Excitatory input from interneurons in the abducens nucleus to medial rectus motoneurons mediating conjugate horizontal nystagmus in the cat

Summary A class of interneurons in the cat abducens nucleus was identified by its antidromic activation from the contralateral ascending MLF, disynaptic activation from the contralateral vestibular nerve and type II response to rotation of the turntable. They were also activated antidromically from the contralateral oculomotor nucleus, the region of medial rectus motoneurons. Extracellular spikes of single interneurons, spontaneous or glutamate-driven, were used as triggers for perior post-spike averaging of three kinds of potentials. (1) The average of the extracellular field potentials within the contralateral oculomotor nucleus consisted of an early positive or positive-negative spike and a late, slow negative wave. The early spike was an action current caused by impulses along the axon of the interneuron. The late potential was the extracellular counterpart of unitary EPSPs. (2) The averaged membrane potential of contralateral medial rectus motoneurons revealed unitary EPSPs with monosynaptic latencies, evidence that interneurons were excitatory in nature. (3) The average of compound potentials of the contralateral medial rectus nerve showed a monosynaptic excitatory effect relevant to unitary EPSPs. This effect was observed with nearly all interneurons. All interneurons thus identified exhibited discharge patterns closely correlated with the activity of medial rectus motoneurons in both slow and quick phases of vestibular nystagmus. It was concluded that these interneurons controlled activities of contralateral medial rectus motoneurons associated with conjugate horizontal eye movements by their monosynaptic excitatory connections.     

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+.     

Properties and localization of the anterior semicircular canal-activated vestibulocollic neurons in the cat

Summary Unit activites of secondary vestibular neurons that selectively responded to stimulation of the anterior semicircular canal nerve (ACN) were recorded extracellularly in the anesthetized cat. Axonal pathways and projections in the spinal cord of the ACN-activated neurons were examined by recording their antidromic responses to stimulation of the lateral and medial vestibulospinal tracts (LVST and MVST), and the bilateral neck extensor motoneuron pools in the C₁segment (C₁dorsal rami [DR] motoneuron pools). In order to determine whether the neurons had ascending axon collaterals to the extraocular motoneurons, the contralateral (c-) inferior oblique (IO) motoneuron pool was also stimulated. Twenty-seven neurons sent their axons to the ipsilateral (i-) C₁DR motoneuron pool via the LVST without any projection to the extraocular motoneuron pool. All the cells except one were located in the ventral part of the lateral vestibular nucleus. This pathway produced monosynaptic EPSPs with short time-to-peak and short half-width in C₁DR motoneurons (16/16 motoneurons). Eight neurons sent axons to the i-C₁DR motoneuron pool via the MVST without any to the extraocular motoneuron pool. Cell somata were located in the descending nucleus or in the ventral part of the lateral nucleus. These neurons did not produce postsynaptic potentials (PSPs) in any C₁DR motoneurons. All thirty-five neurons sending axons to the c-C₁DR motoneuron pool have ascending axon collaterals to the c-IO motoneuron pool.     

Excitatory inputs to cerebellar dentate nucleus neurons from the cerebral cortex in the cat

