Brainstem Neural Circuits Triggering Vertical Saccades and Fixation.

Neurons in the nucleus raphe interpositus have tonic activity that suppresses saccadic burst neurons (BNs) during eye fixations, and that is inhibited before and during saccades in all directions (omnipause neurons, OPNs). We have previously demonstrated via intracellular recording and anatomical staining in anesthetized cats of both sexes that OPNs are inhibited by BNs in the medullary reticular formation (horizontal inhibitory BNs, IBNs). These horizontal IBNs receive monosynaptic input from the caudal horizontal saccade area of the superior colliculus (SC), and then produce monosynaptic inhibition in OPNs, providing a mechanism to trigger saccades. However, it is well known that the neural circuits driving horizontal components of saccades are independent from the circuits driving vertical components. Thus, our previous results are unable to explain how purely vertical saccades are triggered. Here, we again apply intracellular recording to show that a disynaptic vertical IBN circuit exists, analogous to the horizontal circuit. Specifically, we show that stimulation of the SC rostral vertical saccade area produces disynaptic inhibition in OPNs, which is not abolished by midline section between the horizontal IBNs. This excludes the possibility that horizontal IBNs could be responsible for the OPN inhibition during vertical saccades. We then show that vertical IBNs in the interstitial nucleus of Cajal, which receive monosynaptic input from rostral SC, are responsible for the disynaptic inhibition of OPNs. These results indicate that a similarly functioning SC-IBN-OPN circuit exists for both the horizontal and vertical oculomotor pathways. These two IBN-mediated circuits are capable of triggering saccades in any direction.Significance Statement Saccades shift gaze to objects of interest, moving their image to the central retina, where it is maintained for detailed examination (fixation). During fixation, high gain saccade burst neurons (BNs) are tonically inhibited by omnipause neurons (OPNs). Our previous study showed that medullary horizontal inhibitory BNs (IBNs) activated from the caudal superior colliculus (SC) inhibit tonically active OPNs in order to initiate horizontal saccades. The present study addresses the source of OPN inhibition for vertical saccades. We find that OPNs monosynaptically inhibit vertical IBNs in the interstitial nucleus of Cajal during fixation. Those same vertical IBNs are activated by the rostral SC, and inhibit OPN activity to initiate vertical saccades.

Input-output organization of inhibitory neurons in the interstitial nucleus of Cajal projecting to the contralateral trochlear and oculomotor nucleus.

Neurons in the interstitial nucleus of Cajal (INC) that are known to be involved in eye and head movements are excitatory. We investigated the input-output organization of inhibitory INC neurons involved in controlling vertical saccades. Intracellular recordings were made in INC neurons activated antidromically by stimulation of the contralateral trochlear or oculomotor nucleus, and their synaptic input properties from the superior colliculi (SCs) and the contralateral INC were analyzed in anesthetized cats. Many INC neurons projected to the contralateral trochlear nucleus, Forel's field H, INC, and oculomotor nucleus, and mainly received monosynaptic excitation followed by disynaptic inhibition from the ipsi- and contralateral SCs. After sectioning the commissural connections between the SCs, these neurons received monosynaptic excitation from the ipsilateral medial SC and disynaptic inhibition via the INC from the contralateral lateral SC. Another group of INC neurons were antidromically activated from the contralateral oculomotor nucleus, INC and Forel's field H, but not from the trochlear nucleus, and received monosynaptic excitation from the ipsilateral lateral SC and disynaptic inhibition from the contralateral medial SC. The former group was considered to inhibit contralateral trochlear and inferior rectus motoneurons in upward saccades, whereas the latter was considered to inhibit contralateral superior rectus and inferior oblique motoneurons in downward saccades. The mutual inhibition existed between these two groups of INC neurons for upward saccades on one side and downward saccades on the other. This pattern of input-output organization of inhibitory INC neurons suggests that the basic neural circuits for horizontal and vertical saccades are similar.

