Vertical semicircular canal inputs to cat extraocular motoneurons

Summary Synaptic 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.Abbreviations i- Ipsilateral to the recorded motoneuron - c- Contralateral to the recorded motoneuron - ACN Ampullary nerve of the anterior semicircular canal - HCN Ampullary nerve of the horizontal semicircular canal - PCN Ampullary nerve of the posterior semicircular canal - IO Inferior oblique - IR Inferior rectus - LR Lateral rectus - MR Medial rectus - SO Superior oblique - SR Superior rectus - EPSP Excitatory postsynaptic potential - IPSP Inhibitory postsynaptic potential - PSP Postsynaptic potential - MLF Medial longitudinal fasciculus     

Branching pattern and properties of vertical- and horizontal-related excitatory vestibuloocular neurons in the cat

1. The axonal trajectories of excitatory vestibuloocular neurons and their synaptic contacts with extraocular motoneurons were studied by means of spike-triggered signal averaging and microstimulation techniques. A majority of the excitatory neurons related to the vertical semicircular canals were located in the border of the descending and medial nuclei and the rostral half of the descending nucleus. 2. Individual vestibuloocular neurons activated by stimulation of the ampullary nerve of the anterior semicircular canal excited motoneurons within both the contralateral inferior oblique and contralateral superior rectus motoneuron pools. 3. Individual vestibuloocular neurons receiving input from the ampullary nerve of the posterior semicircular canal excited motoneurons in both the contralateral trochlear nucleus and contralateral inferior rectus motoneuron pools. The branching pattern of single vestibuloocular neurons activated by the anterior and posterior canals probably underlies conjugate eye movement during vertical head rotation. 4. Time to peak and shape indices of unitary excitatory postsynaptic potentials (EPSPs) suggested that the location of the synaptic contact of vestibuloocular neurons was on the soma or proximal dendrites of the target extraocular motoneurons. 5. In contrast, we did not find conclusive evidence that single vestibuloocular neurons receiving input from the horizontal semicircular canal give off axon collaterals to motoneurons innervating both the contralateral lateral rectus and the ipsilateral medial rectus muscles. Projection of horizontal vestibuloocular neurons to motoneurons supplying individual muscles might be useful for convergence during horizontal head movement.     

The organization of the vestibulo-oculomotor and trochlear reflex pathways in the rabbit

Summary Intracellular and extracellular responses were recorded with glass micro-electrodes from motoneurons in the IIIrd and IVth cranial nuclei of anesthesized rabbits. Five subgroups of neurons innervating the superior rectus (SR), inferior oblique (IO), inferior rectus (IR), medial rectus (MR), and superior oblique (IVth) extraocular muscles were identified by their antidromic activation from the branches of the IIIrd and IVth cranial nerves. The relative positions of the subgroups thus determined were consistent with the histological data on the rabbit. In the SR, IO, IR, and IVth subgroups the effects of ipsilateral VIIIth nerve stimulation were inhibitory, producing disynaptic IPSPs, while the effects of contralateral VIIIth nerve stimulation were excitatory, producing disynaptic EPSPs. In the MR subgroup, however, a mixture of EPSPs and IPSPs was produced by VIIIth nerve stimulation: this was particularly clear on the ipsilateral side. Sites relaying these VIIIth nerve effects to each of the five subgroups were explored by direct stimulation of various brain stem sites. Stimulation of the superior vestibular nucleus (SV) produced IPSPs monosynaptically in all five subgroups on the ipsilateral side as well as in the contralateral MR subgroup. Stimulation of the medial vestibular nucleus (MV) produced EPSPs monosynaptically in all of the five subgroups on the contralateral side as well as in the ipsilateral MR subgroup. Stimulation of the brachium conjunctivum (BC) also produced EPSPs monosynaptically in the contralateral SR, IO, and IR subgroups. Further, while the recording electrode was placed within each of the five subgroups to observe the extracellular potentials corresponding to the intracellularly recorded IPSPs and EPSPs, the medulla and cerebellum were systematically tracked with a monopolar stimulating electrode. It was thus confirmed that the SV is the sole inhibitory relay site, while excitation is relayed by both the MV and the BC. The origin of the BC pathway was traced to the Y-Group for the IO, to the lateral nucleus of the cerebellum (LN) for the IR, and to both the Y-Group and the LN for the SR subgroup.     

