| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Department of Systems Neurophysiology, Graduate School of Medicine, Tokyo Medical and Dental University, Tokyo, Japan
Submitted 4 April 2005; accepted in final form 18 May 2005
 |
ABSTRACT |
|---|
|
|
|
INTRODUCTION |
|---|
|
showed that after transection of the commissure between the SCs, cats once again visually oriented to objects in a hemifield that had been made blind by prior ablation of the occipitotemporal cortex. This outcome, called the Sprague effect, suggests that the commissural connection of the SC may play an important role in visual-orienting behavior, and may mediate mutual suppression between the two SCs to prevent competing responses in the opposite direction. Later electrophysiological studies confirmed the inhibitory nature of the commissural tectotectal projection. Extracellular recording of local field potentials or single-cell activity showed that visual responses in the superficial layers of the SC are inhibited by stimulation of the contralateral SC (Goodale 1973; Hoffmann and Straschill 1971; Mascetti and Arriagada 1981; Robert and Cuénod 1969). Similarly, tectal output neurons related to saccadic eye movements were found to be inhibited during ipsiversive orienting movements (Infante and Leiva 1986; Peck 1990) or by electrical stimulation of the contralateral SC (Munoz and Istvan 1998). With regard to these physiological studies, the anatomical features of commissural connections between the two SCs have been examined extensively (Behan and Kime 1996a; Edwards 1977; Fish et al. 1982; Grantyn and Grantyn 1982; Magalhães-Castro et al. 1978; Moschovakis and Karabelas 1985; Olivier et al. 1998; Rhoades et al. 1986; Yamasaki et al. 1984).
The existence of a direct inhibitory connection between the two SCs was demonstrated by intracellular recordings of inhibitory postsynaptic potentials (IPSPs) from tectal cells in response to electrical stimulation of the contralateral SC. These IPSPs had a latency consistent with a monosynaptic inhibitory commissural connection (Maeda et al. 1981; Moschovakis and Karabelas 1982). Consistent with these physiological observations, Appell and Behan (1990) found that commissural cells constitute a major source of GABAergic projection to the contralateral SC in the cat. On the other hand, electrophysiological studies in tectal neurons have shown that stimulation of the contralateral SC evokes very small excitatory postsynaptic potentials (EPSPs) at a monosynaptic latency followed by larger monosynaptic IPSPs (Maeda et al. 1981; Moschovakis and Karabelas 1982), suggesting that there is an excitatory component of the tectotectal pathway. Through the use of an electron microscopic technique, tectotectal synaptic terminals were found to be heterogeneous, suggesting the existence of both excitatory and inhibitory commissural neurons (Behan 1985). Recently, using a double-labeling method, Olivier et al. (2000) clearly demonstrated that some tectotectal neurons contained glutamate, whereas others contain 
-aminobutyric acid (GABA), and that almost equal numbers of the two tectotectal populations are present. This finding of equal numbers of GABAergic and glutamatergic tectotectal cells somewhat contradicts previous findings because they invariably indicated that the tectotectal projection was predominantly inhibitory.
Recent studies have suggested that there are two zones in the SC: the rostral fixation zone (Guitton 1991; Munoz and Guitton 1989, 1991; Munoz and Istvan 1998; Munoz and Wurtz 1992, 1993a,b, 1995; Paré and Guitton 1994; Peck and Baro 1997) and the caudal saccade zone (Munoz and Guitton 1989, 1991; Munoz and Istvan 1998; Munoz et al. 1991). In relation to this suggestion, our recent intracellular analysis of collicular inputs to omnipause neurons (OPNs) and excitatory (EBNs) and inhibitory burst neurons (IBNs) revealed that TRNs in the caudal SC projected to the contralateral EBNs and IBNs, whereas TRNs in the rostral SC projected to the OPN region (Izawa et al. 1999; Sugiuchi et al. 2005; Takahashi et al. 2005). IBNs receive strong disynaptic inhibition from the caudal "saccade zone" of the ipsilateral SC and strong monosynaptic excitation from the caudal "saccade zone" of the contralateral SC. These reciprocal inputs supplied by the two SCs at the level of EBNs and IBNs serve to prevent the inappropriate antagonistic action of the brain stem circuit for generating horizontal saccades (Izawa et al. 1999; Sugiuchi et al. 2005). On the other hand, IBNs receive strong disynaptic inhibition from the rostral "fixation zones" of the two SCs by OPNs in the nucleus raphe interpositus (Sugiuchi et al. 2005; Takahashi et al. 2005). This inhibitory effect on IBNs and probably also EBNs by OPNs may serve to prevent unnecessary saccades to unexpected targets during visual fixation.
In these previous studies, stimulation of the rostral SC on each side evoked IPSPs in IBNs at latencies of 1.3–2.8 ms, which suggests that these IPSPs were disynaptic and trisynaptic (Sugiuchi et al. 2005). To explain the inhibition in an IBN evoked bilaterally by stimulation of the rostral SC, there are two possible pathways: by contacting OPNs, TRNs in both SCs may independently inhibit the same IBN, or TRNs on one side of the SC may inhibit an IBN by way of OPNs, and these TRNs may in turn be activated by the opposite SC. Experiments in our previous study, which used surgical cuts made in the brain stem, ensured the existence of the former independent pathways, but did not exclude the possibility of the latter pathway (Sugiuchi et al. 2005). There are two possible pathways whereby TRNs could be activated by stimulation of the opposite SC: commissural excitation of the TRNs and antidromic activation of commissural axon collaterals of the TRNs. It is still unclear how TRNs in the "fixation zone" and the "saccade zone" of the SC are influenced by commissural inputs from the contralateral SC.
The present study was performed to determine whether TRNs that project to different targets in the brain stem receive excitatory or inhibitory inputs from the contralateral SC, and to understand how commissural connections between the two SCs function to maintain visual fixation and to generate and suppress saccades in the cat. Using intracellular recording combined with electrical stimulation of the SC, we showed that TRNs in the caudal "saccade zone" mainly received monosynaptic inhibition from the contralateral rostral SC and mono- or disynaptic inhibition from its caudal part, whereas TRNs in the rostral SC received monosynaptic excitation from the contralateral rostral SC, and mono- or disynaptic inhibition from all rostrocaudal levels of the contralateral SC. The latter population in the rostral SC contained TRNs that projected to the OPN region and TRNs that projected to both the IBN region and the nucleus of the field of Forel (FFH). The functional roles of commissural excitation and inhibition in these different groups of TRNs and non-TRN commissural neurons will be discussed.
|
|
METHODS |
|---|
|
-chloralose (40–45 mg/kg, intravenous [iv], initial dose, supplemented with additional doses of 10–25 mg/kg, iv throughout the remainder of the experiment). During recording, the animals were paralyzed by the intravenous administration of pancuronium bromide (Mioblock, Organon, Oss, The Netherlands), and artificially ventilated with end-tidal CO2 held at 35–40 mmHg. The heart rate was constantly monitored by an electrocardiogram. The body temperature was kept at 37.0–38.5°C by a heating pad. The abducens nerve was detached from the muscle and mounted on a bipolar hook electrode for electrical stimulation. The bone over the parietal and occipital cortex was removed, and the cerebral cortex was removed bilaterally by suction to allow the introduction of stimulating electrodes into the right SC and recording electrodes into the left SC under direct visual observation. Usually, four concentric bipolar stimulating electrodes (inner diameter and outer diameter, 0.1 and 0.3 mm; interelectrode distance along the longitudinal axis, 0.5 mm) were arranged rostrocaudally at 1.0- to 1.2-mm intervals along the presumed horizontal meridian of the motor map in the SC on the right side (McIlwain 1986). For antidromic activation of TRNs in three experiments, four concentric bipolar stimulating electrodes were placed on each side in the SC and two concentric bipolar electrodes of the same type were placed on each side in the FFH. The tips of the SC electrodes were positioned in the intermediate or deep layer (1.5–2.0 mm deep from the surface) (Izawa et al. 1999; Kawamura and Hashikawa 1978; Moschovakis and Karabelas 1985).