Topographic organization of excitatory and inhibitory commissural connections in the superior colliculi and their functional roles in saccade generation.

Our electrophysiological study showed that there are topographic connections between excitatory and inhibitory commissural neurons (CNs) in one superior colliculus (SC) and tectoreticular neurons (TRNs) in the opposite SC. To obtain morphological evidence for these topographic commissural connections between the SCs, tracers were injected into various parts of the SC, the inhibitory burst neuron (IBN) area and Forel's field H (FFH), in the cat. Retrogradely labeled CNs were classified into three types according to their somatic areas and identified as GABA-positive or -negative immunohistochemically. Caudal SC injections labeled small GABA-positive CNs (<200 µm(2)) in the deep layers of the opposite rostral SC. Rostral SC injections mainly labeled medium-sized GABA-negative CNs (200-700 µm(2)) in the upper intermediate layer of the opposite rostral SC and small GABA-positive CNs in its deeper layers. Lateral SC injections labeled small GABA-positive CNs in the opposite medial SC and mainly medium-sized GABA-negative CNs in its lateral part. Medial SC injections labeled small GABA-positive CNs in the lateral SC and medium-sized GABA-negative CNs in the medial SC. In comparison, TRNs projecting to the FFH or IBN region were large (>700 µm(2)) and medium-sized. Many of the medium-sized GABA-negative CNs were TRNs projecting to the FFH. These results indicate that mirror-symmetric excitatory pathways link medial to medial (upper field) and lateral to lateral (lower field) parts of the SCs, whereas upper and lower field representations are linked by reciprocal inhibitory pathways in the tectal commissure. These connections presumably play important roles in conjugate upward and downward vertical saccades.

Commissural mirror-symmetric excitation and reciprocal inhibition between the two superior colliculi and their roles in vertical and horizontal eye movements.

The functional roles of commissural excitation and inhibition between the two superior colliculi (SCs) are not yet well understood. We previously showed the existence of strong excitatory commissural connections between the rostral SCs, although commissural connections had been considered to be mainly inhibitory. In this study, by recording intracellular potentials, we examined the topographical distribution of commissural monosynaptic excitation and inhibition from the contralateral medial and lateral SC to tectoreticular neurons (TRNs) in the medial or lateral SC of anesthetized cats. About 85% of TRNs examined projected to both the ipsilateral Forel's field H and the contralateral inhibitory burst neuron region where the respective premotor neurons for vertical and horizontal saccades reside. Medial TRNs received strong commissural excitation from the medial part of the opposite SC, whereas lateral TRNs received excitation mainly from its lateral part. Injection of wheat germ agglutinin-horseradish peroxidase into the lateral or medial SC retrogradely labeled many larger neurons in the lateral or medial part of the contralateral SC, respectively. These results indicated that excitatory commissural connections exist between the medial and medial parts and between the lateral and lateral parts of the rostral SCs. These may play an important role in reinforcing the conjugacy of upward and downward saccades, respectively. In contrast, medial SC projections to lateral SC TRNs and lateral SC projections to medial TRNs mainly produce strong inhibition. This shows that regions representing upward saccades inhibit contralateral regions representing downward saccades and vice versa.

Commissural excitation and inhibition by the superior colliculus in tectoreticular neurons projecting to omnipause neuron and inhibitory burst neuron regions.