Synaptic organization of the tectal-facial pathways in the cat. I. Synaptic potentials following collicular stimulation

1. The synaptic pathways underlying tectal influence over pinna movements were studied using an acute electrophysiological approach. Under pentobarbital anesthesia, postsynaptic potentials were recorded intracellularly in antidromically identified, cat facial motoneurons following electrical stimulation of the superior colliculus. How collicular topography is reflected in these synaptic potentials was examined using multiple stimulation sites. The pathways responsible for tectally evoked synaptic potentials were studied by making acute brain stem lesions and by intra-axonal horseradish peroxidase (HRP) staining. 2. Monosynaptic excitatory potentials (EPSPs) with latencies ranging from 0.7 to 1.1 ms and amplitudes that were always less than 1 mV were recorded in motoneurons following stimulation of the contralateral superior colliculus. Larger disynaptic EPSPs ranging in latency from 1.2 to 2.0 ms were recorded both in isolation and in association with monosynaptic EPSPs. In addition, disynaptic inhibitory synaptic potentials (IPSPs) with latencies ranging from 1.5 to 2.5 ms were observed, often in combination with monosynaptic EPSPs. Both disynaptic EPSPs and IPSPs were graded, augmented by multiple stimuli and found in all categories of motoneurons. 3. Stimulation of the ipsilateral superior colliculus produced nearly the same spectrum of potentials and latencies as did contralateral tectal stimulation. Occlusion between ipsi- and contralaterally evoked IPSPs suggests there might be a common element in the inhibitory disynaptic pathways. 4. More discrete populations of facial motoneurons were investigated. Specifically, motoneurons innervating the platysma and orbicularis oculi muscles, the intrinsic ear muscles, and muscles that move the vibrissae all displayed tectally elicited mono- and di-synaptic potentials. Collicular input was not restricted to motoneurons involved in orienting the pinnae. 5. The presence, polarity, and amplitude of the synaptic potentials evoked in individual facial motoneurons exhibited variations that were related to the site of stimulation in either the ipsi- or contralateral colliculus. These variations are compatible with the idea that the collicular input to facial motoneurons is topographically organized. 6. Acute lesions at the level of the superior olive indicated that the pathway producing the contralateral monosynaptic EPSPs runs, near the midline, ipsilateral to the target facial nucleus, whereas the contralateral disynaptic and the ipsilateral mono- and disynaptic pathways lie further lateral.(ABSTRACT TRUNCATED AT 400 WORDS)     

The vestibulo-ocular reflex arc in the newborn kitten

Summary Field potentials and postsynaptic potentials were recorded in the vestibular and abducens nuclei and neurons following vestibular nerve stimulation in anesthetized newborn kittens (within 72 h after birth). Stimulation of the ipsilateral vestibular nerve evoked an initial P wave and an N₁ field potential in the vestibular nuclei. No N₂ potential was evoked. Latencies of the peak of the P wave, the onset and the peak of the N₁ potential were 0.99±0.16 ms, 1.66±0.18 ms, and 2.51±0.23 ms, respectively. Ipsilateral vestibular nerve stimulation evoked monosynaptic excitatory postsynaptic potentials (EPSPs) and polysynaptic inhibitory postsynaptic potentials (IPSPs) in vestibular nuclear neurons. Stimulation of the contralateral vestibular nerve evoked polysynaptic IPSPs in vestibular nuclear neurons. In abducens motoneurons, ipsilateral vestibular nerve stimulation evoked monosynaptic EPSPs and disynaptic IPSPs; contralateral vestibular nerve stimulation produced disynaptic EPSPs. We conclude that short circuit pathways of the vestibul-ovestibular and vestibulo-ocular reflex arc are present in the kitten already at birth.Supported by the Japanese Ministry of Education, Science, and Culture Grants-in-Aid for Scientific Research nos. 572 140 30 and 575 700 53     