The vermis overlying the fourth ventricle was removed by suction to facilitate the placement of stimulating electrodes or intraaxonal recording from axons of TRNs in the OPN region and the IBN region. We first identified the location of the abducens nucleus by locating antidromic field potentials following electrical stimulation of the sixth nerve (Maeda et al. 1971; Shinoda and Yoshida 1974). Then, stimulating sites in the OPN (Büttner-Ennever et al. 1988; Curthoys et al. 1981; Evinger et al. 1982) and IBN regions (Hikosaka and Kawakami 1977; Hikosaka et al. 1978) were determined relative to the abducens nucleus (Sugiuchi et al. 2005). For antidromic identification of TRNs projecting to the OPN region and the IBN region, separate electrode arrays were placed in the right OPN and IBN regions contralateral to the recording site in the SC. These electrode arrays consisted of four monopolar electrodes (100 µm in diameter) insulated except at the tip, which were glued together around a pillar, so that the tips of the four electrodes were arranged dorsoventrally at 1-mm intervals. For stimulation of the IBN region, one electrode array was placed 0.8 mm lateral to the midline and 0.5–1.0 mm caudal to the caudal border of the abducens nucleus. For stimulation of the OPN region, the other electrode array was placed 0–0.3 mm lateral to the midline and 0.3–1.0 mm rostral to the rostral border of the abducens nucleus. Stimulus currents were delivered between two adjacent tips, and the pillar was grounded to reduce stimulus artifacts. Negative pulses of 0.2-ms duration were delivered at <500 µA for stimulation of the SC, the FFH, and the OPN and IBN regions. Ranck (1975) estimated the effective current spread of 1.0–1.5 mm around an electrode tip by monopolar stimulation at 500 µA (200-µs-duration pulse) in the mammalian CNS. Because we used bipolar stimulation, the effective current spread should be much less than the estimated values by Ranck (1975) (Shinoda et al. 1977). Sasaki et al. (1970, 1972) estimated that 500 µA could not activate fibers or cells beyond 1.0 mm from an electrode tip, when a concentric bipolar electrode was used. The positions of the stimulating electrodes in the brain stem were marked by passing negative currents of 20 µA for 20 s after each experiment, and the stimulated sites in the SC, the OPN and IBN regions, and the FFH were histologically confirmed on sections stained with thionine. Histological examination showed that the distance between a stimulating electrode in the IBN region and the presumed caudal border of the OPN region was about 2.0 mm (1.5–2.5 mm) in each experiment. Glass microelectrodes for intracellular recording were filled with 0.4 M KCl or 2 M K-citrate and had a resistance of 10–15 M
.
|
|
RESULTS |
|---|
|
) of the contralateral SC in the cat. All lateralities in the present paper are described with reference to the recording site, if not stated otherwise. Antidromic identification of TRNs projecting to the OPN and IBN regions
TRNs in the caudal part of the SC are known to project to EBNs in the contralateral paramedian pontine reticular formation (PPRF) (Grantyn and Grantyn 1982; Izawa et al. 1999; Moschovakis et al. 1988; Scudder et al. 1996; Sugiuchi et al. 2005) and IBNs in the paramedian pontomedullary reticular formation (PPMRF) (Grantyn and Grantyn 1982; Grantyn et al. 1987; Olivier et al. 1993; Scudder et al. 1996), and these TRNs are mainly responsible for the generation of saccades (Gandhi and Keller 1999; Munoz and Istvan 1998). On the other hand, TRNs in the rostral part of the SC are known to be involved in visual fixation (Guitton 1991; Munoz and Guitton 1989, 1991; Munoz and Wurtz 1993a,b, 1995; Peck 1989) and project to OPNs (Büttner-Ennever et al. 1988; Gandhi and Keller 1997; Langer and Kaneko 1990; Paré and Guitton 1994; Raybourn and Keller 1977; Sugiuchi et al. 2005; Takahashi et al. 2005). Therefore we tried to analyze the properties of commissural inputs onto these two groups of TRNs. To determine the projection sites of TRNs in the brain stem, we recorded intracellular potentials from cell bodies of TRNs in the left SC and identified TRNs that projected to different sites in the brain stem by their antidromic responses to stimulation of the contralateral OPN and IBN regions (Fig. 1A). For this purpose, we stimulated three dorsoventral sites in the OPN region (Fig. 1D) and three dorsoventral sites in the IBN region (Fig. 1E) on the right side. Intracellular recordings were made from 95 TRNs, but 23 of them could not be used for analysis of synaptic potentials because of quick spontaneous diffusion of Cl– from the recording electrode into the cells. Therefore the remaining 72 TRNs were used for the present analysis. Their resting membrane potentials ranged from –45 to –70 mV (mean ± SD, –54 ± 18 mV, n = 72).
|
In support of this interpretation, the latencies of the antidromic spikes in a TRN were very similar at three sites in the OPN region (within 0.1-ms difference) (Fig. 1F, 5–7) because the passing stem axon was activated there. Furthermore, this neuron was antidromically activated at different latencies (0.5, 0.7, and 1.1 ms) by stimulation of the three different sites (Fig. 1, B, 8–10 and E, 8–10) in the IBN region (Fig. 1F, 8–10), suggesting that the stimulus activated thin TRN axon collaterals ramifying in the IBN region, and most probably terminating there. Therefore TRNs that were antidromically activated from the OPN and IBN regions were considered to project to the IBN region. Such IBN-projecting TRNs as in Fig. 1F were found at all rostrocaudal levels of the SC, and the latencies of the antidromic spikes in TRNs of the caudal SC that were activated from the IBN region ranged from 0.5 to 1.2 ms (0.8 ± 0.2 ms, n = 47) (see Fig. 5Ab).
|
, 1972). Such neurons that were activated antidromically from the IBN region were always activated from the OPN region at <500 µA. This observation ensured that stimulation of the OPN region at this intensity well covered the tectoreticular tract. On the other hand, the possibility of inadvertent current spread from a stimulating electrode in the IBN region to axons in the OPN region could be excluded because the distance between the stimulating electrode and the presumed caudal border of the OPN region was about 2.0 mm (1.5–2.0 mm) in each experiment. An analysis of commissural inputs to these different groups of TRNs revealed that the properties of synaptic inputs from the contralateral SC to TRNs in the rostral and caudal parts of the SC were different. Accordingly, we will first describe the properties of commissural inputs from the SC to caudal TRNs and then to rostral TRNs.
|
To analyze the properties of commissural inputs from the contralateral SC to TRNs in the caudal SC, we recorded intracellular potentials from the caudal part of the left SC and stimulated the right OPN region, the right IBN region, and four rostrocaudal sites in the right SC, as shown in Fig. 1A. Figure 2, A–C shows a typical example of commissural input to a caudal TRN. In this caudal TRN, antidromic spikes were evoked by stimulation of the right OPN region (Fig. 2A, 5) and also the right IBN region (Fig. 2A, 8). Therefore this neuron was considered to be a TRN that projected to the contralateral IBN region. Stimulation of all four rostrocaudal sites in the contralateral SC evoked large hyperpolarizations at 500 µA (Fig. 2B). To determine whether these hyperpolarizations were IPSPs or disfacilitation attributed to a decrease in EPSPs, we iontophoretically injected Cl– into the cell. After the injection of Cl–, hyperpolarizing potentials were changed to large depolarizing potentials, indicating that these hyperpolarizations were inhibitory postsynaptic potentials (IPSPs) (Coombs et al. 1955; Eccles 1964). This input pattern from the contralateral SC was usually observed in most TRNs in the caudal SC. With respect to the IPSPs, generally their amplitudes were larger, their latencies were shorter, and the slopes of their falling phase were steeper, when more rostral sites were stimulated (Fig. 2B). We determined the onsets of IPSPs by superimposing IPSPs on their corresponding field potentials recorded just outside the penetrated cells or by superimposing the IPSPs on reversed depolarizing potentials after Cl– injection into the cells. The latencies of the IPSPs from sites 1–4 in the contralateral SC were 1.0, 1.1, 1.4, and 1.7 ms, respectively (Fig. 2B, 1–4). The latencies of antidromic spikes of putative inhibitory commissural neurons (see Tectal neurons mediating commissural excitation or inhibition) evoked by stimulation of the contralateral SC were 0.3–1.2 ms (see Fig. 10, C–F). Therefore the IPSPs evoked at sites 1 and 2 were safely considered to be monosynaptic, and those evoked at site 4 appeared to be disynaptic (Fig. 2B).
|
|
; Shinoda et al. 1976, 1982, 1987; Sugiuchi et al. 2005). As shown in this example, the commissural inhibition was usually stronger from the most rostral SC site. However, in other TRNs examined, the strength of this inhibition was almost equal from individual rostrocaudal sites of the contralateral SC. Such an example is shown in Fig. 2, D–F. In this caudal TRN, stimulation of four rostrocaudal SC sites evoked IPSPs of similar large amplitudes and with short latencies at 500 µA (Fig. 2E). The latencies of the IPSPs were 1.1–1.2 ms, and therefore the IPSPs evoked at all four sites were considered to be monosynaptic. These IPSPs were still evoked at 150 µA (Fig. 2F), but their amplitudes were smaller and the slopes of the falling phase were slower than at 500 µA. With a decrease in the stimulus intensity, monosynaptic inhibition was still evoked at site 4 in this TRN (Fig. 2F, 4), indicating that at least some inhibitory commissural neurons must exist in the caudal SC. In brief, we examined commissural input to 28 TRNs in the caudal SC. All of them projected to the contralateral IBN region, and received commissural inhibition from all four rostrocaudal sites of the contralateral SC. In nearly 60% of TRNs, the commissural inhibition tended to be stronger and mainly monosynaptic from the most rostral SC stimulating site, and disynaptic from the most caudal SC stimulating site. This inhibition was almost equally strong and monosynaptic from both the rostral and caudal SC in the remaining 40% of the TRNs tested even at lower stimulation strengths (100–200 µA).