Previous electrophysiological studies have shown that the commissural connections between the two superior colliculi are mainly inhibitory with fewer excitatory connections. However, the functional roles of the commissural connections are not well understood, so we sought to clarify the physiology of tectal commissural excitation and inhibition of tectoreticular neurons (TRNs) in the "fixation " and "saccade " zones of the superior colliculus (SC). By recording intracellular potentials, we identified TRNs by their antidromic responses to stimulation of the omnipause neuron (OPN) and inhibitory burst neuron (IBN) regions and analyzed the effects of stimulation of the contralateral SC on these TRNs in anesthetized cats. TRNs in the caudal SC (saccade neurons) projected to the IBN region, and received mono- or disynaptic inhibition from the entire rostrocaudal extent of the contralateral SC. In contrast, TRNs in the rostral SC projected to the OPN or IBN region and received monosynaptic excitation from the most rostral level of the contralateral SC, and mono- or disynaptic inhibition from its entire rostrocaudal extent. Among the rostral TRNs with commissural excitation, IBN-projecting TRNs also projected to Forel's field H (vertical gaze center), suggesting that they were most likely saccade neurons related to vertical saccades. In contrast, TRNs projecting only to the OPN region were most likely fixation neurons. Most putative inhibitory neurons in the rostral SC had multiple axon branches throughout the rostrocaudal extent of the contralateral SC, whereas excitatory commissural neurons, most of which were rostral TRNs, distributed terminals to a discrete region in the rostral SC.

Physiological characterization of synaptic inputs to inhibitory burst neurons from the rostral and caudal superior colliculus.

The caudal superior colliculus (SC) contains movement neurons that fire during saccades and the rostral SC contains fixation neurons that fire during visual fixation, suggesting potentially different functions for these 2 regions. To study whether these areas might have different projections, we characterized synaptic inputs from the rostral and caudal SC to inhibitory burst neurons (IBNs) in anesthetized cats. We recorded intracellular potentials from neurons in the IBN region and identified them as IBNs based on their antidromic activation from the contralateral abducens nucleus and short-latency excitation from the contralateral caudal SC and/or single-cell morphology. IBNs received disynaptic inhibition from the ipsilateral caudal SC and disynaptic inhibition from the rostral SC on both sides. Stimulation of the contralateral IBN region evoked monosynaptic inhibition in IBNs, which was enhanced by preconditioning stimulation of the ipsilateral caudal SC. A midline section between the IBN regions eliminated inhibition from the ipsilateral caudal SC, but inhibition from the rostral SC remained unaffected, indicating that the latter inhibition was mediated by inhibitory interneurons other than IBNs. A transverse section of the brain stem rostral to the pause neuron (PN) region eliminated inhibition from the rostral SC, suggesting that this inhibition is mediated by PNs. These results indicate that the most rostral SC inhibits bilateral IBNs, most likely via PNs, and the more caudal SC exerts monosynaptic excitation on contralateral IBNs and antagonistic inhibition on ipsilateral IBNs via contralateral IBNs. The most rostral SC may play roles in maintaining fixation by inhibition of burst neurons and facilitating saccadic initiation by releasing their inhibition.

Vestibular projection to the periarcuate cortex in the monkey.

Vestibular inputs to the cerebral cortex are important for spatial orientation, body equilibrium, and head and eye movements. We examined vestibular input to the periarcuate cortex in the Japanese monkey by analyzing laminar field potentials evoked by electrical stimulation of the vestibular nerve. Laminar field potential analysis in the depths of the cerebral cortex showed that vestibular-evoked potentials consisted of early-positive and late-negative potentials and early-negative and late-positive potentials in the superficial and deep layers of the periarcuate cortex, respectively, with latencies of 4.8-6.3 ms, suggesting that these potentials were directly conveyed to the cortex through the thalamus. These potentials were distributed continuously in the fundus, dorsal and ventral banks of the spur and the bottom of the junctional part of the arcuate sulcus and spur. This vestibular-projecting area overlapped the cortical distribution of corticovestibular neurons that were retrogradely labeled by tracer injection into the vestibular nuclei (previously reported area 6 pa), and also the distribution of smooth pursuit-related neurons recorded in the periarcuate cortex including area 8 in a trained monkey. These results are discussed in relation to the function of vestibular information in control of smooth pursuit and efferents of the smooth pursuit-related frontal eye field.

The entire trajectory of single climbing and mossy fibers in the cerebellar nuclei and cortex.