Pathways for the vestibulo-ocular reflex excitation arising from semicircular canals of rabbits

Summary In anesthetized albino rabbits, ampullary branches of the vestibular nerve were stimulated electrically. Prominent and stable reflex contraction was induced in extra-ocular muscles by applying single current pulses of relatively long duration, 3–5 msec. Survey with a glass microelectrode revealed that, during application of relatively wide pulses to a canal, primary vestibular fibers discharged impulses repetitively at a rate as high as 300–1400/sec and that after being transmitted across second-order vestibular neurons these impulses built up summated EPSPs in oculomotor neurons, large enough to trigger off motoneuronal discharges. From each semicircular canal, prominent reflex contraction was evoked selectively in two muscles; from the anterior canal in the ipsilateral superior rectus and contralateral inferior oblique; from the horizontal canal in the ipsilateral medial rectus and contralateral lateral rectus; and from the posterior canal in the ipsilateral superior oblique and contralateral inferior rectus. Acute lesion experiments indicated that signals for this excitation reached IIIrd and IVth nuclei via three different pathways; from the anterior canal through the ipsilateral brachium conjunctivum, from the horizontal canal through the ipsilateral fasciculus longitudinalis medialis and from the posterior canal through the contralateral fasciculus longitudinalis medialis.This work was supported by a grant from Educational Ministry of Japan (844021).     

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.     

Sacculo-ocular reflex connectivity in cats

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

Synaptic linkage in the vestibulo-ocular and cerebello-vestibular pathways to the VIth nucleus in the rabbit

Summary Intra- and extra-cellular responses were recorded with glass microelectrodes from motoneurons in the VIth cranial nuclei of anesthesized rabbits. VIth nucleus motoneurons were identified by their antidromic activation from the VIth nerve. In these motoneurons stimulation of the ipsilateral VIIIth nerve produced IPSPs with disynaptic latencies (mean and S.D., 1.08 ± 0.1 msec) while stimulation of the contralateral VIIIth nerve produced EPSPs with disynaptic latencies (mean and S.D., 1.20 ± 0.18 msec). Correspondingly, direct stimulation of the ipsilateral medial vestibular nucleus (MV), produced IPSPs with monosynaptic latencies (mean and S.D., 0.61±0.15 msec) while direct stimulation of the contralateral MV produced EPSPs with monosynaptic latencies (mean and S.D., 0.61±0.09 msec). Further, with the recording electrode placed within the VIth nucleus to observe the extracellular potentials corresponding to the intracellularly recorded IPSPs and EPSPs, the medulla was systematically tracked with a monopolar stimulating electrode. It was demonstrated that the inhibitory relay cells could be effectively stimulated in the rostral half of the ipsilateral MV and the excitatory relay cells in the rostral half of the contralateral MV.Pharmacological investigation suggested that the inhibitory transmitter involved in the vestibular inhibition is gamma amino-butyric acid or a related substance.Electric stimulation of the flocculus produced a prominant depression in the inhibitory vestibulo-ocular reflex pathway to the VIth nucleus, while the excitatory pathway was free of any similar flocculus inhibition.     

Reticulospinal excitation and inhibition of neck motoneurons

Summary Responses of neck motoneurons to electrical stimulation of the pontomedullary reticular formation were recorded intracellularly in cerebellectomized cats anesthetized with chloralose. Stimulation of nucleus reticularis (n.r.) ventralis and the dorsal part of n.r. gigantocellularis evoked short latency, monosynaptic inhibitory postsynaptic potentials (IPSPs) in the majority of motoneurons supplying the ipsilateral splenius, biventer cervicis and complexus muscles and in 25% of motoneurons projecting in the ipsilateral spinal accessory nerve. Monosynaptic IPSPs were also evoked by stimulating the medial longitudinal fasciculus (MLF) but lesion and collision experiments indicated that these IPSPs were independent of those evoked by reticular stimulation. Monosynaptic IPSPs were also occasionally observed following stimulation of the contralateral reticular formation, especially of the dorsal part of n.r. gigantocellularis.Monosynaptic excitatory postsynaptic potentials (EPSPs) were evoked in all classes of neck motoneurons studied by stimulation of n.r. pontis caudalis, gigantocellularis and ventralis. Each reticular nucleus appeared to contribute to this excitation. The excitation was bilateral but large monosynaptic EPSPs were most often seen in motoneurons ipsilateral to the stimulus site. Data indicated that pontine EPSPs were mediated by ventromedial reticulospinal fibers while medullary EPSPs were mediated by ventrolateral reticulospinal fibers. Neck motoneurons thus receive at least three distinct direct reticulospinal inputs, two excitatory and one inhibitory.Supported in part by grants NSF BMS 75-00487 and NIH NS 02619Recipient of N.I.H. Fellowship 1 F32 NS 05027     

