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.

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So Much to See, So Little Time: How the Superior Colliculus (SC) Suppresses Unwanted Saccades. Focus on “Physiological Characterization of Synaptic Inputs to Inhibitory Burst Neurons From the Rostral and Caudal Superior Colliculus”

Journal of Neurophysiology ◽

10.1152/jn.00977.2004 ◽

2005 ◽

Vol 93 (2) ◽

pp. 641-642 ◽

Cited By ~ 1

Author(s):

David M. Waitzman

Keyword(s):

Superior Colliculus ◽

Synaptic Inputs ◽

Burst Neurons ◽

Physiological Characterization

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

Journal of Neurophysiology ◽

10.1152/jn.2001.85.6.2639 ◽

2001 ◽

Vol 85 (6) ◽

pp. 2639-2642 ◽

Cited By ~ 20

Author(s):

Kaoru Yoshida ◽

Yoshiki Iwamoto ◽

Sohei Chimoto ◽

Hiroshi Shimazu

Keyword(s):

Superior Colliculus ◽

Short Pulse ◽

Single Pulse ◽

Synaptic Organization ◽

Postsynaptic Potentials ◽

Disynaptic Inhibition ◽

Alert Cats ◽

Omnipause Neurons ◽

Pulse Stimulation ◽

Stimulation Of

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

Annals of the New York Academy of Sciences ◽

10.1196/annals.1325.020 ◽

2005 ◽

Vol 1039 (1) ◽

pp. 209-219 ◽

Cited By ~ 21

Author(s):

MAYU TAKAHASHI ◽

YURIKO SUGIUCHI ◽

YOSHIKO IZAWA ◽

YOSHIKAZU SHINODA

Keyword(s):

Superior Colliculus ◽

Synaptic Inputs ◽

Burst Neurons

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Commissural Excitation and Inhibition by the Superior Colliculus in Tectoreticular Neurons Projecting to Omnipause Neuron and Inhibitory Burst Neuron Regions

Journal of Neurophysiology ◽

10.1152/jn.00347.2005 ◽

2005 ◽

Vol 94 (3) ◽

pp. 1707-1726 ◽

Cited By ~ 38

Author(s):

M. Takahashi ◽

Y. Sugiuchi ◽

Y. Izawa ◽

Y. Shinoda

Keyword(s):

Superior Colliculus ◽

Inhibitory Neurons ◽

Functional Roles ◽

Commissural Neurons ◽

Burst Neuron ◽

Electrophysiological Studies ◽

Disynaptic Inhibition ◽

Forel's Field H ◽

Commissural Connections ◽

Stimulation Of

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.

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Axonal branching patterns and location of nigrothalamic and nigrocollicular neurons in the cat

Journal of Neurophysiology ◽

10.1152/jn.1980.43.4.883 ◽

1980 ◽

Vol 43 (4) ◽

pp. 883-895 ◽

Cited By ~ 59

Author(s):

M. E. Anderson ◽

M. Yoshida

Keyword(s):

Substantia Nigra ◽

Superior Colliculus ◽

Caudate Nucleus ◽

Spontaneous Activity ◽

Conduction Time ◽

Antidromic Activation ◽

Axonal Projections ◽

Branching Patterns ◽

Ventromedial Thalamus ◽

Stimulation Of

1. Antidromic activation from the thalamus and the superior colliculus was used to identify the axonal projections of neurons in the substantia nigra. 2. Up to 43% of the nigral neurons studied in individual animals had branching axons that could be activated antidromically from both the ipsilateral ventromedial thalamus and the ipsilateral superior colliculus. 3. For several neurons, the conduction time spent in the unbranched axonal segment could be calculated using measurable collision and antidromic latency times. Time in the unbranched segment was less than 20% of the antidromic latency for most neurons studied. 4. Latencies for antidromic activation from the thalamus were measured and would be appropriate if these axons were to mediate the monosynaptic nigrothalamic inhibition reported earlier. 5. Stimulation of the caudate nucleus produced inhibition of spontaneous activity of both collicular- and thalamic-projecting neurons.

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Visual input to commissural neurons of the cat's superior colliculus

Visual Neuroscience ◽

10.1017/s0952523800004880 ◽

1991 ◽

Vol 7 (4) ◽

pp. 389-393 ◽

Cited By ~ 7

Author(s):

James T. McIlwain

Keyword(s):

Superior Colliculus ◽

Action Potentials ◽

Optic Tract ◽

Extracellular Recording ◽

Response Latencies ◽

Antidromic Activation ◽

Commissural Neurons ◽

Direct Input ◽

Y Cells ◽

Stimulation Of

AbstractCells projecting into the commissure of the cat's superior colliculus were identified during extracellular recording by antidromic activation. Electrical stimulation of the ipsilateral optic tract evoked action potentials in the majority of commissural neurons. Response latencies of 1.4 ± 0.5 ms (mean ± S.D.) in a few cells indicated that some commissural neurons receive direct input from the axons of retinal Y–cells. Most commissural cells responded 5.9 ± 1.9 ms (mean ± S.D.) following optic tract shock, implying that the responsible pathway was composed of more slowly conducting axons or did not proceed directly to the colliculus. Results of previous studies of retinal inputs to cells in the deep tectal layers suggest that the later responses were mediated by an indirect Y pathway through the visual cortex.

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