To compare the nature of commissural inhibition in TRNs located in different rostrocaudal sites in the SC, we recorded intracellular potentials from cells along the presumed horizontal meridian of the motor map (McIlwain 1986). Figure 3 shows a typical example of commissural inhibition on four TRNs located in different rostrocaudal sites of the SC in one cat. These TRNs were antidromically activated from the contralateral IBN region (not illustrated). All of the TRNs received commissural inhibition from the four rostrocaudally distributed sites in the contralateral SC. In each TRN, the slopes of the falling phase of IPSPs were steeper and the amplitudes of the IPSPs were usually larger, when more rostral sites were stimulated. In the most rostral TRN (Fig. 3Ba), small EPSPs preceded the IPSPs evoked from rostral stimulation sites (Fig. 3Ba, 1 and 2), but in the other TRNs, only IPSPs were apparent. For each TRN, the IPSPs were largest and their latencies, which ranged from 0.7 to 1.2 ms, were shortest when the most rostral site was stimulated in the contralateral SC. This indicates that all four of these TRNs received monosynaptic inhibition from the most rostral SC. This finding also suggested that inhibitory commissural neurons might be distributed with higher density in the rostral part of the SC. However, because many TRNs received monosynaptic inhibition from the more caudal SC, a few inhibitory commissural neurons must also be located in the caudal SC. In addition, TRNs tended to receive longer-latency inhibition from more caudal SC levels that was often disynaptic. Therefore it is highly likely that this late inhibition was mediated by rostral inhibitory commissural neurons that were orthodromically activated from the more caudal SC.
|
To specifically examine commissural input patterns in TRNs of the rostral SC, we recorded intracellular potentials from TRNs in the left rostral SC and examined the effects of stimulation of four rostrocaudal sites of the contralateral SC on these TRNs in the same way as shown in Fig. 2. In the rostral SC, TRNs were classified into two types with regard to their projection to the brain stem: TRNs that projected to the OPN region and those that projected to the IBN region. Among 44 TRNs examined in the rostral one-fourth of the SC, 31 TRNs were antidromically activated from both the OPN and IBN regions, whereas the other 13 TRNs were activated only from the OPN region, but not from the IBN region. We will describe commissural inputs to these two types of rostral TRNs separately.
The effects of stimulation of the contralateral SC in TRNs that projected to the OPN region are illustrated in Fig. 4. In the example shown in Fig. 4, B–D, antidromic spikes were evoked at a latency of 0.7 ms by stimulation of the OPN region (site 5) at 50 µA (Fig. 4B, 5), but not by stimulation of the IBN region (Fig. 4C, 8–10). In this TRN, stimulation of the contralateral rostral SC evoked a depolarization followed by a hyperpolarization (Fig. 4D, 1, middle traces). To determine whether this depolarization was an EPSP or disinhibition resulting from a decrease in IPSPs, we passed a hyperpolarizing current through a recording electrode and injected Cl– into the cell. This reversed the later hyperpolarization to a depolarizing potential without affecting the early depolarization (Fig. 4D, 1, top traces). Therefore this depolarization was an EPSP and the later hyperpolarization was an IPSP (Coombs et al. 1955; Eccles 1964). As the stimulation sites moved caudally, EPSPs and IPSPs decreased in amplitude (Fig. 4D, 2–3) and only IPSPs were evoked by stimulus site 4 (Fig. 4D, 4). The EPSPs were considered to be monosynaptic because their latencies were 0.8–1.1 ms. The latencies of the IPSPs were 1.2 (site 1), 1.7 (site 2), 1.9 (site 3), and 1.8 ms (site 4). Judging from the latencies of antidromic spikes in presumed inhibitory commissural neurons (see Tectal neurons mediating commissural excitation or inhibition and Fig. 10, C–F), the IPSPs evoked at site 1 were considered to be monosynaptic and those at site 4 were considered to be disynaptic.
Figure 4, E–G shows another example of a TRN projecting to the OPN region. In this tectal neuron, antidromic spikes were not evoked by stimulation of the IBN region at 500 µA (Fig. 4F). However, partial spikes evoked at latencies of 1.2 and 1.0 ms by stimulation at sites 5 and 7 in the OPN region, respectively (Fig. 4E), were judged to be antidromic because they were evoked at constant latencies in an all-or-none manner at threshold. Similar antidromic spikes were also evoked by stimulation of site 2 in the contralateral SC (Fig. 4G, 2). Therefore we considered this neuron to be a TRN terminating in the OPN region with a commissural axon. Stimulation of the three rostral sites of the contralateral SC evoked small depolarizations followed by large IPSPs (Fig. 4G, 1–3) and stimulation of its most caudal part evoked only large IPSPs (Fig. 4G, 4) at 500 µA. Sharp spikelike depolarizations such as those in Fig. 4E, 5 and 7 also appeared in Fig. 4G, 1 and 2. Sharp spikes in Fig. 4G, 2 were judged to be antidromic because they were evoked at constant latencies in an all-or-none manner at threshold. However, sharp depolarizations in Fig. 4G, 1 were not antidromic spikes for the following reason. As stimulus intensities were decreased at sites 1 and 2 (top traces in Fig. 4G, 1 and 2), the IPSPs became smaller, and as a result, it became clear that these sharp potentials were attributed to the curtailment of EPSPs by the large IPSPs. The latencies of the EPSPs were very short (<1.0 ms) and therefore monosynaptic (Coombs et al. 1955; Eccles 1964). The latencies of the IPSPs ranged from 1.0 to 1.4 ms and were most probably monosynaptic (see DISCUSSION). As the SC stimulation sites moved more caudally, the EPSP amplitude decreased, but the IPSPs did not change so much. These results indicate that a TRN terminating in the OPN region received excitation from the rostral part of the contralateral SC and inhibition from all rostrocaudal sites within the contralateral SC. In this TRN, inhibition was also caused by stimulation of the contralateral IBN region at latencies of 1.6–1.8 ms (Fig. 4F, 8–10). This inhibition was most likely disynaptic because latencies of antidromic spikes in TRNs projecting to the IBN region were 0.5–1.7 ms (see Fig. 5, Ab and Gb).
In summary, we analyzed 13 TRNs projecting to the contralateral OPN region. The latencies of EPSPs and IPSPs evoked by stimulation of the contralateral SC ranged from 0.7 to 1.3 ms (mean ± SD, 0.9 ± 0.2 ms, n = 22) (Fig. 5E) and 0.9 to 2.0 ms (1.4 ± 0.3 ms, n = 37) (Fig. 5F), respectively. All of these TRNs received monosynaptic excitation from the rostral sites and mono- or disynaptic inhibition from all rostrocaudal levels of the contralateral SC. Both the excitation and the inhibition were generally stronger from the more rostral SC. Furthermore, most of these TRNs were disynaptically inhibited by stimulation of the contralateral IBN region. The latencies of antidromic spikes evoked by stimulation of the OPN region were often longer in most OPN-projecting TRNs (Fig. 5Da) than in IBN-projecting TRNs (Fig. 5Ga), suggesting that tectoreticular axons terminating in the OPN region, and probably their cell bodies, are smaller than those terminating in the IBN region. This suggestion was partly supported by the experience that intracellular recording from OPN-projecting TRNs was more difficult than recording from IBN-projecting TRNs.