Vestibuloocular reflex of the adult flatfish. III. A species-specific reciprocal pattern of excitation and inhibition

In juvenile flatfish the vestibuloocular reflex (VOR) circuitry that underlies compensatory eye movements adapts to a 90 degrees relative displacement of vestibular and oculomotor reference frames during metamorphosis. VOR pathways are rearranged to allow horizontal canal-activated second-order vestibular neurons in adult flatfish to control extraocular motoneurons innervating vertical eye muscles. This study describes the anatomy and physiology of identified flatfish-specific excitatory and inhibitory vestibular pathways. In antidromically identified oculomotor and trochlear motoneurons, excitatory postsynaptic potentials (EPSPs) were elicited after electrical stimulation of the horizontal canal nerve expected to provide excitatory input. Electrotonic depolarizations (0.8-0.9 ms) preceded small amplitude (<0.5 mV) chemical EPSPs at 1.2-1.6 ms with much larger EPSPs (>1 mV) recorded around 2.5 ms. Stimulation of the opposite horizontal canal nerve produced inhibitory postsynaptic potentials (IPSPs) at a disynaptic latency of 1.6-1.8 ms that were depolarizing at membrane resting potentials around -60 mV. Injection of chloride ions increased IPSP amplitude, and current-clamp analysis showed the IPSP equilibrium potential to be near the membrane resting potential. Repeated electrical stimulation of either the excitatory or inhibitory horizontal canal vestibular nerve greatly increased the amplitude of the respective synaptic responses. These observations suggest that the large terminal arborizations of each VOR neuron imposes an electrotonic load requiring multiple action potentials to maximize synaptic efficacy. GABA antibodies labeled axons in the medial longitudinal fasciculus (MLF) some of which were hypothesized to originate from horizontal canal-activated inhibitory vestibular neurons. GABAergic terminal arborizations were distributed largely on the somata and proximal dendrites of oculomotor and trochlear motoneurons. These findings suggest that the species-specific horizontal canal inhibitory pathway exhibits similar electrophysiological and synaptic transmitter profiles as the anterior and posterior canal inhibitory projections to oculomotor and trochlear motoneurons. Electron microscopy showed axosomatic and axodendritic synaptic endings containing spheroidal synaptic vesicles to establish chemical excitatory synaptic contacts characterized by asymmetrical pre/postsynaptic membrane specializations as well as gap junctional contacts consistent with electrotonic coupling. Another type of axosomatic synaptic ending contained pleiomorphic synaptic vesicles forming chemical, presumed inhibitory, synaptic contacts on motoneurons that never included gap junctions. Altogether these data provide electrophysiological, immunohistochemical, and ultrastructural evidence for reciprocal excitatory/inhibitory organization of the novel vestibulooculomotor projections in adult flatfish. The appearance of unique second-order vestibular neurons linking the horizontal canal to vertical oculomotor neurons suggests that reciprocal excitation and inhibition are a fundamental, developmentally linked trait of compensatory eye movement circuits in vertebrates.     

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.     

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.     