The present study has revealed that OC axons gave rise to a number of thin collaterals. Due to the abundance of these non-CF thin collaterals, it seems better to make a distinction between the terms CFs and OC axons, as was done in the present paper. The present findings on the innervation of PC dendrites by CFs are basically similar to those in previous reports (Ramón y Cajal, 1911; Palay and Chan-Palay, 1974). The number of swellings on a single CF in the present study (n = 250) is comparable to a previously measured value in the rat (n = 288; Rossi et al., 1993) and larger than a value in the frog (n = about 100 beads; Llinás et al., 1969). The average number of CFs per OC axon in this study was close to the number (n = about 7) inferred in the rat by counting the total number of IO neurons and PCs (Schild, 1970). Contact of interneurons by some swellings of CFs in the molecular layer was emphasized by Scheibel and Scheibel (1954) in their study with Golgi staining. Despite the contact of CF terminals on interneurons, the formation of a synaptic structure between them has been excluded in an electron-microscopic study (Hámori and Szentàothai, 1980). On the other hand, electrophysiological studies have demonstrated a weak excitatory effect of CFs on some interneurons (Eccles et al., 1966). Terminals in the granular layer were originated either from thin collaterals of OC axons or from retrograde collaterals of CF terminal arborizations. The former was the main source of swellings in the granular layer. The morphology of the thin collaterals in the present study was consistent with "globose varicosities connected by a fine thread" as described in Golgi preparations and electron micrograms (Chan-Palay and Palay, 1971). Swellings of thin collaterals (about 1.7% of the total number of swellings per OC axon) were most abundant in the upper portion of the granular layer just underneath the PC layer, in which Golgi cells are usually located. Furthermore, some of these swellings were observed to touch presumed Golgi cells in the present study, which is consistent with electron-microscopic findings on the innervation of somata of Golgi cells by thin collaterals (Hámori and Szentàothai, 1980; Chan-Palay and Palay, 1971). Inferior olive stimulation has been shown electrophysiologically to have a weak direct excitatory effect on Golgi cells (Eccles et al., 1966). Ninety-one percent of the OC axons examined had nuclear collaterals; since the possibility of insufficient staining could not be excluded, this percentage may be an underestimation. The ratio of swellings in the cerebellar nuclei versus those of CF terminal arborizations was about 0.036 in individual OC axons in the present study. However, since the volume of the cerebellar nuclei is much smaller than that of the cerebellar cortex, and significant convergence of input from OC axons to cerebellar nucleus neurons is present (Sugihara et al., 1996), cerebellar nucleus projection of OC fibers can still be functionally important. Some swellings seemed to make contact with the soma and the proximal portions of dendrites of large neurons in the present study, which is consistent with the steep rising phase of postsynaptic excitatory potentials in cerebellar nucleus neurons following IO stimulation (Kitai et al., 1977; Shinoda et al., 1987). Although intracellular potentials were presumably recorded only from large output neurons in the cerebellar nuclei, the present study suggested that small neurons were also innervated by OC axons. The present study revealed that virtually all reconstructed LRN axons projected not only to the Cx as mossy fibers, but also to the DCN including the VN by their axon collaterals. None of the LRN neurons specifically projected to the DCN without projecting to the Cx, namely all axon terminals of LRN neurons in the DCN and VN belonged to axon collaterals of mossy fibers projecting to the Cx. (ABSTRACT TRUNCATED)

Neural organization from the superior colliculus to motoneurons in the horizontal oculomotor system of the cat.