Summary 1. In anesthetized cats, we investigated excitatory and inhibitory inputs from the cerebral cortex to dentate nucleus neurons (DNNs) and determined the pathways responsible for mediating these inputs to DNNs. 2. Intracellular recordings were made from 201 DNNs whose locations were histologically determined. These neurons were identified as efferent DNNs by their antidromic responses to stimulation of the contralateral red nucleus (RN). Stimulation of the contralateral pericruciate cortex produced excitatory postsynaptic potentials (EPSPs) followed by long-lasting inhibitory postsynaptic potentials (IPSPs) in DNNs. The most effective stimulating sites for inducing these responses were observed in the medial portion (area 6) and its adjacent middle portion (area 4) of the precruciate gyrus. Convergence of cerebral inputs from area 4 and area 6 to single DNNs was rare. 3. To determine the precerebellar nuclei responsible for mediation of the cerebral inputs to the dentate nucleus (DN), we examined the effects of stimulation of the pontine nucleus (PN), the nucleus reticularis tegmenti pontis (NRTP) and the inferior olive (IO). Systematic mapping was made in the NRTP and the PN to find effective low-threshold stimulating sites for evoking monosynaptic EPSPs in DNNs. Stimulation of either the PN or the NRTP produced monosynaptic EPSPs and polysynaptic IPSPs in DNNs. Using a conditioning-testing paradigm (a conditioning stimulus to the cerebral peduncle (CP) and a test stimulus to the PN or the NRTP) and intracellular recordings from DNNs, we tested cerebral effects on neurons in the PN and the NRTP making a monosynaptic connection with DNNs. Conditioning stimulation of the CP facilitated PN- and NRTP-induced monosynaptic EPSPs in DNNs. This spatial facilitation indicated that the excitatory inputs from the cerebral cortex to DNNs are at least partly relayed via the PN and the NRTP. 4. Stimulation of the contralateral IO produced monosynaptic EPSPs and polysynaptic IPSPs in DNNs. These monosynaptic EPSPs were facilitated by conditioning stimulation of the CP, strongly suggesting that the IO is partly responsible for mediating excitatory inputs from the cerebral cortex to the DN. A comparison was made between the latencies of IO-evoked IPSPs in DNNs and the latencies of IO-evoked complex spikes in Purkinje cells. Such a comparison indicated that the shortest-latency IPSPs evoked from the IO were not mediated via the Purkinje cells and suggested the pathway mediated by inhibitory interneurons in the DN. 5. The functional significance of the excitatory inputs from the PN and the NRTP to the DN is discussed in relation to the motor control mechanisms of the cerebellum.     

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.     

Supraspinal monosynaptic excitation and inhibition of thoracic back motoneurons

Summary The effects of brain stem stimulation on thoracic back motoneurons were studied in cats anesthetized with pentobarbital. The population sampled consisted of the extensors interspinales (IS), longissimus dorsi (LD) and spinalis dorsi (SD), and of unidentified (UIC) motoneurons. The location of the motoneurons, between Th 1 and Th 10, at widely varying distances from the stimulating electrode permitted linear regression analysis of the descending neural influences.EPSPs evoked by MLF stimulation in all types of motoneurons were produced by a pathway with an average conduction velocity in the thoracic cord of 127 m/sec, and were monosynaptic. IPSPs were also produced by MLF stimulation. The IPSPs in IS and UIC motoneurons were monosynaptic and were produced by a pathway with an average conduction velocity of 69 m/sec.Stimulation of Deiters' nucleus evoked short latency EPSPs in many motoneurons. EPSPs in LD and UIC motoneurons were shown to be monosynaptic, although latency scatter and sample size made accurate determination of vestibulospinal conduction velocity impossible.Stimulation of the labyrinth evoked disynaptic EPSPs and IPSPs in many cells, as previously observed in neck motoneurons. IPSPs were frequently produced by stimulation of the contralateral labyrinth, probably by a pathway with a relay in the contralateral medial vestibular nucleus. Ipsilateral stimulation usually produced EPSPs. The excitatory pathway relays in Deiters' nucleus and, we suggest, in the descending vestibular nucleus.Supported in part by a research grant from the Public Health Service (NSO2619).     

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     

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.     

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.     

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.     

