons and sent their axons to the c-IR motoneuron pool but not to the cervical cord. Most of them (86%) were located in the medial nucleus. The third group of neurons, termed vestibulo-collic (contralateral) (VCc) neurons, sent axons to the cC 1LC motoneuron pool via the contralateral ventral funiculus but not to the oculomotor nuclei. They were mostly (75%) found in the descending nucleus. The last group of neurons were vestibulo-collic (ipsilateral) (VCi) neurons, which gave off axons to the ipsilateral (i-) C1LC motoneuron pool via the ipsilateral ventral funiculus but not to the oculomotor nuclei. One of them also sent an axon collateral to the c-C1LC motoneuron pool. The majority of them (74%) were located in the ventral part of the lateral nucleus. It was also observed in some of the VOC and VCi neurons that they produced unitary EPSPs in the c-C1LC and i-C1LC motoneurons, respectively. Their synaptic sites were estimated to be on the cell somata and/or proximal dendrites of the motoneurons.

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.

Properties of secondary vestibular neurons fired by stimulation of ampullary nerve of the vertical, anterior or posterior, semicircular canals in the cat.

Experiments on cats were performed to study the pathway and location of the secondary vestibulo-ocular neurons in response to stimulation of the ampullary nerves of the vertical, anterior or posterior, semicircular canals. Experiments on the medial longitudinal fasciculus transection disclosed that vertical canal-evoked, disynaptic excitation and inhibition were transmitted to the extraocular motoneurons through the contra- and ipsilateral medial longitudinal fasciculus respectively. Secondary vestibular neurons, which receive input from the ampullary nerve of the vertical semicircular canals and send their axons to contralateral medial longitudinal fasciculus, were intermingled in the rostral half of the descending and lateral part of the medial vestibular nuclei. A direct excitatory connection of some of these neurons to the target extraocular motoneurons was confirmed by means of a spike-triggered signal averaging technique. It was also found that neurons activated by antidromic stimulation of ipsilateral medial longitudinal fasciculus were located in the superior vestibular nucleus, some of which made direct inhibitory connections to the target extraocular motoneurons. Both excitatory and inhibitory vestibuloocular neurons made synaptic contact in about half of the impaled target motoneurons.

Vertical semicircular canal inputs to cat extraocular motoneurons

SummarySynaptic potentials were recorded in identified extraocular motoneurons in anesthetized cats, following stimulation of ampullary nerves of the anterior and posterior semicircular canals.Superior rectus motoneurons received disynaptic EPSPs and IPSPs following stimulation of the two ampullary nerves of the anterior and posterior semicircular canals, respectively. In the inferior rectus motoneurons, the effects of anterior and posterior semicircular canal stimulation were a mirror image of those on superior rectus motoneurons.Inferior oblique motoneurons developed disynaptic EPSPs and IPSPs following stimulation of the ampullary nerves of the contralateral anterior and ipsilateral posterior semicircular canals, respectively. In addition, some inferior oblique motoneurons displayed disynaptic IPSPs following stimulation of the contralateral ampullary nerve of the posterior semicircular canal. In the superior oblique (trochlear) motoneurons, disynaptic EPSPs and IPSPs were recorded after stimulation of the contralateral posterior and ipsilateral anterior semicircular canals, respectively.There was no significant connection between the ampullary nerves of the vertical semicircular canals and motoneurons innervating lateral and medial rectus muscles.

Horizontal canal input to cat extraocular motoneurons.

Synaptic potentials were recorded in identified extraocular motoneurons in the anesthetized cat, following stimulation of the horizontal canal nerve (HCN). Weak stimulation of the HCN evoked disynaptic EPSPs in ipsilateral medial rectus (i-MR), contralateral lateral rectus (c-LR) and disynaptic IPSPs in i-LR motoneurons. Weak stimulation of the HCN produced longer latency IPSPs (probably trisynaptic) in c-MR motoneurons. It is suggested that the HCN projects to an excitatory interneuron in the vestibular nucleus whose axon in turn projects to a third order inhibitory interneuron in the IIIrd nucleus which finally projects to c-MR motoneurons. Essentially there is no influence of the HCN stimulation on bilateral superior rectus (SR), inferior rectus (IR), superior oblique (SO) and inferior oblique (IO) motoneurons.