The neural organization of the superior colliculus (SC) projection to horizontal ocular motoneurons was analyzed in anesthetized cats using intracellular recording and transneuronal labeling. Intracellular responses to SC stimulation were analyzed in lateral rectus (LR) and medial rectus (MR) motoneurons and internuclear neurons in the abducens nucleus (AINs). LR motoneurons and AINs received excitation from the contralateral SC and inhibition from the ipsilateral SC. The shortest excitation (0.9-1.9 ms) and inhibition (1.4-2.4 ms) were mainly disynaptic from the SC and were followed by tri- and polysynaptic responses evoked with increasing stimuli or intensity. All MR motoneurons received excitation from the ipsilateral SC, whereas none of them received any short-latency inhibition from the contralateral SC, but some received excitation. The latency of the ipsilateral excitation in MR motoneurons (1.7-2.8 ms) suggested that this excitation was trisynaptic via contralateral AINs, because conditioning SC stimulation spatially facilitated trisynaptic excitation from the ipsilateral vestibular nerve. To locate interneurons mediating the disynaptic SC inputs to LR motoneurons, last-order premotor neurons were labeled transneuronally after injecting wheat germ agglutinin-conjugated horseradish peroxidase into the abducens nerve, and tectoreticular axon terminals were labeled after injecting dextran-biotin into the ipsilateral or contralateral SC in the same preparations. Transneuronally labeled neurons were mainly distributed ipsilaterally in the paramedian pontine reticular formation (PPRF) rostral to retrogradely labeled LR motoneurons and the vestibular nuclei, and contralaterally in the paramedian pontomedullary reticular formation (PPMRF) caudomedial to the abducens nucleus and the vestibular nuclei. Among the last-order premotor neuron areas, orthogradely labeled tectoreticular axon terminals were observed only in the PPRF and the PPMRF contralateral to the injected SC and seemed to make direct contacts with many of the labeled last-order premotor neurons in the PPRF and the PPMRF. These morphological results confirmed that the main excitatory and inhibitory connections from the SC to LR motoneurons are disynaptic and that the PPRF neurons that receive tectoreticular axon terminals from the contralateral SC terminate on ipsilateral LR motoneurons, whereas the PPMRF neurons that receive tectoreticular axon terminals from the contralateral SC terminate on contralateral LR motoneurons.

Input patterns and pathways from the six semicircular canals to motoneurons of neck muscles. II. The longissimus and semispinalis muscle groups.

To reveal patterns of input from the six semicircular canals to motoneurons of various neck muscles and their relationship to the mechanical actions of individual neck muscles, patterns of input to neck motoneurons of the longissimus and the semispinalis muscle groups were investigated in the upper cervical spinal cord of anesthetized cats. Intracellular potentials were recorded from motoneurons of the longissimus muscle group (obliquus capitis superior muscle, OCS; splenius muscle, SPL; longissimus muscle, LONG) and the semispinalis muscle group (biventer cervicis muscle, BIV; complexus muscle, COMP), and effects of separate electrical stimulation of the six ampullary nerves on them were analyzed in each preparation. Neck motoneurons usually received convergent inputs from all of the six ampullary nerves, and motoneurons that supplied a particular muscle had a homogeneous pattern of input from the six ampullary nerves. Two different patterns of input were identified for motoneurons of these two muscle groups; one pattern for motoneurons of the longissimus muscle group and the other pattern for motoneurons of the semispinalis muscle group. Motoneurons of the OCS, the SPL, and the LONG muscles received excitation from the three contralateral ampullary nerves and inhibition from the three ipsilateral ampullary nerves. BIV and COMP motoneurons received excitation from the bilateral anterior canal nerves (ACNs) and the contralateral canal nerve (LCN) and inhibition from the bilateral posterior canal nerves (PCNs) and the ipsilateral LCN. Latencies of postsynaptic potentials (PSPs) evoked by stimulation of each of the six ampullary nerves indicated that the earliest component of excitatory PSPs (EPSPs) and inhibitory PSPs (IPSPs) was disynaptic in these motoneurons. However, trisynaptic IPSPs were evoked by stimulation of the contralateral PCN in a considerable number of BIV and COMP motoneurons. In OCS, SPL, and LONG motoneurons, all of the excitation from the contralateral and all of the inhibition from the ipsilateral ampullary nerves were mediated through the ipsilateral medial longitudinal fascicle (MLF). In BIV and COMP motoneurons, disynaptic excitation from the contralateral ACN and LCN and disynaptic inhibition from the ipsilateral LCN and bilateral PCNs were mediated through the ipsilateral MLF, whereas disynaptic excitation from the ipsilateral ACN was mediated through the ipsilateral lateral vestibulospinal tract. The patterns of semicircular canal input to neck motoneurons of these two muscle groups are related closely to the mechanical actions of the individual neck muscles and the optimal stimulus to the semicircular canals such that the connections will tend to stabilize head positions in response to head perturbations.