While analyzing commissural inputs to TRNs projecting to the IBN region, we found that many TRNs in the rostral SC received commissural excitation from the contralateral SC making them different from TRNs in the caudal SC. Figure 6 shows an example of a rostral TRN projecting to the IBN region. This tectal neuron penetrated in the rostral one-fourth of the SC was antidromically activated from the OPN (Fig. 6B, 5) and IBN regions (Fig. 6B, 10). Stimulation of the most rostral part of the contralateral SC evoked depolarizations with occasional spikes, which were followed by large hyperpolarizations (Fig. 6C, 1). Stimulation of the more caudal SC evoked only hyperpolarizations (Fig. 6C, 2 and 3) but stimulation of the most caudal SC evoked very small depolarizations followed by hyperpolarizations (Fig. 6C, 4). At a weaker stimulus intensity (Fig. 6D, middle traces), a similar response pattern was observed in the same TRN. To determine the synaptic nature of the depolarizations and hyperpolarizations, Cl– was injected into the cell (Fig. 6D, top traces). With this procedure, the hyperpolarizations were reversed to depolarizing potentials, but the depolarizations were not affected so much, indicating that the hyperpolarizations were IPSPs and the depolarizations were EPSPs (Coombs et al. 1955; Eccles 1964). These temporal and spatial features of synaptic inputs from the different rostrocaudal levels of the contralateral SC to a rostral TRN projecting to the IBN region were very similar to those observed in rostral TRNs projecting to the OPN region, but were different from those observed in caudal TRNs projecting to the IBN region in that caudal TRNs mainly received commissural inhibition without commissural excitation.
|
|
Commissural excitation of TRNs that projected to the FFH
To better understand the functional role of commissural excitation in rostral TRNs projecting to the OPN or IBN region, we examined whether these TRNs also projected to the FFH. In this experiment, a stimulating electrode was placed in the FFH on each side and four stimulating electrodes were placed in the SC on each side. Intraaxonal recordings were made from axons of TRNs in either the OPN or IBN region (Fig. 8). The records in Fig. 8, A and B show an example of intraaxonal spikes recorded in the left IBN region. Stimulation of the right rostral SC (sites 5 and 6) evoked direct spikes at 500 µA (Fig. 8B, 5 and 6, top traces) and indirect or synaptically activated spikes at lower stimulus intensities (Fig. 8B, 5 and 6, bottom traces). Stimulation of the right caudal SC (sites 7 and 8) evoked only indirect spikes (Fig. 8B, 7 and 8) in this TRN. Therefore this axon was considered to arise from a TRN in the rostral SC. The same TRN was antidromically activated from the right FFH (Fig. 8B, i-FFH), but not from the left FFH (Fig. 8B, c-FFH). The effects of stimulation of the contralateral SC on this TRN were examined by stimulating four rostrocaudal sites in the left SC (Fig. 8B, 1–4). This TRN was directly activated from site 2 and synaptically from site 1, but not activated from sites 3 or 4. Accordingly, this TRN with commissural excitation was considered to be located in the right rostral SC and to project to the right FFH and the left SC and IBN region, as shown schematically in Fig. 8A. Figure 8, C and D shows another example of intraaxonal spikes recorded in the left OPN region. Stimulation of the rostral sites (sites 5 and 6) of the right SC evoked both direct and/or indirect spikes at near thresholds for the direct spikes (Fig. 8D, 5 and 6), and stimulation of the caudal SC (site 7) evoked only indirect spikes (Fig. 8D, 7). This neuron was not activated from either FFH (Fig. 8D, c-FFH and i-FFH), but was synaptically activated from the rostral part of the contralateral SC (Fig. 8D, 1 and 2). Therefore this rostral TRN was considered to receive commissural excitation and was most likely to project to the contralateral OPN region (see DISCUSSION and Fig. 9Ba). It should also be noted that both TRNs in Fig. 8 were excited orthodromically from sites adjacent to the presumed locations of their cell bodies in the ipsilateral SC.
|
|
Tectal neurons mediating commissural excitation or inhibition
The experimental results that have been described so far indicate that commissural excitation is exerted on rostral TRNs from the most rostral part of the contralateral SC, whereas commissural inhibition is exerted on TRNs throughout the rostrocaudal extent of the SC from the entire rostrocaudal extent of the contralateral SC. Furthermore, the shortest latency inhibition originates from the most rostral part of the contralateral SC. Based on these findings, we tried to find candidate commissural neurons that mediated either excitation or inhibition from the contralateral rostral SC to TRNs.
We searched for neurons in the left rostral SC that were activated antidromically from the contralateral SC, while stimulating four rostrocaudal sites in the right SC at 500 µA (Figs. 10 and 11). Two groups of tectal commissural neurons were identified: neurons with multiple axon collaterals in the contralateral SC that lacked projections to either the OPN or IBN region (Fig. 10, A and B), and neurons with an axon collateral limited to the rostral, contralateral SC that also projected to the OPN or IBN region (Fig. 11, A–D). Figure 10, A and B shows a typical example of a commissural neuron with multiple axon collaterals in the contralateral SC. This commissural neuron was located in the most rostral SC because extracellular spikes were recorded from a cell body in the most rostral SC. It was activated from all of the four rostrocaudal stimulating sites in the contralateral SC (Fig. 10Ba, 1–4). Spikes were evoked at short, fixed latencies of <1.0 ms, and they followed double-pulse stimulation at intervals of <1.0 ms (Fig. 10B, 1c and 2c, and 3b and 4b). Therefore these spikes were considered to be antidromically activated from each stimulation site in the contralateral SC. Spike latencies were 0.9 (site 1), 1.0 (site 2), 1.1 (site 3), and 1.3 ms (site 4), suggesting that the commissural axon ran in the rostrocaudal direction in the contralateral SC after crossing the midline at the rostral level of the SC. This neuron was not activated by stimulation of three dorsoventral sites in each of the contralateral OPN and IBN regions at 500 µA (not illustrated). Therefore this commissural neuron was considered to be a purely intratectal commissural neuron.
|
Figure 11, A–D shows an example of extracellular records from a commissural neuron of the second type. This neuron was also located in the most rostral part of the left SC, and was activated from the contralateral SC (Fig. 11B, 2) and the contralateral OPN (Fig. 11B, 5), but not from the contralateral IBN region (not illustrated). Spikes were evoked in an all-or-none manner at threshold (30 µA) (Fig. 11Ca) by stimulation of the contralateral rostral SC (site 2) and followed double-pulse stimuli at an interval of 0.6 ms (Fig. 11Cb), indicating that these were antidromic spikes. In a similar way, spikes evoked by stimulation of the OPN region were regarded as antidromic (Fig. 11C, c and d). A spike collision test (Fig. 11D) confirmed that this TRN sent its axons to both the contralateral SC and the contralateral OPN region (Shinoda et al. 1976). As in this example, commissural neurons of this second type projected to the most rostral sites of the contralateral SC and also projected to the OPN or the IBN region. This second type of commissural neuron that projects to the OPN or IBN region was considered to be excitatory because TRNs that terminated on OPNs (Takahashi et al. 2005) and IBNs (Sugiuchi et al. 2005) were excitatory. That is, excitatory commissural neurons were most likely TRNs that had commissural axons.
Commissural neurons of different types are summarized in Fig. 11, E–H. In this analysis, spikes were recorded intracellularly or extracellularly from cell bodies in the rostral SC. Among 44 rostral commissural neurons that were activated antidromically from the contralateral SC, nine were TRNs that were also activated antidromically from the OPN region but not from the IBN region (Fig. 11E) and 19 were TRNs that were antidromically activated from both the OPN and IBN regions (Fig. 11F). The other 16 neurons were not activated from either the OPN or the IBN region (Fig. 11, G and H). Among them, 11 were antidromically activated from three to four rostrocaudal sites in the contralateral SC (Fig. 11H) and the other five were activated only from the most rostral one or two sites (Fig. 11G). The first three groups of commissural neurons (Fig. 11, E–G) were most likely excitatory because they projected to only the rostral SC, whereas the last group (Fig. 11H) was most likely inhibitory because they projected to the entire SC and did not project to either the OPN or the IBN region. For intratectal commissural neurons with multiple axon collaterals, the latencies of antidromic spikes evoked by contralateral SC stimulation were longer from the caudal SC (Fig. 10F) than from the rostral SC (Fig. 10C). For rostral TRNs with commissural axons, the latencies of antidromic spikes evoked by contralateral SC stimulation ranged from 0.3 to 1.2 ms (0.5 ± 0.2 ms, n = 39) (Fig. 10G).
Inputs to intratectal commissural neurons with multiple axon collaterals in the contralateral SC
To understand the functional role of commissural inhibition in TRNs, we examined inputs to presumed inhibitory commissural neurons in two ways. First, we searched for commissural axons in the caudal half of the SC, while stimulating the contralateral rostral SC (Fig. 12A). Stimulation of the most rostral part of the contralateral SC evoked direct spikes at a threshold of 50 µA (Fig. 12B, 1, right), and direct and indirect spikes at 500 µA (Fig. 12B, 1, left). The cell body of this axon was considered to be located near site 1 in the SC because such activation of direct and indirect spikes usually occurs when a cell body and excitatory presynaptic fibers on it are activated near a stimulating electrode (see Sugiuchi et al. 2005 for a more detailed identification method) (Jankowska et al. 1975; Shinoda et al. 1976, 1982, 1987). This commissural axon did not arise from a TRN because this axon was not antidromically activated from either the OPN or IBN region at 500 µA (Fig. 12C, 5–10). As shown in Fig. 11H, commissural axons projecting to the caudal SC belonged to intratectal neurons (non-TRNs) with multiple axon collaterals. Therefore this commissural axon was most likely an axon of a non-TRN with multiple axon collaterals whose cell body was located in the contralateral rostral SC. Stimulation of the more caudal SC (sites 2 and 3) also evoked direct and indirect spikes (Fig. 12B, 2 and 3), but stimulation of the most caudal SC (site 4) evoked only indirect spikes at fluctuating latencies with double-pulse stimuli (Fig. 12B, 4, right). In short, this neuron located in the rostral SC projected to the caudal part of the contralateral SC and received excitatory inputs from all four rostrocaudal sites of the ipsilateral SC. Similar results were obtained in four other commissural axons recorded in the caudal SC.
