Disynaptic Inhibition of Omnipause Neurons Following Electrical Stimulation of the Superior Colliculus in Alert Cats

We investigated the synaptic organization responsible for the inhibition of omnipause neurons (OPNs) following stimulation of the superior colliculus (SC) in alert cats. Stimulation electrodes were implanted bilaterally in the rostral and caudal SC where a short-pulse train induced small and large saccades, respectively. Effects of single-pulse stimulation on OPNs were examined with intracellular and extracellular recordings. In contrast to monosynaptic excitatory postsynaptic potentials, which were induced by rostral SC stimulation, inhibitory postsynaptic potentials were induced with disynaptic latencies (1.3–1.9 ms) from both the rostral and caudal SC in most OPNs. Analysis of a larger extracellular sample complemented intracellular observations. Monosynaptic activation of OPNs was elicited more frequently from rostral sites than from caudal sites, whereas spike suppression with disynaptic latencies was induced by caudal as well as rostral stimulation with similar frequencies. The results imply that disynaptic inhibition is produced by activation of SC cells that are distributed over wide regions related to saccades of different sizes. We suggest that signals from these neurons initiate a saccadic pause of OPNs through single inhibitory interneurons.

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Monosynaptic activation of medium-lead burst neurons from the superior colliculus in the alert cat

Journal of Neurophysiology ◽

10.1152/jn.1996.75.6.2658 ◽

1996 ◽

Vol 75 (6) ◽

pp. 2658-2661 ◽

Cited By ~ 33

Author(s):

S. Chimoto ◽

Y. Iwamoto ◽

H. Shimazu ◽

K. Yoshida

Keyword(s):

Superior Colliculus ◽

Single Pulse ◽

Inhibitory Input ◽

Abducens Nucleus ◽

Extracellular Recordings ◽

Burst Neurons ◽

Alert Cat ◽

Omnipause Neurons ◽

Pulse Stimulation ◽

Stimulation Of

1. Extracellular recordings were made from medium-lead burst neurons (MLBNs) in the paramedian pontomedullary reticular formation rostral and caudal to the abducens nucleus in the alert cat. 2. Single-pulse stimulation of the contralateral superior colliculus during intersaccadic intervals evoked no response in most MLBNs. When collicular stimulation was applied at the beginning of saccades, spikes of MLBNs were consistently evoked with short latencies. The shortest latency was 0.8 ms, indicating monosynaptic activation of MLBNs from the superior colliculus. 3. Results suggest that monosynaptic excitatory effects from the colliculus are concealed by inhibitory input from omnipause neurons (OPNs) during intersaccadic intervals and that the monosynaptic collicular activation is disclosed when this inhibition is removed by a pause in OPN activity at the beginning of saccades.

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Long-term potentiation facilitates behavioral responding to single-pulse stimulation of the perforant path.

Behavioral Neuroscience ◽

10.1037/0735-7044.99.4.603 ◽

1985 ◽

Vol 99 (4) ◽

pp. 603-620 ◽

Cited By ~ 17

Author(s):

Ronald W. Skelton ◽

James J. Miller ◽

Anthony G. Phillips

Keyword(s):

Single Pulse ◽

Long Term Potentiation ◽

Perforant Path ◽

Term Potentiation ◽

Pulse Stimulation ◽

Stimulation Of

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Sympatholytic response to stimulation of superior laryngeal nerve in rats

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1991.260.2.r290 ◽

1991 ◽

Vol 260 (2) ◽

pp. R290-R297 ◽

Cited By ~ 4

Author(s):

D. H. Huangfu ◽

P. G. Guyenet

Keyword(s):

Receptor Antagonist ◽

Superior Laryngeal Nerve ◽

Single Pulse ◽

Laryngeal Nerve ◽

Ventrolateral Medulla ◽

Gamma Aminobutyric Acid ◽

Onset Latency ◽

Medullary Reticular Formation ◽

Pulse Stimulation ◽

Stimulation Of

The central pathway mediating a sympatholytic response to stimulation of the superior laryngeal nerve (SLN) was studied in halothane-anesthetized, paralyzed rats. Single-pulse stimulation of SLN inhibited lumbar sympathetic nerve discharge (LSND) with onset latency of 113 +/- 1.7 ms. LSND inhibition was markedly attenuated by bilateral microinjection of kynurenic acid (Kyn, glutamate receptor antagonist, 4.5 nmol/side) into the caudal ventrolateral medulla (CVL) or by bilateral administration of bicuculline methiodide (Bic; gamma-aminobutyric acid-receptor antagonist, 225 pmol/side) into the rostral ventrolateral medulla (RVL). In 13 of 14 cases, the baroreceptor reflex was also severely reduced. Injections of Bic or Kyn elsewhere in the medullary reticular formation were ineffective. Single-pulse stimulation of SLN inhibited 19 of 26 RVL reticulospinal barosensitive cells (onset latency 46 +/- 1.4 ms). This inhibition was attenuated (from 92 +/- 6 to 14 +/- 12%) by iontophoretic application of Bic (n = 7), which also reduced the cells' inhibitory response to aortic coarctation. The remaining seven barosensitive neurons were unaffected by SLN stimulation. In conclusion, the sympathetic baroreflex and the sympathoinhibitory response to SLN stimulation appear to be mediated by similar medullary pathways.

