Neocortical Disynaptic Inhibition Requires Somatodendritic Integration in Interneurons

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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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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Crossed disynaptic inhibition of sacral motoneurones.

The Journal of Physiology ◽

10.1113/jphysiol.1978.sp012580 ◽

1978 ◽

Vol 285 (1) ◽

pp. 425-444 ◽

Cited By ~ 58

Author(s):

E Jankowska ◽

Y Padel ◽

P Zarzecki

Keyword(s):

Disynaptic Inhibition

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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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Uncrossed disynaptic inhibition of second-order vestibular neurons and its interaction with monosynaptic excitation from vestibular nerve afferent fibers in the frog

Journal of Neurophysiology ◽

10.1152/jn.1996.76.5.3087 ◽

1996 ◽

Vol 76 (5) ◽

pp. 3087-3101 ◽

Cited By ~ 33

Author(s):

H. Straka ◽

N. Dieringer

Keyword(s):

Nmda Receptor ◽

Nmda Receptors ◽

Large Diameter ◽

Vestibular Nerve ◽

Vestibular Neurons ◽

Postsynaptic Potential ◽

Afferent Fibers ◽

Viiith Nerve ◽

Disynaptic Inhibition ◽

Preferential Activation

1. Eighth nerve evoked responses in central vestibular neurons (n = 146) were studied in the isolated brain stem of frogs. Ninety percent of these neurons responded with a monosynaptic excitatory postsynaptic potential (EPSP) after electrical stimulation of the ipsilateral VIIIth nerve. In 5% of these neurons, the EPSP was truncated by a disynaptic inhibitory postsynaptic potential (IPSP), and in 5% of these neurons a pure disynaptic IPSP was evoked. 2. Disynaptic IPSPs superimposed upon apparently pure EPSPs were revealed by bath application of the glycine receptor antagonist strychnine (0.5–5 microM) or of the gamma-aminobutyric acid-A (GABAA) receptor antagonist bicuculline (0.5–2 microM). The evoked EPSP increased in most central vestibular neurons (strychnine: 15 out of 16 neurons; bicuculline 26 out of 29 neurons). At higher stimulus intensities, the evoked spike discharge increased from 2 to 3 spikes before up to 8-10 spikes per electrical pulse during the application of blocking agents. The unmasked disynaptic inhibitory component increased with stimulus intensity to a different extent in different neurons. 3. Lesion studies demonstrated that these inhibitory components were generated ipsilaterally with respect to the recording side. The disynaptic strychnine-sensitive inhibition was mediated by neurons located either in the ventral vestibular nuclear complex (VNC) or in the adjacent reticular formation. The spatial distribution of the disynaptic inhibition was investigated by simultaneous recordings of VIIIth nerve-evoked field potentials at different rostrocaudal locations of the VNC. A significant strychnine-sensitive component was detected in the middle and caudal parts but not in the rostral part of the VNC. A bicuculline-sensitive component was detected in the rostral and in the caudal parts but not in the middle part of the VNC. In view of a similar rostrocaudal distribution of glycineor GABA-immunoreactive neurons in the VNC of frogs, our results suggest that part of the disynaptic inhibition is mediated by local interneurons with a spatially restricted projection area. 4. The monosynaptic EPSP of second-order vestibular neurons was mediated in part by N-methyl-D-aspartate (NMDA) and in part by non-NMDA receptors. The relative contribution of the NMDA receptor-mediated component of the EPSP decreased with stronger stimuli. This negative correlation could have resulted from a preferential activation of NMDA receptors via thick vestibular nerve afferent fibers. Alternatively, the activation of NMDA receptors became disfacilitated at higher stimulus intensities due to the recruitment of disynaptic inhibitory inputs. Comparison of data obtained in the presence and in the absence of these glycine and GABAA receptor blockers indicates a preferential activation of NMDA receptors via larger-diameter vestibular nerve afferent fibers. 5. The kinetics of NMDA receptors (delay, rise time) activated by afferent nerve inputs were relatively fast. These fast kinetics were independent of superimposed IPSPs. The association of these receptors with large-diameter vestibular nerve afferent fibers suggests that fast NMDA receptor kinetics might be matched to the more phasic response dynamics of the large diameter vestibular afferent neurons to natural head accelerations.

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