|
|
|
DISCUSSION |
|---|
|
|
The first intracellular analysis of the commissural effects of the SC on TRNs by Maeda et al. (1979) revealed that stimulation of the contralateral SC evoked short-latency inhibition (0.7–1.4 ms, median 1.0 ms) in TRNs. These IPSPs were characterized as monosynaptic because the latencies of antidromic spikes of the commissural neurons in the SC ranged from 0.4 to 1.2 ms (median 0.6 ms). These authors also showed the existence of monosynaptic commissural excitation, although its amplitude was very small. The present study confirmed the presence of short-latency IPSPs and EPSPs. However, it further showed that the commissural excitation was strong enough to evoke spikes in rostral TRNs, and was monosynaptic mainly from the rostral SC. On the other hand, commissural inhibition was monosynaptic from the rostral SC and mono- or disynaptic from its caudal part. Previous anatomical studies showed that there is a connection between the two SCs, and that these commissural neurons are located in the rostral half of the SC (Behan and Kime 1996a; Edwards 1977; Magalhães-Castro et al. 1978; Olivier et al. 1998). The present electrophysiological findings are consistent with this anatomical finding in that both excitatory and inhibitory commissural neurons are distributed similarly in the rostral SC (Olivier et al. 2000). These anatomical studies did not show whether commissural neurons are TRNs. Moschovakis et al. (1988) injected horseradish peroxidase (HRP) into single SC neurons and showed that many saccade-related burst neurons (their T-cells) sent their axons to both the predorsal bundle and the tectal commissure. However, the targets of these TRNs in the brain stem or spinal cord were not determined.
In addition to the above anatomical evidence, the presence of clear temporal facilitation of the monosynaptic inhibition ensured that tectal commissural neurons are mainly responsible for the commissural inhibition. However, some portion of this inhibition may be caused by extratectal fibers stimulated in the SC. The substantia nigra projects extensively to the ipsilateral SC with little contralateral projection (Beckstead et al. 1981; Harting et al. 1988) and this projection is GABAergic (Chevalier et al. 1981; Di Chiara 1979; Karabelas and Moschovakis 1985; Vincent et al. 1978). The ipsilateral projection is localized (Hikosaka and Wurtz 1983; Jiang et al. 2003), whereas the contralateral projection is mediated by the collicular commissure and seems to be widespread in the SC (Jiang et al. 2003). Because the contralateral projection is not substantial in the cat (Beckstead et al. 1981), the involvement of this pathway in the observed commissural inhibition must be negligible in the present experiments. The prepositus hypoglossi nucleus (PH) projects bilaterally to the SCs (Corvisier and Hardy 1991; Edwards et al. 1979; Hartwich-Young et al. 1990; Higo et al. 1992; McCrea and Baker 1985; Stechison et al. 1985) and some of the contralateral projection is widespread and is mediated by the tectal commissure (Corvisier and Hardy 1997). However, axon terminals of the PH do not appear to terminate on large neurons (most probably TRNs) (Corvisier and Hardy 1997). Therefore these neurons are not likely to be involved in monosynaptic commissural excitation and inhibition, although the PH contains both excitatory and inhibitory neurons (McCrea 1988). Moreover, disynaptic nature of the commissural inhibition should not be attributed to the involvement of passing-fiber activation.
In the present experiments, stimulus intensities used for stimulation of the SC with a concentric bipolar electrode were 
500 µA. The estimated effective current spread was about 1.0 mm (Ranck 1975: Sasaki et al. 1970, 1972). Therefore there might be some overlap in the populations of SC neurons activated by adjacent SC electrodes because the intervals between the adjacent electrodes were 1.0–1.2 mm. However, this overlap was considered to be rather small. For example, stimulation of the most rostral site evoked large EPSPs (Fig. 6C, 1), but stimulation of its adjacent site evoked only IPSPs (Fig. 6C, 2). Therefore although there may be some overlap between the populations of SC neurons activated, it is reasonable to conclude that each response represents the population effect around a stimulating electrode.
Inhibitory and excitatory commissural neurons
Strong commissural excitation from the contralateral SC was mainly observed in TRNs located in the rostral one-fourth of the SC, although a small EPSP was sometimes observed to precede the commissural IPSP in more caudal TRNs. The latencies of EPSPs in rostral TRNs ranged from 0.7 to 1.4 ms (Fig. 5, E and H) and they were considered to be mainly monosynaptic. The effective stimulus sites for evoking monosynaptic commissural excitation were localized to the rostral half, especially to the rostral one-fourth, of the SC, and the amplitudes of the EPSPs abruptly decreased as the stimulus sites shifted more caudally. Generally, the most caudal stimulus site was not effective. On the other hand, commissural inhibition of TRNs was caused from the entire rostrocaudal extent of the contralateral SC, monosynaptically from the most rostral SC and mono- or disynaptically from the most caudal SC. TRNs located in either the rostral or the caudal part of the SC received monosynaptic inhibition from the rostral SC, suggesting that inhibitory commissural neurons located mainly in the rostral SC might have multiple axon collaterals and inhibit TRNs in the entire contralateral SC. This suggestion was partly supported by our examination of antidromic activation of intratectal neurons from the contralateral SC. A population of intratectal neurons was observed that could be driven antidromically from both the rostral and caudal SC.
In this study, we found four types of commissural neurons in the SC (Fig. 11, E–H). Commissural neurons that sent their axons only to the rostral part of the contralateral SC (Fig. 11, E and F) were almost always TRNs that sent their other axons to either the OPN (Fig. 11E) (cFN in Fig. 13Aa) or IBN region (Fig. 11F) (cVSN in Fig. 13Ab). These commissural neurons were considered to be excitatory because TRNs terminating on OPNs (Paré and Guitton 1994; Takahashi et al. 2005) and IBNs (Chimoto et al. 1996; Sugiuchi et al. 2005) are excitatory. A small population of purely intratectal neurons appeared to project exclusively to the rostral SC (Fig. 11G). On the other hand, most purely intratectal commissural neurons sent multiple axon collaterals throughout the rostrocaudal extent of the contralateral SC (cIN in Fig. 13B). These neurons were not activated from the OPN or the IBN region (Fig. 11H) and are considered to be inhibitory (see RESULTS, Tectal neurons mediating commissural excitation or inhibition). One of the questions that have not been solved to date is whether commissural neurons send axons to the caudal part of the contralateral SC. Most studies have not localized a tracer injection in the caudal SC for retrograde labeling of commissural neurons (Edwards 1977; Magalhães-Castro et al. 1978). We injected a tracer into a localized area of the caudal part of the SC and retrogradely labeled neurons in the rostral part of the contralateral SC (unpublished observation), which anatomically supports the notion that rostral commissural neurons may send their axon collaterals to the contralateral caudal SC. The commissural connection between the caudal SCs was observed in the anterograde experiments of Behan and Kime (1996a), but few cells were seen caudally by Olivier et al. (2000).
There are two possible sources for disynaptic inhibition evoked from the contralateral caudal SC: the inhibitory interneurons may be located in the opposite SC or in the same SC relative to inhibited TRNs. The former possibility was confirmed in Fig. 12 because putative inhibitory commissural neurons in the rostral SC were synaptically activated from the caudal SC (Fig. 12B, 2–4, right). The latter possibility is highly unlikely because the commissural connections between the caudal SCs were almost negligible (Edwards 1977; Olivier et al. 2000).
Among TRNs with axons penetrated in the IBN region (Fig. 9C), there were two groups: those with axon collaterals to the FFH (Fig. 9C, c and d) and those without axon collaterals to the FFH (Fig. 9Cb). The latter TRNs, which were located more caudally in the SC, did not receive commissural excitation, and presumably are involved in the generation of horizontal saccades (HSN in Fig. 13Bb). In contrast, TRNs projecting to both the IBN region and the FFH (Fig. 9C, c and d) are most likely related to oblique saccades (OSN in Fig. 13Bb). Among them, TRNs with commissural excitation (Fig. 9Cc) were located in the rostral SC where the vertical meridian of the motor map for saccades is represented (cVSN in Fig. 13, Ab and Bb). The comparison of TRNs with axons penetrated in the OPN (Fig. 9B) and IBN regions (Fig. 9C) indicates that TRNs that received commissural excitation but lacked FFH collaterals were found in the former group (Fig. 9Ba), but not in the latter group (Fig. 9Ca). These TRNs in the former group (Fig. 9Ba) that were located in the most rostral SC (site 5) were therefore most likely fixation neurons terminating in the OPN region, whereas the TRNs in the latter group were most likely saccade neurons related to horizontal saccades. TRN axons penetrated in the OPN region contained populations terminating in the OPN and the IBN regions. TRNs in Fig. 9, Bc and Cc may constitute a single class and those in Fig. 9, Bd and Cd another class.