Superior vestibular nucleus neurones related to the excitatory vestibulo-ocular reflex of anterior canal origin and their ascending course in the cat☆

Stimulation of the superior vestibular nucleus and the anterior canal nerve evoked mono- and disynaptic excitatory postsynaptic potentials, respectively, in contralateral inferior oblique motoneurones of the cat. Combined stimulation revealed that the superior vestibular nucleus relayed excitatory anterior canal signals to the motoneurones. Thirty-six superior vestibular neurones receiving anterior canal inputs were activated antidromically by microstimulation of the contralateral inferior oblique motoneurone pool. Their axons ascended neither in the brachium conjunctivum nor in the medial longitudinal fasciculus, but proceeded rostrally in the ventral part of the brain stem.

The commissural inhibition on secondary vestibulo-ocular neurons in the vertical semicircular canal systems in the cat

The commissural inhibition on secondary vestibulo-ocular neurons (VOns) from the contralateral (c-) vertical canal system in the same geometric plane was studied in the anesthetized cat. The secondary VOns were identified by their orthodromic responses to stimulation of the ampullary nerves of the anterior (ACN) or posterior (PCN) semicircular canals and also by their antidromic responses to stimulation of the IIIrd and IVth nuclei. The majority of ACN-activated excitatory VOns in the descending and medial nuclei (32/36, 89%) and in the superior nucleus (20/23, 87%), received commissural inhibition from the c-PCN, while only few ACN-activated inhibitory VOns (3/35, 9%) in the superior nucleus received commissural inhibition from the c-PCN. On the other hand, all of the PCN-activated excitatory (50/50) and inhibitory (30/30) VOns in the vestibular nuclei received commissural inhibition following c-ACN stimulation.

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.

Vestibulo-ocular reflex from the posterior canal nerve to extraocular motoneurons in the cat

SummaryIn the anesthetized cat, the posterior canal nerve (PCN) was stimulated by electric pulses and synaptic responses were recorded intracellularly in the three antagonistic pairs of extraocular motoneurons. Pure reciprocal effects were obtained in the motoneurons innervating the antagonistic pair of ipsilateral oblique muscles and the antagonistic pair of contralateral vertical rectus muscles. These responses consisted of low threshold disynaptic excitatory postsynaptic potentials (EPSPs) in either the contralateral superior oblique (c-SO) (trochlear) or contralateral inferior rectus (c-IR) motoneurons and of disynaptic inhibitory postsynaptic potentials (IPSPs) in either the ipsilateral inferior oblique (i-IO) or ipsilateral superior rectus (i-SR) motoneurons. In addition, disynaptic IPSPs were also found in (i-SO) motoneurons. Mixtures of low threshold (dior trisynaptic) EPSPs and IPSPs were found in all other extraocular motoneurons except for the contralateral lateral rectus (c-LR) motoneurons. These results may afford a basis for the characteristic eye movements induced by vertical canal nerve stimulation.

Floccular influence on excitatory relay neurones of vestibular reflexes of anterior semicircular canal origin in the cat.

Floccular influence on excitatory vestibular reflex arcs of anterior semicircular canal origin was examined in the anaesthetized cat. Stimulation of the anterior semicircular canal nerve (ACN) evoked disynaptic excitatory postsynaptic potentials (EPSPs) in all sampled inferior oblique (IO), superior rectus (SR), and biventor cervicis (BIV) muscle motoneurones of the contralateral side. Conditioning stimulus to the flocculus depressed the amplitude of the EPSPs in both IO and SR motoneurones by 50% on the average but not in any BIV motoneurones. The excitatory vestibulo-ocular neurones identified by orthodromic and antidromic responses to stimulation of the ACN and the contralateral IO motoneurone pool, respectively, were classified as VOC (vestibulo-ocular neurones with axons descending to the cervical segment) or VO (vestibulo-ocular proper) neurones on the basis of whether or not they responded antidromically to stimulation of the spinal cord in the C1 segment. All of the VO neurones in the superior vestibular nucleus (n = 19) were inhibited from the flocculus while the activities of three-fourths of the VO neurones (36/48) in the other vestibular nuclei were not suppressed by floccular stimulation. In contrast, none of VOC neurones (n = 49) received floccular inhibition. Besides inhibition, floccular stimulation induced the antidromic or orthodromic responses in some VO and VOC neurones.