1. Single axons of pontine nucleus neurons (PN axons) receiving cerebral input were stained intra-axonally with horseradish peroxidase (HRP) in the cerebellum of cats. The axonal trajectory of single PN axons was reconstructed from serial sections of the cerebellum and the brain stem. 2. Axons were penetrated in the white matter near the dentate nucleus, and, after electrophysiological identification, PN axons were injected iontophoretically with HRP. The identification criteria for the PN axons were 1) their direct responses to stimulation of the contralateral pontine nucleus (PN), 2) their synaptic activation from the contralateral cerebral cortex, and 3) the decrease in threshold for evoking direct spikes in stimulation of the PN by conditioning stimuli applied in the cerebral cortex. 3. Two hundred thirty-three axons were electrophysiologically identified as PN axons receiving the input from the cerebral cortex. Ninety-six of them were stained successfully with HRP, and reconstructions were made from 40 well-stained PN axons. All of them gave rise to mossy fibers and terminated in the granular layer of the cerebellar cortex as typical mossy fiber rosettes. Out of these, 22 gave axon collaterals to the dentate nucleus. Virtually all of the axon branches observed in the dentate nucleus were axon collaterals of mossy fibers from the PN to the cerebellar cortex. In 7 of these 22 PN axons, cell bodies were retrogradely labeled with HRP, and all of them were found in the contralateral PN. 4. The stained-stem axons arising from the PN ran medially in the pons, crossed the midline, and then ascended dorsocaudally in the branchium pontis. After passing in the white matter anterior to or lateral to the dentate nucleus, they entered into the cerebellar cortex. On their way, one to three axon collaterals were given off from parent axons to the dentate nucleus. The diameter of these collaterals was very thin (mean, 0.6 microns), compared with the large diameter of the parent axons (mean, 2.1 microns). 5. Some axon collaterals were very simple and had only one terminal branch with or without short branchlets, whereas others were more complex, and single axon collaterals ramified before forming a terminal arborization. Axon collaterals of single PN axons mainly spread mediolaterally or dorsoventrally in the frontal plane but had a very narrow rostrocaudal extension. 6. Terminal branches usually bore swellings en passant along their length and one terminal swelling at their end. The number of swellings per axon collateral ranged 23-180 (116 +/- 52, mean +/- SD).(ABSTRACT TRUNCATED AT 400 WORDS)
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.
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.
Physiological characterization of synaptic inputs to inhibitory burst neurons from the rostral and caudal superior colliculus. J Neurophysiol 93: 697-712, 2005; doi:10.1152/jn.00502.2004. 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.
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.
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)
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