Sudden bilateral hearing loss due to gastric carcinoma and its histological evidence.

Six temporal bones and a brain tissue sample removed at autopsy from four patients with bilateral sudden hearing loss related to gastric adenocarcinoma were histologically studied. The pathological remains suggest that the sudden hearing loss of these patients may have occurred via one of two different mechanisms: (1) metastasis to the internal auditory meatus damaging the auditory nerve or (2) inner ear haemorrhage damaging Corti's organ. These two mechanisms may cause bilateral sudden deafness in patients with gastric adenocarcinoma.

Four convergent patterns of input from the six semicircular canals to motoneurons of different neck muscles in the upper cervical cord.

This study was performed to investigate the pattern of input and the pathways from the six semicircular canals to motoneurons of various neck muscles in anesthetized cats. Intracellular postsynaptic potentials from neck motoneurons were recorded in response to electrical stimulation of the six ampullary nerves. The results showed that motoneurons of a particular neck muscle have a homogeneous convergent pattern of input from the six semicircular canals; there are four patterns of input from the six semicircular canals to motoneurons of various neck muscles; and the trisynaptic connection between the semicircular canal nerves and neck motoneurons was identified in addition to the disynaptic connection.

Trisynaptic inhibition from the contralateral vertical semicircular canal nerves to neck motoneurons mediated by spinal commissural neurons.

1. Neck motoneurons usually receive disynaptic excitation and inhibition from individual semicircular canal nerves. However, in motoneurons of some neck muscles, trisynaptic inhibition is evoked by stimulation of the contralateral vertical canal nerves. The present study was performed to analyze this pathway and the location and properties of the last-order interneurons responsible for mediating this trisynaptic inhibition from the contralateral vertical canal nerves to neck motoneurons in anesthetized cats. 2. Bipolar stimulating electrodes were implanted on the contralateral anterior (ACN), lateral (LCN), and posterior canal nerve (PCN), and postsynaptic potentials (PSPs) evoked by electrical stimulation of individual canal nerves were intracellularly recorded from motoneurons of the obliquus capitis inferior (OCI), longus capitis (LC), and rectus capitis posterior (RCP) muscles. Stimulation of the contralateral ACN evoked trisynaptic inhibitory PSPs (IPSPs) in OCI and LC motoneurons and disynaptic excitatory PSPs (EPSPs) in RCP motoneurons. Stimulation of the contralateral PCN evoked di- and trisynaptic IPSPs in OCI and RCP motoneurons and disynaptic EPSPs in LC motoneurons. Stimulation of the contralateral LCN evoked disynaptic EPSPs in all of the motoneurons examined. 3. To determine the pathway that mediates these trisynaptic IPSPs from the vertical canal nerves to neck motoneurons, a lesion was made in the lower medulla, and the patterns of PSPs evoked by stimulation of the three contralateral canal nerves were compared before and after the lesion. Interruption of the ipsilateral medial longitudinal fascicle (MLF) abolished all disynaptic EPSPs and IPSPs from the three contralateral canal nerves in OCI, LC, and RCP motoneurons. In contrast, trisynaptic IPSPs evoked by stimulation of the contralateral ACN or PCN remained unaffected by sectioning the MLFs bilaterally. Sectioning of the contralateral lateral vestibulospinal tract (LVST) eliminated the trisynaptic IPSPs in OCI and LC motoneurons evoked by contralateral ACN stimulation and trisynaptic IPSPs in OCI and RCP motoneurons evoked by contralateral PCN stimulation but did not affect disynaptic EPSPs and IPSPs. 4. Stimulation of the contralateral LVST in the lower medulla after sectioning the bilateral MLFs evoked disynaptic IPSPs in OCI, LC, and RCP motoneurons. Because the LVST only projects ipsilaterally, this finding indicates that the last-order interneurons that mediate the trisynaptic inhibition through the LVST are most likely commissural neurons located in the spinal cord. 5. To determine the locations of last-order commissural neurons terminating on OCI motoneurons, wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) was injected into the OCI muscle nerve at C1.(ABSTRACT TRUNCATED AT 400 WORDS)