IBN-projecting TRNs with commissural excitation
As mentioned above, TRNs with commissural excitation were classified into two groups: IBN-projecting TRNs and OPN-projecting TRNs. We will discuss the functional roles of these two groups in this and the next section, respectively. The present study indicated that TRNs in the rostral SC displaying commissural excitation projected to both the IBN region (probably also the EBN region) and the FFH. Our previous studies showed that OPNs receive monosynaptic excitation from the rostral pole of the SC (Takahashi et al. 2005), whereas IBNs receive monosynaptic excitation from the more caudal part of the SC (Sugiuchi et al. 2005). These findings indicate that the rostral TRNs that project to the IBN region are not likely fixation neurons, but are more likely related to the generation of saccades. Because rostral TRNs with commissural excitation in the two SCs mutually activate each other and often project to the ipsilateral FFH, these TRNs are most likely related to vertical saccades. This interpretation is compatible with the anatomical finding that 92% of commissural neurons were reported to be located in the rostral portion of the SC, in the region between the collicular rostral tip and the plane corresponding to the vertical meridian (Magalhães-Castro et al. 1978), although recent data showed the more caudal distribution of commissural neurons (Olivier et al. 2000). Furthermore, TRNs in the lateral and medial part of the rostral SC probably make excitatory connections with TRNs in the lateral and medial part of the contralateral rostral SC, respectively. Such point-to-point organization existed only between the lateral parts of the two SCs, but not between the medial parts (Edwards 1977). More detailed information on the nature of these point-to-point connections between the bilateral SCs is needed.
The SC neurons located in the most rostral part of the SC lie on or near the representation of the vertical meridian of the motor map (Guitton et al. 1980; McIlwein 1986; Robinson 1972; Sparks and Mays 1983; Stanford et al. 1996). Little is known about neural connections between the SC and vertical ocular motor neurons. Since single-unit recording study of single fibers in the trochlear nerve was reported in the trained monkey (Fuchs and Luschei 1971), the activity of vertical ocular motoneurons has not been systematically analyzed in relation to different directions of saccades in trained alert animals. For example, it is not known whether neurons in the two SCs fire simultaneously for vertical eye movements. The question is whether the SC on one side controls both vertical eye movements with contra- and ipsilateral horizontal components or it controls vertical eye movements with only a contralateral horizontal component. In the latter case, simultaneous bilateral activation of the SCs must occur during pure vertical saccades. Rostral TRNs projecting to the FFH in the two SCs that were found in the present study may serve to produce pure vertical saccades by commissurally exciting each other (Fig. 13Ab). In the former case, the SC on one side must exert excitatory influences on homologous vertical motoneurons on both sides; i.e., ocular motor neurons innervating a particular vertical eye muscle must receive convergent inputs from both SCs. The finding that the SC projects bilaterally to the FFH with an ipsilateral dominance (Graham 1977; Harting 1980; Wang and Spencer 1996) may support this possibility. Because the question of whether SC neurons on one side are active for oblique saccades directed to the ipsilateral side has not been systematically examined, further analysis of the direction tuning of SC saccade neurons is needed to understand the functional role of these rostral TRNs with commissural excitation.
OPN-projecting TRNs with commissural excitation
In addition to rostral TRNs that project to the IBN region, TRNs that project to the OPN region received monosynaptic excitation from the rostral part of the contralateral SC. Some of these cells also have a commissural axon projecting to the same site in the contralateral SC, suggesting that these rostral TRNs mutually excite each other by their commissural collaterals (Fig. 13Aa). Because OPN-projecting TRNs do not project to the FFH, they are not saccade neurons. Instead they are likely to be fixation neurons. Munoz and Istvan (1998) showed that fixation neurons in the rostral SC are antidromically activated from the contralateral SC in the monkey. During visual fixation, fixation neurons in the FEF and the parietal cortex fire tonically (Bizzi 1968; Bruce and Goldberg 1985; Suzuki and Azuma 1977), and may activate fixation neurons in the ipsilateral rostral SC (Sommer and Wurtz 2000). These fixation neurons project to the OPN region (Büttner-Ennever et al. 1999; Gandhi and Keller 1997) and terminate there on omnipause neurons that project to paramedian pontomedullary reticular formation (IBN region) (Strassman et al. 1987; Sugiuchi et al. 2005; Takahashi et al. 2005) and paramedian pontine reticular formation (PPRF) (EBN region) (Nakao et al. 1980; Strassman et al. 1987). Because tectal fixation neurons on both sides converge onto single OPNs (Takahashi et al. 2005), these neurons may mutually excite each other through tectotectal connections and reinforce the bilateral suppression of saccade generation by OPNs during visual fixation.
Functional role of tectal inhibition
OPN-projecting TRNs received disynaptic inhibition evoked by stimulation of the IBN region (Fig. 4F). This disynaptic inhibition may be attributable to antidromic activation of TRNs whose main axons pass the stimulation site in the IBN region and whose recurrent collaterals terminate on inhibitory interneurons within the SC (Fig. 13Aa). This circuitry may normally function to suppress the activity of fixation neurons in the rostral SC. As a consequence, the OPNs, which are tonically activated by such fixation neurons during fixation, would be disfacilitated during saccades. The identification of ipsilaterally projecting inhibitory interneurons terminating on OPN-projecting TRNs (iIN in Fig. 13Aa) remains to be determined (Behan and Appell 1992; Behan and Kime 1996b). However, there are a variety of GABAergic interneurons reported in the SC (Mize 1988; Okada 1992; Saito and Isa 1999).
Putative inhibitory commissural neurons with multiple collaterals in the contralateral SC received monosynaptic excitation from the IBN region (Fig. 12, D and G). It is known that TRNs have recurrent collaterals in the SC (Moschovakis and Karabelas 1985; Moschovakis et al. 1988). Therefore it is most likely that the monosynaptic excitation seen in such commissural neurons arose from antidromic activation of the recurrent collaterals of TRNs (Fig. 13B), although afferent fibers to the SC might be activated at the IBN region. At present, the only known afferent fibers to the SC around the IBN region are from prepositus hypoglossi neurons (PHNs) and vestibular nucleus neurons. Some PHNs project to the SC and this projection is bilateral (Corvisier and Hardy 1997; McCrea and Baker 1985), and therefore this possibility may not be excluded. Because the excitation from the vestibular nucleus is disynaptic to TRNs (Maeda et al. 1978), the vestibular nucleus is not likely to be responsible for this effect. At present, the most likely explanation is that monosynaptic excitation of putative inhibitory commissural neurons evoked by stimulation of the IBN region is caused by recurrent collaterals of TRNs. Before the onset of saccades, saccade neurons in the SC start firing, and saccade command signals are sent to the PPRF for contralateral saccades. Based on our present findings, we posit that at the same time, these signals activate inhibitory commissural neurons in the same SC. These inhibit TRNs throughout the contralateral SC (Fig. 13B). As a result, during the saccades to the contralateral side, saccade-related TRNs in the contralateral SC are inhibited, so that the generation of saccades to the ipsilateral side will be suppressed.
Assuming that inhibitory commissural neurons inhibit both OPN-projecting (Fig. 13Ba) and IBN-projecting TRNs (Fig. 13Bb) in the contralateral SC, this inhibition in the SC may provoke a kind of reciprocal inhibition of horizontal saccadic eye movement. Recently, we found that there is a suppression area in the frontal eye field (FEF) of the monkey, stimulation of which inhibits the generation of saccades ipsilateral to the stimulation side (Izawa et al. 2004). This suppression most probably occurs at the level of the SC and/or the PPRF (Izawa et al. 2004). From the present work it appears that inhibitory commissural neurons in the SC may be a good candidate to explain FEF suppression of ipsiversive saccades. There are two possible connections from the FEF to the inhibitory commissural neurons in the ipsilateral SC. Neurons in the FEF are known to terminate in the SC (Künzle and Akert 1977; McHaffie et al. 2001; Miyashita and Tamai 1989), and the rostral SC receives input from the FEF (Segraves and Goldberg 1987). Therefore it is highly likely that inhibitory commissural neurons in the rostral SC receive direct input from the FEF. On the other hand, inhibitory commissural neurons may receive indirect inputs from movement neurons in the FEF. The present results suggest this possibility because inhibitory commissural neurons received recurrent excitation from TRNs (most likely saccade neurons) in the more caudal part of the ipsilateral SC (Figs. 12, F and G and 13Bb). When saccades occur, saccade neurons in the SC may excite inhibitory commissural neurons in the rostral SC by their recurrent collaterals. Those commissural cells would in turn inhibit TRNs on the contralateral side and suppress saccades to the ipsilateral side.