Direct excitatory and inhibitory synaptic inputs from the medial mesodiencephalic junction to motoneurons innervating extraocular oblique muscles in the cat

Summary This study investigated the nature of synaptic inputs from the Forel's field H (FFH) in the medial mesodiencephalic junction to inferior oblique (IO) motoneurons in the oculomotor nucleus and superior oblique (SO) motoneurons in the trochlear nucleus in anesthetized cats, using intracellular recording techniques. Stimulation of the FFH induced monosynaptic EPSPs in IO motoneurons on both sides. Paired stimulation of the ipsilateral FFH and contralateral vestibular nerve substantiated that the FFH-induced EPSPs were caused mainly by direct excitatory fibers from the FFH to IO motoneurons and partly by axon collaterals of excitatory neurons in the vestibular nuclei. Among parts of the FFH, the medial part was most effective for producing the EPSPs. Systematic tracking with the stimulating electrode in and around the FFH revealed that effective sites of stimulation inducing negative field potentials in the IO subdivision of the oculomotor nucleus, identified as extracellular counterparts of the EPSPs in IO motoneurons, were also located in the interstitial nucleus of Cajal, nearby reticular formation and posterior commissure, besides within and near the medial part of the FFH. Areas far rostral, dorsal and ventral to the FFH were ineffective. EPSP-IPSPs or EPSPs were mainly induced in SO motoneurons on both sides by FFH stimulation. Latencies of these EPSPs and IPSPs were close to those of the EPSPs in IO motoneurons, indicating their monosynaptic nature. Effective stimulation sites for inducing these synaptic potentials overlapped those for the EPSPs in IO motoneurons. Based on these results, it was suggested that excitatory and inhibitory premotor neurons directly controlling IO and SO motoneurons were located within and near the medial part of the FFH.     

Connections between utricular nerve and neck flexor motoneurons of decerebrate cats

We studied the circuitry between the utricular (UT) nerve and ventral neck motoneurons innervating the longus capitis (LC), a neck flexor muscle, in decerebrate cats. We recorded intracellularly from 63 LC (ipsilateral 37, contralateral 26) motoneurons in C1 and C2 segments. UT nerve stimulation evoked disynaptic, excitatory postsynaptic potentials in all ipsilateral LC motoneurons, and inhibitory postsynaptic potentials that were at least trisynaptic in almost all contralateral LC motoneurons. UT effects on neck motoneurons innervating muscles involved in flexion and lateral turning are similar to the connections between the UT nerve and neck extensor motoneurons. These neuron circuits may play a role in fixing the head and the neck to the body during horizontal linear acceleration.     

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

Summary 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. In some cases, small collaterals crossed the midline within the oculomotor nucleus to terminate in the inferior rectus subdivision on the contralateral side. The axon proceeded further rostral to project to the interstitial nucleus of Cajal and beyond. The main termination sites of posterior canal neurons were in the superior rectus and inferior oblique subdivisions of the oculomotor nucleus. Minor collaterals were also observed to reach the midline area within the oculomotor nucleus, however, prospective contralateral termination sites could not be identified. More rostral projections were found in the interstitial nucleus of Cajal. The described axonal arborization of second order vestibular neurons reflects the organization of intrinsic coordinate systems as exemplified by the geometry of the semicircular canal and the extraocular muscle planes. These neurons are interpreted to provide a matrix for coordinate system transformation, i.e. from vestibular into oculomotor reference frames, and to play a role in gaze control and related reflexes by distributing their signals to multiple termination sites.Abbreviations DV descending vestibular nucleus - INC interstitial nucleus of Cajal - INT nucleus intercalatus - IQ inferior oblique subdivision - LV lateral vestibular nucleus - MLF medial longitudinal fasciculus - MRF medullary reticular formation - MV medial vestibular nucleus - nVII facial nerve - PH nucleus praepositus hypoglossi - PRF pontine reticular formation - RO nucleus Roller - SR superior rectus subdivision - SV superior vestibular nucleus - III oculomotor nucleus - IV trochlear nucleus - VI abducens nucleus - VII facial nucleus - XII hypoglossal nucleus Supported by NIH grants EY04613 and NS02619     