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

Journal of Neurophysiology ◽

10.1152/jn.1988.60.2.769 ◽

1988 ◽

Vol 60 (2) ◽

pp. 769-797 ◽

Cited By ~ 30

Author(s):

P. P. Vidal ◽

P. J. May ◽

R. Baker

Keyword(s):

Superior Colliculus ◽

Common Element ◽

Synaptic Organization ◽

Facial Nucleus ◽

Synaptic Potentials ◽

Facial Motoneurons ◽

Brain Stem Lesions ◽

Stem Lesions ◽

Discrete Populations ◽

Stimulation Of

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

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Neural Organization of the Pathways From the Superior Colliculus to Trochlear Motoneurons

Journal of Neurophysiology ◽

10.1152/jn.01073.2006 ◽

2007 ◽

Vol 97 (5) ◽

pp. 3696-3712 ◽

Cited By ~ 13

Author(s):

Yoshiko Izawa ◽

Yuriko Sugiuchi ◽

Yoshikazu Shinoda

Keyword(s):

Superior Colliculus ◽

Interstitial Nucleus Of Cajal ◽

Saccadic System ◽

Neural Organization ◽

Premotor Neurons ◽

Monosynaptic Inhibition ◽

Disynaptic Inhibition ◽

Forel's Field H ◽

Stimulation Of ◽

Monosynaptic Excitation

The neural organization of the pathways from the superior colliculus (SC) to trochlear motoneurons was analyzed in anesthetized cats using intracellular recording and transneuronal labeling techniques. Stimulation of the ipsilateral or contralateral SC evoked excitation and inhibition in trochlear motoneurons with latencies of 1.1–2.3 and 1.1–3.8 ms, respectively, suggesting that the earliest components of excitation and inhibition were disynaptic. A midline section between the two SCs revealed that ipsi- and contralateral SC stimulation evoked disynaptic excitation and inhibition in trochlear motoneurons, respectively. Premotor neurons labeled transneuronally after application of wheat germ agglutinin-conjugated horseradish peroxidase into the trochlear nerve were mainly distributed ipsilaterally in the Forel's field H (FFH) and bilaterally in the interstitial nucleus of Cajal (INC). Consequently, we investigated these two likely intermediaries between the SC and trochlear nucleus electrophysiologically. Stimulation of the FFH evoked ipsilateral mono- and disynaptic excitation and contralateral disynaptic inhibition in trochlear motoneurons. Preconditioning stimulation of the ipsilateral SC facilitated FFH-evoked monosynaptic excitation. Stimulation of the INC evoked ipsilateral monosynaptic excitation and inhibition, and contralateral monosynaptic inhibition in trochlear motoneurons. Preconditioning stimulation of the contralateral SC facilitated contralateral INC-evoked monosynaptic inhibition. These results revealed a reciprocal input pattern from the SCs to vertical ocular motoneurons in the saccadic system; trochlear motoneurons received disynaptic excitation from the ipsilateral SC via ipsilateral FFH neurons and disynaptic inhibition from the contralateral SC via contralateral INC neurons. These inhibitory INC neurons were considered to be a counterpart of inhibitory burst neurons in the horizontal saccadic system.

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Respiratory motor responses to cranial nerve afferent stimulation in rats

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1996.271.4.r1054 ◽

1996 ◽

Vol 271 (4) ◽

pp. R1054-R1062 ◽

Cited By ~ 4

Author(s):

F. Hayashi ◽

D. R. McCrimmon

Keyword(s):

Cranial Nerve ◽

Superior Laryngeal Nerve ◽

Single Pulse ◽

Short Latency ◽

Lung Inflation ◽

Dorsal Respiratory Group ◽

Inspiratory Activity ◽

Pharyngeal Branch ◽

Pulse Stimulation ◽

Stimulation Of

It was hypothesized that, because rats appear to lack a prominent disynaptic projection from the dorsal respiratory group to phrenic motoneurons (Phr), they would lack the short-latency excitation of Phr output seen in cats in response to stimulation of some cranial nerve afferents. Single-pulse superior laryngeal nerve (SLN) stimulation elicited a short-latency bilateral excitation of glossopharyngeal (IX) and hypoglossal (XII) nerves and an ipsilateral excitation of pharyngeal branch of vagus (PhX) in 67% of rats, but no excitation of Phr. Vagus (X) stimulation elicited a bilateral excitation of Phr and a predominantly ipsilateral excitation of IX and PhX. Single-pulse stimulation of SLN or X also elicited longer-latency, bilateral decreases in activity of all recorded nerves. Repetitive stimulation (50 Hz) of SLN or X suppressed inspiratory activity and prolonged expiration. Lung inflation (7.5 cmH2O) inhibited Phr and PhX activity; X stimulation inhibited Phr but prolonged PhX activity. In conclusion, rats predictably lack the SLN-induced short latency Phr excitation but exhibit other short latency reflexes for which the underlying circuitry is not clear.

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Physiological Characterization of Synaptic Inputs to Inhibitory Burst Neurons From the Rostral and Caudal Superior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.00502.2004 ◽

2005 ◽

Vol 93 (2) ◽

pp. 697-712 ◽

Cited By ~ 27

Author(s):

Y. Sugiuchi ◽

Y. Izawa ◽

M. Takahashi ◽

J. Na ◽

Y. Shinoda

Keyword(s):

Superior Colliculus ◽

Abducens Nucleus ◽

Antidromic Activation ◽

Synaptic Inputs ◽

Burst Neurons ◽

Physiological Characterization ◽

Monosynaptic Inhibition ◽

Disynaptic Inhibition ◽

Stimulation Of

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.

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