Mono- and disynaptic pathways from Forel's field H to dorsal neck motoneurones in the cat

Summary 1. We analysed the synaptic actions produced by Forel's field H (FFH) neurones on dorsal neck motoneurones and the pathways mediating the effects. 2. Stimulation of ipsilateral FFH induced negative field potentials of several hundred microvolts with the latency of about 1.1 ms in the medial ponto-medullary reticular formation, being largest in the ventral part of the nucleus reticularis pontis caudalis (NRPC), and in the dorsal part of the nucleus reticularis gigantocellularis (NRG). 3. Stimulation of ipsilateral FFH induced excitatory postsynaptic potentials (EPSPs) in 90% (47/52) and inhibitory postsynaptic potentials (IPSPs) in 19% (10/52) of the reticulospinal neurones (RSNs) in the NRPC and the NRG. Latencies of the EPSPs and IPSPs were 0.7–3.0 ms, the majority of which were in the monosynaptic range. The monosynaptic connexions were confirmed by spike triggered averarging technique both in excitatory (n=4) and inhibitory (n=2) pathways. 4. Single stimulation of FFH induced EPSPs at the segmental latencies of 0.3–1.0 ms in neck motoneurones, which were clearly in the monosynaptic range. Repetitive stimulation of FFH produced marked temporal facilitation of EPSPs in neck motoneurones. The facilitated components of the EPSPs had a little longer latencies and their amplitude reached several times as large as that evoked by single stimulation in all the tested motoneurones. These facilitated excitations are assumed to be mediated by RSNs in the NRPC and NRG, since RSNs were mono- and polysynaptically fired by stimulation of FFH and they were previously shown to directly project to neck moteneurones. 5. EPSPs were induced in 91% (82/91) of motoneurones supplying m. biventer cervicis and complexus (BCC; head elevator), 10% (3/29) of motoneurones supplying m. splenius (SPL; lateral head flexor). Eikewise, stimulation of FFH produced EMG responses in BCC muscles, while not in SPL muscle. Thus FFH neurones produce excitations preferentially in BCC motoneurones. 6. Systematic tracking in and around FFH revealed that the effective sites for evoking above effects were in FFH and extended caudally along their efferent axonal course. 7. These results suggested that FFH neurones connect with neck motoneurones (chiefly BCC, head elevator) mono-, diand/or polysynaptically and are mainly concerned with the control of vertical head movements.     

Monosynaptic inhibition of neck motoneurons by the medial vestibular nucleus

Summary Stimulation of the brain stem in cats anesthetized with pentobarbital evoked short-latency IPSPs in many neck motoneurons. From the segmental delay of these IPSPs, and from comparison of their latencies with those of monosynaptic EPSPs evoked in the same motoneuron population by stimulation of the brain stem, it is concluded that the IPSPs are monosynaptic and are produced by descending inhibitory fibers.As many as thirteen electrodes were inserted into the medulla and pons to compare threshold stimuli required to evoke monosynaptic IPSPs from different locations. The points with the lowest threshold were in the medial vestibular nucleus and the medial longitudinal fasciculus. The IPSPs are apparently produced by fibers that originate in the medial vestibular nucleus and reach the upper cervical segments via the MLF.Electrical stimulation of the ipsilateral labyrinth often produces disynaptic IPSPs in neck motoneurons, very probably by means of a relay in the medial nucleus. This inhibitory pathway between labyrinth and neck motoneurons, together with the previously described excitatory pathway relaying in Deiters' nucleus, provides some of the pathways utilized by the labyrinth in regulation of head position.     