Direct projections from vestibular nuclei to facial nucleus in cats

Postsynaptic potentials were recorded from motoneurons in the facial nucleus in response to stimulation of the vestibular and trigeminal nerves. The motoneurons were identified by antidromic activation from their peripheral axons. Disynaptic excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) and mixed EPSP/IPSPs were recorded in response to vestibular nerve stimulation, ranging in latency from 0.9 to 2.1 ms, with most at 1.5 ms. Activity in secondary vestibular axons recorded within the facial nucleus occurred at a latency of 0.7-1.1 ms. The amplitudes of the vestibular postsynaptic potentials were small, generally less than a millivolt, but double shocks produced marked summation. The average time to peak of ipsilateral vestibular EPSPs, 1.1 ms, was faster than that of either ipsilateral IPSPs, 1.6 ms, or contralateral EPSPs, 1.4 ms. The double-spiked vestibular activity was detectable in double-peaked PSPs. Disynaptic EPSPs, ranging in latency from 2.0 to 3.0 ms, were recorded in response to trigeminal nerve stimulation. The average time to peak was 1.3 ms. The multiple-spiked activity of the trigeminal neurons was detectable in multipeaked EPSPs. Inhibitory ipsilateral effects (Vi IPSPs) were recorded twice as often as excitatory ipsilateral effects (Vi EPSPs), being found in 29% versus 15% of the motoneurons. Contralateral effects were found in 13% of the motoneurons studied, and almost all were excitatory. Analysis of synaptic potential shapes suggested that the excitatory and inhibitory vestibular synapses probably contact distal dendrites preferentially, with the excitatory connections being somewhat closer to the soma. The trigeminal inputs probably contact the facial motoneurons more extensively near the soma. Horseradish peroxidase was injected into the facial nucleus, and retrograde uptake by vestibular neurons was studied. The majority of filled vestibular neurons was ipsilateral to the injection site, especially in the medial vestibular nucleus, ventral y group, and supravestibular nucleus. On the contralateral side, filled vestibular cells were found almost exclusively in the medial nucleus. Filled cells were also noted in the trigeminal nucleus, predominantly ipsilaterally at all rostrocaudal levels. We have demonstrated monosynaptic projections to facial motoneurons from both vestibular and trigeminal nuclei. The trigeminal input is likely to be involved in facial reflexes, especially blinking and grimacing. The afferent vestibular population overlaps that going to the oculomotor and cervical motoneurons; these projections may be collaterals of single vestibular neurons.4+.     

Synaptic actions of cutaneous A delta and C fibers on primate hindlimb alpha-motoneurons

Postsynaptic potentials evoked in hindlimb alpha-motoneurons by stimulation of a cutaneous nerve (sural) with finely graded stimulus strengths were analyzed in the primate, monitoring the spinal cord potentials and afferent nerve volleys in the sural nerve. It was observed that activities in A alpha beta, A delta and C fibers of the cutaneous nerve elicited characteristic excitatory and/or inhibitory postsynaptic potentials (EPSPs and/or IPSPs) with different latencies and durations in extensor and flexor motoneurons. Volleys in A delta fibers of the cutaneous nerve produced EPSPs in 57% of flexor and 31% of extensor motoneurons tested, whereas IPSPs were produced by A delta volleys in 41% of flexor and 62% of extensor motoneurons. EPSPs with longer latencies and longer durations were evoked by cutaneous C fiber volleys in 55% of flexor and 34% of extensor motoneurons, whereas IPSPs due to C volleys were recorded in 9% of flexor and 14% of extensor motoneurons. A alpha beta and A delta volleys caused motoneurons to fire in several instances, and some motoneurons discharged repetitively during the depolarizations evoked by activities in C fibers of the nerve. Central latency for transmission in interneuronal chains in the spinal cord was estimated from the onset of the cord potential (N3 wave) to the onset of the postsynaptic potential evoked by A delta volleys. Ranges of central latencies of the EPSPs and IPSPs evoked by A delta volleys were 2.0-7.0 ms and 3.5-8.5 ms, respectively. It is postulated that there may be at least two interneurons interposed in the excitatory reflex pathway from A delta afferent fibers to motoneurons and the A delta inhibitory pathway may involve longer interneuronal chains. In a few motoneurons, however, sural volleys with strengths sufficient to activate A delta fibers produced EPSPs with a central latency of about 1 ms, suggesting activation of a disynaptic segmental pathway with one interposed interneuron. Stimulation of the sural nerve with strengths sufficient to activate cutaneous C fibers produced slow negative cord dorsum potentials with long latencies. It is proposed that primate motoneurons, which show characteristic postsynaptic potentials evoked by cutaneous A delta and C fiber volleys, may provide a suitable model for analyzing the role of high threshold cutaneous afferent fibers not only in the flexor withdrawal reflex but also in motor control functions.     