The present result also showed that fixation neurons in the SC receive commissural inhibition from the opposite SC (Fig. 13Ba). The functional role of this commissural inhibition of fixation neurons by the opposite SC may be as follows. Presumably the tonic activity of fixation neurons in the SCs on both sides needs to be ceased to allow saccades because their projections converge on single OPNs (Takahashi et al. 2005). Before gaze changes, saccade neurons in the SC fire to generate saccades to the contralateral side, and at the same time activate inhibitory commissural neurons by their recurrent collaterals in the same SC. The widespread projections of commissural neurons include inhibition of fixation neurons in the contralateral SC. As a result, the tonic activity of fixation neurons in the SC is decreased. This decrease in tonic activity is also accelerated by simultaneous disfacilitation because of a decrease in tonic activity in fixation neurons in the FEF on the same side. Therefore OPNs are disfacilitated as the result of a decrease in the tonic activity in their tectal fixation neuron inputs. As a result, EBNs and IBNs on the side contralateral to the activated SC are disinhibited, so that saccades to the contralateral side will be generated in the brain stem. To further understand the functional role of this commissural inhibition between the SCs, an analysis of the exact inputs to such inhibitory commissural neurons from the FEF and other cortical areas and the cerebellum will be required.
|
|
GRANTS |
|---|
|
|
|
ACKNOWLEDGMENTS |
|---|
|
|
|
FOOTNOTES |
|---|
Address for reprint requests and other correspondence: Y. Shinoda, Department of Systems Neurophysiology, Graduate School of Medicine, Tokyo Medical and Dental University, 1-5-45, Yushima, Bunkyo-ku, Tokyo 113-8519, Japan (E-mail: yshinoda.phy1{at}med.tmd.ac.jp)
|
|
REFERENCES |
|---|
|
Beckstead RM, Edwards SB, and Frankfurter A. A comparison of the intranigral distribution of nigrotectal neurons labeled with horseradish peroxidase in the monkey, cat and rat. J Neurosci 1: 121–125, 1981.[Abstract]
Behan M. An EM-autoradiographic and EM-HRP study of the commissural projection of the superior colliculus of the cat. J Comp Neurol 234: 105–116, 1985.[CrossRef][Web of Science][Medline]
Behan M and Appell PP. Intrinsic circuitry in the cat superior colliculus: projections from the superficial layers. J Comp Neurol 315: 230–243, 1992.[CrossRef][Web of Science][Medline]
Behan M and Kime NM. Spatial distribution of tectotectal connections in the cat. Prog Brain Res 112: 131–142, 1996a.[Web of Science][Medline]
Behan M and Kime NM. Intrinsic circuitry in the deep layers of the cat superior colliculus. Vis Neurosci 13: 1031–1042, 1996b.
Bizzi E. Discharge of frontal eye field neurons during saccadic and following eye movements in unanesthetized monkeys. Exp Brain Res 6: 69–80, 1968.[Web of Science][Medline]
Bruce CJ and Goldberg ME. Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53: 603–635, 1985.
Büttner-Ennever JA, Cohen B, Pause M, and Fries W. Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey, and its homologue in man. J Comp Neurol 267: 307–321, 1988.[CrossRef][Web of Science][Medline]
Büttner-Ennever JA, Horn AK, Henn V, and Cohen B. Projections from the superior colliculus motor map to omnipause neurons in monkey. J Comp Neurol 413: 55–67, 1999.[CrossRef][Web of Science][Medline]
Chevalier G, Thierry AM, Shibazaki T, and Feger J. Evidence for a GABAergic inhibitory nigrotectal pathway in the rat. Neurosci Lett 21: 67–70, 1981.[CrossRef][Web of Science][Medline]
Chimoto S, Iwamoto Y, Shimazu H, and Yoshida K. Monosynaptic activation of medium-lead burst neurons from the superior colliculus in the alert cat. J Neurophysiol 75: 2658–2661, 1996.
Coombs JS, Curtis DR, and Eccles JC. The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J Physiol 130: 326–373, 1955.
Corvisier J and Hardy O. Possible excitatory and inhibitory feedback to the superior colliculus: a combined retrograde and immunocytochemical study in the prepositus hypoglossi nucleus of the guinea pig. Neurosci Res 12: 486–502, 1991.[Web of Science][Medline]
Corvisier J and Hardy O. Topographical characteristics of the preposito-collicular projections in the cat as revealed by Phaseolus vulgaris-leucoagglutinin technique. A possible organization underlying temporal-to-spatial transformations. Exp Brain Res 114: 461–471, 1997.[CrossRef][Web of Science][Medline]
Curthoys IS, Nakao S, and Markham CH. Cat medial pontine reticular neurons related to vestibular nystagmus: firing pattern, location and projection. Brain Res 222: 75–94, 1981.[CrossRef][Web of Science][Medline]
Di Chiara G, Porceddu ML, Morelli ML, Mulas ML, and Gessa GL. Evidence for a GABAergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat. Brain Res 176: 273–284, 1979.[CrossRef][Web of Science][Medline]
Eccles JC. Physiology of Synapses. Berlin: Springer-Verlag, 1964.
Edwards SB. The commissural projection of the superior colliculus in the cat. J Comp Neurol 173: 23–40, 1977.[CrossRef][Web of Science][Medline]
Edwards SB, Ginsburgh CL, Henkel CK, and Stein BE. Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184: 309–330, 1979.[CrossRef][Web of Science][Medline]
Evinger C, Kaneko CRS, and Fuchs AF. Activity of omnipause neurons in alert cats during saccadic eye movements and visual stimuli. J Neurophysiol 47: 827–844, 1982.
Fish S, Goodman DK, Kuo DC, Polcer JD, and Rhoades RW. The intercollicular pathway in the golden hamster: an anatomical study. J Comp Neurol 204: 6–20, 1982.[CrossRef][Web of Science][Medline]
Fuchs AF and Luschei ES. The activity of single trochlear nerve fibers during eye movements in the alert monkey. Exp Brain Res 13: 78–89, 1971.[Web of Science][Medline]
Gandhi NJ and Keller EL. Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in monkey. J Neurophysiol 78: 2221–2225, 1997.
Gandhi NJ and Keller EL. Comparison of saccades perturbed by stimulation of the rostral superior colliculus, the caudal superior colliculus, and the omnipause neuron region. J Neurophysiol 82: 3236–3253, 1999.
Goodale MA. Cortico-tectal and intertectal modulation of visual responses in the rat's superior colliculus. Exp Brain Res 17: 75–86, 1973.[Web of Science][Medline]
Graham J. An autoradiographic study of the efferent connections of the superior colliculus in the cat. J Comp Neurol 173: 629–654, 1977.[CrossRef][Web of Science][Medline]
Grantyn A, Jacques VO-M, and Berthoz A. Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. II. Morphological properties as revealed by intra-axonal injections of horseradish peroxidase. Exp Brain Res 66: 355–377, 1987.[Web of Science][Medline]
Grantyn AA and Grantyn R. Axonal patterns and site of termination of cat superior colliculus neurons projecting in the tecto-bulbo-spinal tract. Exp Brain Res 46: 243–256, 1982.[Web of Science][Medline]
Guitton D. Control of saccadic eye and gaze movements by the superior colliculus and basal ganglia. In: Eye Movements, edited by Carpenter RHS. Boca Raton, FL: CRC, 1991, p. 244–276.
Guitton D, Crommelinck M, and Roucoux A. Stimulation of the superior colliculus in the alert cat. I. Eye movements and neck EMG activity evoked when the head is restrained. Exp Brain Res 39: 63–73, 1980.[Web of Science][Medline]
Harting JK, Huerta MF, Frankfurter AJ, Strominger NL, and Royce GJ. Ascending pathways from the monkey superior colliculus: an autoradiographic analysis. J Comp Neurol 192: 853–882, 1980.[CrossRef][Web of Science][Medline]
Harting JK, Huerta MF, Hashikawa R, Weber JT, and van Lieshout DP. Neuroanatomical studies of the nigrotectal projection in the cat. J Comp Neurol 278: 615–631, 1988.[CrossRef][Web of Science][Medline]
Hartwich-Young R, Nelson JS, and Sparks DL. The perihypoglossal projection to the superior colliculus in the rhesus monkey. Vis Neurosci 4: 29–42, 1990.[Web of Science][Medline]
Higo S, Kawano J, Matsuyama T, and Kawamura S. Differential projections to the superior colliculus layers from the perihypoglossal nuclei in the cat. Brain Res 599: 19–28, 1992.[CrossRef][Web of Science][Medline]
Hikosaka O, Igusa Y, Nakao S, and Shimazu H. Direct inhibitory synaptic linkage of pontomedullary reticular burst neurons with abducens motoneurons in the cat. Exp Brain Res 33: 337–352, 1978.[Web of Science][Medline]
Hikosaka O and Kawakami T. Inhibitory reticular neurons related to the quick phase of vestibular nystagmus: their location and projection. Exp Brain Res 27: 377–396, 1977.[Web of Science][Medline]
Hikosaka O and Wurtz RH. Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J Neurophysiol 49: 1285–1301, 1983.
