Yuriko Sugiuchi

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

Summary1. 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.

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.

Vestibular projections to the spinal cord: the morphology of single vestibulospinal axons.

The three-dimensional distribution of LVST and MVST axons was examined in the cat cervical spinal cord using an intra-axonal staining method. LVST and MVST axons were electrophysiologically identified by their responses to stimulation of the vestibular nucleus, bilateral vestibular primary afferents, the LVST and the MVST were stained with injection of HRP. The axonal trajectory was reconstructed from serial histological sections. LVST axons were found to have multiple axon collaterals in the cervical cord. The maximum number of the identified collaterals for one neuron was 7. These collaterals were observed in either LVST axons terminating at the cervical cord or those projecting below Th2. The rostro-caudal extension of terminals for each collateral was very restricted (mean = 760 μm) and much narrower than intercollateral intervals (mean = 1470 μm). In the gray matter, collaterals ramified successively, pursued a delta-like path, and terminated mainly in lamina VIII and in the medial part of lamina VII and many boutons made apparent contact with the cell bodies and the proximal dendrites of motoneurons in the ventromedial nucleus. Some terminals were also distributed to the ventrolateral part of lamina VII adjacent to lamina IX. One group of LVST axons projected to lamina IX in the lateral ventral horn and terminated on large neurons there, probably motoneurons of forelimb muscles. MVST axons had one to seven axon collaterals at C1–C3 within the range of the stained axon. Stem axons ran in the ventromedial funiculus and primary collaterals arose from them at right angles. Each collateral had a very nar-row rostrocaudal spread as in LVST axons. Terminals were distributed in laminae VIII and IX, including the ventromedial nucleus, the spinal accessory nucleus, and the commissural nucleus. Many terminals seemed to make contact with retrogradely labelled motoneurons of neck muscles. Both crossed and uncrossed MVST axons had these characteristics.

Long descending motor tract axons and their control of neck and axial muscles

It has been tacitly assumed that a long descending motor tract axon consists of a private line connecting the cell of origin to a single muscle, as a motoneuron innervates a single muscle. However, this notion of a long descending motor tract referred to as a private line is no longer tenable, since recent studies have showed that axons of all major long descending motor tracts send their axon collaterals to multiple spinal segments, suggesting that they may exert simultaneous influences on different groups of spinal interneurons and motoneurons of multiple muscles. The long descending motor systems are divided into two groups, the medial and the lateral systems including interneurons and motoneurons. In this chapter, we focus mainly on the medial system (vestibulospinal, reticulospinal and tectospinal systems) in relation to movement control of the neck, describe the intraspinal morphologies of single long descending motor tract axons that are stained with intracellular injection of horseradish peroxidase, and provide evidence that single long motor-tract neurons are implicated in the neural implementation of functional synergies for head movements.

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.

Synaptic Inputs and Their Pathways from Fixation and Saccade Zones of the Superior Colliculus to Inhibitory Burst Neurons and Pause Neurons

Abstract: The caudal part of the superior colliculus (SC) plays an important role in the generation of saccades, whereas the rostral part of the SC is considered to be involved in visual fixation. The present study was performed to determine neural connections from the rostral and caudal parts of the SC to inhibitory burst neurons (IBNs) and pause neurons (PNs) in the nucleus raphe interpositus in the anesthetized cat, and to reveal the functional role of the rostral SC on eye movements. The intracellular potentials from IBNs and PNs were recorded, and the effects of stimulation of the SC on these neurons were analyzed. The results show that IBNs receive monosynaptic excitation from the contralateral caudal SC, and disynaptic inhibition from the ipsilateral caudal SC via contralateral IBNs. In addition, IBNs receive disynaptic inhibition from the rostral part of the SC on either side via inhibitory interneurons other than IBNs. Intracellular recording from PNs revealed that they receive convergent excitation from the rostral parts of the bilateral superior colliculi and that the rostral SC inhibits IBNs on both sides via PNs. The neural connections determined in this study support the functional independence of the rostral SC and are consistent with the notion that the “fixation zone” is localized in the rostral SC. These results show that the fixation zone in the rostral SC may suppress the initiation of bilateral saccades via pause neurons.

Functional synergies among neck muscles revealed by branching patterns of single long descending motor-tract axons.

In this chapter, we describe our recent work on the divergent properties of single, long descending motor-tract neurons in the spinal cord, using the method of intra-axonal staining with horseradish peroxidase, and serial-section, three-dimensional reconstruction of their axonal trajectories. This work provides evidence that single motor-tract neurons are implicated in the neural implementation of functional synergies for head movements. Our results further show that single medial vestibulospinal tract (MVST) neurons innervate a functional set of multiple neck muscles, and thereby implement a canal-dependent, head-movement synergy. Additionally, both single MVST and reticulospinal axons may have similar innervation patterns for neck muscles, and thereby control the same functional sets of neck muscles. In order to stabilize redundant control systems in which many muscles generate force across several joints, the CNS routinely uses a combination of a control hierarchy and sensory feedback. In addition, in the head-movement system, the elaboration of functional synergies among neck muscles is another strategy, because it helps to decrease the degrees of freedom in this particularly complicated control system.

Chapter 19 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.

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 Forels 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.

Chapter 11 Functional significance of excitatory projections from the precerebellar nuclei to interpositus and dentate nucleus neurons for mediating motor, premotor and parietal cortical inputs

Publisher Summary This chapter presents two possible models of the input-output organization of the cerebellar nucleus. The present findings suggest that excitatory inputs from the cerebral cortex to the cerebellar nucleus via the pontine nucleus; the nucleus reticularis tegmenti pontis and the inferior olive could at least partly contribute to the increase of activity of cerebellar nuclear neurons at the onset of movement. Deep cerebellar nucleus neurons give rise to output fibers that convey excitatory signals to their targets. Efferent neurons in the dentate nucleus (DN) and interpositus nucleus (IN) exert excitatory influences on the red nucleus and the motor cortex via the ventrolateral nucleus of the thalamus. Cerebral influences on neurons in the DN are investigated with intracellular recordings from dentate nucleus neurons (DNNs) in nembutal-anesthetized cats by stimulating the cerebral cortex and the cerebral peduncle. The chapter shows that inputs from the cerebral cortex are conveyed to efferent DNNs and interpositus nucleus neurons (INNs) by way of several parallel pathways.