Axonal trajectories of inhibitory vestibulocollic neurons activated by the anterior semicircular canal nerve and their synaptic effects on neck motoneurons in the cat

Summary Somatic location, axonal trajectories and synaptic effects of inhibitory vestibulocollic neurons which were activated by selective stimulation of the anterior semicircular canal nerve (ACN) were studied in the anesthetized cat. ACN stimulation evoked disynaptic inhibitory postsynaptic potentials (IPSPs) in neck flexor motoneurons. This was seen in all the (64/64) tested motoneurons innervating the ipsilateral (i-) longus capitis (LC) and the i-sternocleidomastoideus (SCM) muscles and in 86% (38/44) of the motoneurons innervating the contralateral (c-) LC muscle. The inhibitory relay neurons, identified by orthodromic and antidromic responses to stimulation of the ACN and the i- and c-LC motoneuron pools, were classified as VCi (vestibulocollic neurons sending an axon to the i-LC motoneuron pool) and VCc (vestibulocollic neurons sending an axon to the c-LC motoneuron pool) neurons. Neither VCi nor VCc neurons were activated antidromically by localized stimulation of the ascending medial longitudinal fasciculus (asc. MLF) or the 3rd nuclei. They were located in the medial, descending and ventral lateral vestibular nuclei. It was also observed that VCi neurons produced unitary IPSPs in i-LC and i-SCM motoneurons in the C1 segment. Inhibitory synapses were estimated to be on the cell somata and/or the proximal dendrites of the motoneurons.     

Convergence pattern of uncrossed excitatory and inhibitory semicircular canal-specific inputs onto second-order vestibular neurons of frogs

Second-order vestibular neurons of frogs receive converging monosynaptic excitatory and disynaptic excitatory and inhibitory inputs following electrical pulse stimulation of an individual semicircular canal nerve on the ipsilateral side. Here we revealed, in the in vitro frog brain, disynaptic inhibitory postsynaptic potentials (IPSPs) by bath application of antagonists specific for glycine or gamma-aminobutyric acid-A (GABA(A)) receptors. Differences in the response parameters between disynaptic IPSPs and excitatory postsynaptic potentials (EPSPs) suggested that disynaptic IPSPs originated from a more homogeneous subpopulation of thicker vestibular nerve afferent fibers than mono- or disynaptic EPSPs. To investigate a possible size-related organization of these canal-specific, parallel pathways, we combined long-lasting anodal currents of variable intensities with strong cathodal test pulses, to block pulse-evoked responses reversibly in a graded manner according to the size-related sensitivity of vestibular nerve afferent fibers. The anodal current intensity required to block a particular response component was about 15 times lower than the strength of the cathodal test pulse that activated this response component. These large threshold differences were exploited for a selective anodal suppression of the responses from thick vestibular nerve afferent fibers. In fact, response components known to originate exclusively from thick-caliber afferent fibers such as the electrically transmitted monosynaptic EPSP component exhibited the lowest thresholds for cathodal test pulses and were the first to disappear in the presence of small anodal polarization steps. Thresholds for the activation/inactivation of responses and current intensities required for response saturation/blockade were used to assess the fiber spectrum that evoked the different response components. Mono- and disynaptic EPSPs appeared to originate from a broad spectrum of thick and thin vestibular nerve afferent fibers. The spectrum of afferent fibers that activated disynaptic IPSPs on the other hand was more homogeneous and consisted of thick and intermediate fibers. Such a canal-specific and fiber type-related organization of converging inputs of second-order vestibular neurons via feedforward projections was shown for the first time by this study in frogs, but might also prevail in mammals. Similar differences in these feedforward pathways have been proposed earlier in a vestibular side-loop model. Our results are consistent with the basic assumptions of this model and relate to the processing and tuning of dynamic vestibular signals.