Direct excitation of neck motoneurons by interstitiospinal fibers

1. Responses of neck motoneurons to stimulation of the interstitial nucleus of cajal (INC) were recorded intracellularly in cats under chloralose anesthesia. When stimuli were applied within or close to the INC, short latency, monosynaptic excitatory postsynaptic potentials (EPSPs) were evoked in many neck motoneurons. Such EPSPs were not evoked by stimulating mesencephalic regions outside the INC. 2. Stimulation of the ipsilateral INC produced monosynaptic EPSPs consistently in biventer cervicis-complexus (BCC) motoneurons, while such EPSPs were observed in about two thirds of the splenius (SP) motoneurons and half of the trapezius (TR) motoneurons tested. Stimulation of the contralateral INC produced weak monosynaptic EPSPs in about half the BCC motoneurons and in a few SP and TR motoneurons. All types of motoneurons also received longer latency, apparently polysynaptic, PSPs from both INCs. In BCC and TR motoneurons these were mainly EPSPs, in SP, mixed excitatory and inhibitory PSPs. 3. Monosynaptic EPSPs evoked by INC stimulation were not eliminated by acute and chronic parasagittal and transverse lesions placed to interrupt the bifurcating axons of all vestibulospinal and many reticulospinal neurons. No significant collision was observed between EPSPs evoked by INC and vestibular or reticular stimulation. The EPSPs evoked by stimulation of the INC therefore appear to have been produced by activation of interstitiospinal neurons rather than by an axon reflex mechanism. 4. The properties of a number of interstitiospinal neurons were observed while recording extracellularly from the mesencephalon to map the location of the INC. One third of the interstitiospinal neurons activated antidromically from the C4 segment could also be activated antidromically from L1. These lumbar-projecting neurons had conduction velocities ranging from 15--123 m/s. Several interstitiospinal neurons sending axons to the ventral horn of the neck segments were identified and two of these were found to be branching neurons that projected both to the neck and to lower levels of the spinal cord.     

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     

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     

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     

Synaptic organization of the vestibulo-trochlear pathway

Summary Field and intracellular potentials evoked in the trochlear nucleus (TN) of the cat following stimulation of the ipsi and contralateral vestibular nerves (V_i, V_c) and the vestibular nuclei (VN) were recorded with microelectrodes.Single shock stimulation of either V_c or V_i evokes in the TN the presynaptic potentials, n₁ and n₂, which are generated by the action currents of repetitively firing axons of vestibular neurons reaching the TN via the medial longitudinal fascicle (MLF). In the case of V_c stimulation a slow negative potential (n₃) follows the presynaptic components of the field complex while a slow positive potential (p-wave) is evoked by V_i stimuli. The n₃ wave is composed of the excitatory synaptic and action currents generated in trochlear motoneurons (TMns) while the p-wave is produced by the inhibitory synaptic current. Disynaptic EPSPs and IPSPs are recorded intracellularly in TMns following V_c and V_i stimulation, respectively. Each synaptic potential shows a biphasic rising phase due to the synchronous n₁ and n₂ presynaptic barrage.On stimulation of the ipsilateral superior and contralateral medial vestibular nuclei, the latencies of the IPSPs and EPSPs, respectively, are reduced to the monosynaptic range. Thus, it has been directly demonstrated that the VN are the mediating links for both the short latency excitatory and inhibitory vestibuloocular reflexes. The above data suggest that IPSPs are for the most part generated at or near the soma of the motoneurons. As for the site of generation of the EPSPs, a predominantly dendritic origin is suggested.The organization of the neuronal circuitry is discussed in relation to the vestibular induced eye movements.     

Excitatory connections between neurons of the central cervical nucleus and vestibular neurons in the cat

 The central cervical nucleus (CCN) of the cat receives input from upper cervical muscle afferents, particularly primary spindle afferents. Its axons cross in the spinal cord, and while in the contralateral restiform body give off collaterals to the vestibular nuclei. In order to study the connections between CCN axons and vestibular neurons, we stimulated the area of the CCN in decerebrate cats while recording intra- or extracellularly from neurons in the contralateral vestibular nuclei. CCN stimulation evoked excitatory postsynaptic potentials (EPSPs) or extracellularly recorded firing in the lateral, medial and descending vestibular nuclei. The latency of EPSPs (mean 1.6 ms) was on average 0.4 ms longer than the latency of antidromic spikes evoked in the CCN by stimulation of the contralateral vestibular nuclei (mean 1.2 ms), demonstrating that the excitation was typically monosynaptic. The results provide further evidence that the CCN is an important excitatory relay between upper cervical muscle afferents and neurons in the contralateral vestibular nuclei. Received: 1 August 1996 / Accepted: 16 December 1996     

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.     

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.