The vestibulocollic reflex.

Stabilization of the head is required not only for adequate motor performance, such as maintaining balance while standing or walking, but also for the adequate reception of sensory inputs such as visual and auditory information. The vestibular organs, which consist of three approximately orthogonal semicircular canals (anterior, horizontal, posterior) and two otolith organs (utriculus, sacculus), provide the most important input for the detection of head movement. Activation of afferents from these receptors evokes the vestibulocollic reflex (VCR), which stabilizes head position in space. In this review, which is the outgrowth of a session of the vestibular symposium held in Hawaii in April, 1994, we discuss the neural substrate of this reflex and some aspects of the central processing involved in its production. Some topics are not considered, in particular the important interaction between the VCR and the cervicocollic reflex evoked by activation of neck afferents (70,119), and attempts to model the reflex (69).

Input patterns and pathways from the six semicircular canals to motoneurons of neck muscles. I. The multifidus muscle group.

1. The pattern of connections between the six semicircular canals and neck motoneurons of the multifidus muscle group was investigated by recording intracellular potentials from motoneurons in the upper cervical cord of anesthetized cats. 2. Synaptic potentials were recorded in motoneurons of the rectus capitis posterior (RCP) muscle at C1, the obliquus capitis inferior (OCI) muscle at C1 and C2, and the cervical multifidus muscle (Multi) at C4 in response to electrical stimulation of individual ampullary nerves of the six semicircular canals. Excitatory or inhibitory postsynaptic potentials (EPSPs or IPSPs, respectively) were evoked by separate stimulation of individual ampullary nerves in all of the neck motoneurons. Virtually all of the neck motoneurons received convergent inputs from the six ampullary nerves. 3. Motoneurons that supplied a single muscle had a homogeneous pattern of input from the six semicircular canals. There were two patterns of input from the six semicircular canals to motoneurons of the multifidus muscle group. RCP and Multi motoneurons were excited by stimulation of the bilateral anterior canal nerves (ACNs) and the contralateral lateral canal nerve (LCN) and inhibited by stimulation of the bilateral posterior canal nerves (PCNs) and the ipsilateral LCN. This input pattern is similar to that previously observed in other dorsal extensor muscles, whereas the other input pattern observed in OCI motoneurons is entirely new. OCI motoneurons at C1 and C2 were excited by stimulation of the ipsilateral ACN, PCN, and the contralateral LCN and inhibited by stimulation of the contralateral ACN, PCN, and the ipsilateral LCN. 4. Most postsynaptic potentials (PSPs) were disynaptic, but there were trisynaptic inhibitory connections between the contralateral ACN and PCN and OCI motoneurons, and between the contralateral PCN and RCP motoneurons. 5. The pathways for mediating these inputs from different semicircular canals to neck motoneurons were determined by making lesions in the lower medulla. Transection of the ipsilateral medial longitudinal fascicle (MLF) abolished the following potentials: all disynaptic PSPs in RCP motoneurons except the disynaptic EPSPs from the ipsilateral ACN, and in OCI motoneurons, disynaptic PSPs from the bilateral LCNs, and disynaptic IPSPs from the contralateral PCN. Complete bilateral section of the MLF did not affect the disynaptic EPSPs from the ipsilateral ACN in RCP motoneurons, the disynaptic EPSPs from the ipsilateral ACN and PCN in OCI motoneurons, nor the trisynaptic IPSPs from the contralateral ACN and PCN in COI motoneurons and from the contralateral PCN in RCP motoneurons.(ABSTRACT TRUNCATED AT 400 WORDS)

[Cerebello-cerebral loop for motor control--controversial issues on extra-cerebellar afferents to the deep cerebellar nuclei].

Intracellular recording was made from dentate nucleus neurons (DNNs) in anesthetized cats, to investigate cerebral inputs to DNNs and their responsible pathways. Stimulation of the medial portion of the contralateral pericruciate cortex most effectively produced EPSPs followed by long-lasting IPSPs in DNNs. Stimulation of the pontine nucleus (PN), the nucleus reticularis tegmenti pontis (NRTP) and the inferior olive (IO) produced monosynaptic EPSPs and polysynaptic IPSPs in DNNs. The results indicate that the excitatory input from the cerebral cortex to DNNs is at least partly relayed via the PN, the NRTP and the IO. Intraaxonal injection of HRP visualized the morphology of mossy fibers from the PN to the dentate nucleus (DN) and the cerebellar cortex. 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.

Organization of excitatory inputs from the cerebral cortex to the cerebellar dentate nucleus.

Intracellular recording was made from dentate nucleus neurons (DNNs) in anesthetized cats, to investigate cerebral inputs to DNNs and their responsible pathways. Stimulation of the medial portion of the contralateral pericruciate cortex most effectively produced EPSPs followed by long-lasting IPSPs in DNNs. Stimulation of the pontine nucleus (PN), the nucleus reticularis tegmenti pontis (NRTP) and the inferior olive (IO) produced monosynaptic EPSPs and polysynaptic IPSPs in DNNs. The results indicate that the excitatory input from the cerebral cortex to DNNs is at least partly relayed via the PN, the NRTP and the IO. Intraaxonal injection of HRP visualized the morphology of mossy fibers from the PN to the DN and the cerebellar cortex. 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.

Synaptic organization of the vestibulo-collic pathways from six semicircular canals to motoneurons of different neck muscles.

The pattern of inputs from six semicircular canals to neck motoneurons was investigated by stimulating six ampullary nerves electrically and recording intracellular potentials from motoneurons of the rectus capitis dorsalis (RD), the complexus (COMP) and the obliquus capitis caudalis (OCA) muscles at the upper cervical cord of the cat. RD and COMP motoneurons received disynaptic excitation from bilateral anterior and contralateral horizontal ampullary nerves and disynaptic inhibition from bilateral posterior and ipsilateral horizontal ampullary nerves. OCA motoneurons received excitation from ipsilateral vertical and contralateral horizontal ampullary nerves and inhibition from contralateral vertical and ipsilateral horizontal ampullary nerves. Ipsilateral disynaptic inhibitory postsynaptic potentials and contralateral disynaptic excitatory postsynaptic potentials to these motoneurons were mediated by the medial longitudinal fasciculus (MLF) and the other postsynaptic potentials by the extra-MLF pathways. The results indicated that motoneurons of a neck muscle have its own characteristic pattern of inputs from six semicircular canals.

Spinal commissural neurons mediating vestibular input to neck motoneurons in the cat upper cervical spinal cord.

Spinal commissural neurons (CNs) activated di- or trisynaptically by stimulation of ipsilateral vestibular afferents were stained with intraaxonal injection of horseradish peroxidase in the cat upper cervical spinal cord. Stem axons of CNs in lamina VIII or VII, after crossing the midline, had ascending and/or descending main branches that gave off multiple axon collaterals to laminae IX and VIII over a few cervical segments. Terminal boutons appeared to make contact with proximal dendrites and somata of retrogradely-labelled neck motoneurons. Therefore, these CNs were regarded as mediating vestibular afferent input to contralateral neck motoneurons trisynaptically at the shortest.