Hoffman KP and Straschill M. Influence of cortico-tectal and intertectal connections on visual responses in the cat's superior colliculus. Exp Eye Res 12: 120–131, 1971.[CrossRef][Web of Science][Medline]
Infante C and Leiva J. Simultaneous unitary neuronal activity in both superior colliculi and its relation to eye movements in the cat. Brain Res 381: 390–392, 1986.[CrossRef][Web of Science][Medline]
Izawa Y, Sugiuchi Y, and Shinoda Y. Neural organization from the superior colliculus to motoneurons in the horizontal oculomotor system of the cat. J Neurophysiol 81: 2597–2611, 1999.
Izawa Y, Suzuki H, and Shinoda Y. Suppression of visually and memory-guided saccades induced by electrical stimulation of the monkey frontal eye field. I. Suppression of ipsilateral saccades. J Neurophysiol 92: 2248–2260, 2004.
Jankowska E, Padel Y, and Tanaka R. The mode of activation of pyramidal tract cells by intracortical stimuli. J Physiol 249: 617–636, 1975.
Jiang H, Stein BE, and McHaffie JG. Opposing basal ganglia processes shape midbrain visuomotor activity bilaterally. Nature 423: 982–986, 2003.[CrossRef][Medline]
Karabelas AB and Moschovakis AK. Nigral inhibitory termination of efferent neurons of the superior colliculus: an intracellular horseradish peroxidase study in the cat. J Comp Neurol 239: 309–329, 1985.[CrossRef][Web of Science][Medline]
Kawamura K and Hashikawa T. Cell bodies of origin of reticular projections from the superior colliculus in the cat: an experimental study with the use of horseradish peroxidase as a tracer. J Comp Neurol 182: 1–16, 1978.[CrossRef][Web of Science][Medline]
Künzle H and Akert K. Efferent connections of cortical, area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. J Comp Neurol 173: 147–164, 1977.[CrossRef][Web of Science][Medline]
Langer TP and Kaneko CR. Brainstem afferents to the oculomotor omnipause neurons in monkey. J Comp Neurol 295: 413–427, 1990.[CrossRef][Web of Science][Medline]
Maeda M, Shibazaki T, and Yoshida K. Vestibular and visual influences on superior colliculus neurons in the cat. In: Integrative Control Functions of the Brain, Tokyo: Kodansha, 1978, vol. 1, p. 90–92.
Maeda M, Shibazaki T, and Yoshida K. Monosynaptic inhibition evoked in superior colliculus neurons following contralateral collicular stimulation. In: Integrative Control Functions of the Brain, edited by Ito M. Amsterdam: Elsevier/North-Holland, 1979, p. 68–71.
Maeda M, Shibazaki T, and Yoshida K. The role of tecto-reticular and tecto-spinal pathways in eye-head coordination. In: Progress in Oculomotor Research, edited by Fuchs A and Becker R. Amsterdam: Elsevier/North-Holland, 1981, p. 317–324.
Maeda M, Shimazu H, and Shinoda Y. Rhythmic activities of secondary vestibular efferent fibers recorded within the abducens nucleus during vestibular nystagmus. Brain Res 34: 361–365, 1971.[CrossRef][Web of Science][Medline]
Magalhães-Castro HH, de Lima AD, Saraiva PES, and Magalhães-Castro B. Horseradish peroxidase labeling of cat tectotectal cells. Brain Res 148: 1–13, 1978.[CrossRef][Web of Science][Medline]
Mascetti GG and Arriagada JR. Tectotectal interactions through the commissure of the superior colliculi. An electrophysiological study. Exp Neurol 71: 122–133, 1981.[CrossRef][Web of Science][Medline]
McCrea RA. The nucleus prepositus. In: Neuroanatomy of the Oculomotor System, edited by Büttner-Ennever JA. New York: Elsevier, 1988, p. 203–233.
McCrea RA and Baker R. Anatomical connections of the nucleus prepositus of the cat. J Comp Neurol 237: 377–407, 1985.[CrossRef][Web of Science][Medline]
McHaffie JG, Thomson CM, and Stein BE. Corticotectal and corticostriatal projections from the frontal eye fields of the cat: an anatomical examination using WGA-HRP. Somatosens Mot Res 18: 117–130, 2001.[CrossRef][Web of Science][Medline]
McIlwain JT. Effects of eye position on saccades evoked electrically from superior colliculus of alert cats. J Neurophysiol 55: 97–112, 1986.
Miyashita E and Tamai Y. Subcortical connections of frontal "oculomotor" areas in the cat. Brain Res 502: 75–87, 1989.[CrossRef][Web of Science][Medline]
Mize RR. Immunocytochemical localization of gamma-aminobutyric acid (GABA) in the cat superior colliculus. J Comp Neurol 276: 169–187, 1988.[CrossRef][Web of Science][Medline]
Moschovakis AK and Karabelas AB. Tectotectal interactions in the cat. Soc Neurosci Abstr 8: 293, 1982.
Moschovakis AK and Karabelas AB. Observations on the somatodendritic morphology and axon trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus of the cat. J Comp Neurol 239: 276–308, 1985.[CrossRef][Web of Science][Medline]
Moschovakis AK, Karabelas AB, and Highstein SM. Structure–function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. J Neurophysiol 60: 263–302, 1988.
Munoz DP and Guitton D. Fixation and orientation control by the tecto-reticulo-spinal system in the cat whose head is unrestrained. Rev Neurol (Paris) 145: 567–579, 1989.[Medline]
Munoz DP and Guitton D. Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. J Neurophysiol 66: 1624–1641, 1991.
Munoz DP, Guitton D, and Pelisson D. Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges. J Neurophysiol 66: 1642–1666, 1991.
Munoz DP and Istvan PJ. Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J Neurophysiol 79: 1193–1209, 1998.
Munoz DP and Wurtz RH. Role of the rostral superior colliculus in active visual fixation and execution of express saccades. J Neurophysiol 67: 1000–1002, 1992.
Munoz DP and Wurtz RH. Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 70: 559–575, 1993a.
Munoz DP and Wurtz RH. Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. J Neurophysiol 70: 576–589, 1993b.
Munoz DP and Wurtz RH. Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J Neurophysiol 73: 2334–2348, 1995.
Nakao S, Curthoys IS, and Markham CH. Direct inhibitory projection of pause neurons to nystagmus-related pontomedullary reticular burst neurons in the cat. Exp Brain Res 40: 283–293, 1980.[Web of Science][Medline]
Okada Y. The distribution and function of gamma-aminobutyric acid (GABA) in the superior colliculus. Prog Brain Res 90: 249–262, 1992.[Web of Science][Medline]
Olivier E, Corvisier J, Pauluis Q, and Hardy O. Evidence for glutamatergic tectotectal neurons in the cat superior colliculus: a comparison with GABAergic tectotectal neurons. Eur J Neurosci 12: 2354–2366, 2000.[CrossRef][Web of Science][Medline]
Olivier E, Grantyn AA, Chat M, and Berthoz A. The control of slow orienting eye movements by tectoreticulospinal neurons in the cat: behavior, discharge patterns and underlying connections. Exp Brain Res 93: 435–449, 1993.[Web of Science][Medline]
Olivier E, Porter JD, and May PJ. Comparison of the distribution and somatodendric morphology of tectotectal neurons in the cat and monkey. Vis Neurosci 15: 903–922, 1998.[CrossRef][Web of Science][Medline]
Paré M and Guitton D. The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons. Exp Brain Res 101: 109–122, 1994.[Web of Science][Medline]
Peck CK. Visual responses of neurons in cat superior colliculus in relation to fixation of targets. J Physiol 414: 301–315, 1989.
Peck CK. Neuronal activity related to head and eye movements in cat superior colliculus. J Physiol 421: 79–104, 1990.
Peck CK and Baro JA. Discharge patterns of neurons in the rostral superior colliculus of cat: activity related to fixation of visual and auditory targets. Exp Brain Res 113: 291–302, 1997.[CrossRef][Web of Science][Medline]
Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98: 417–440, 1975.[CrossRef][Web of Science][Medline]
Raybourn MS and Keller EL. Colliculoreticular organization in primate oculomotor system. J Neurophysiol 40: 861–878, 1977.
Rhoades RW, Mooney RD, Szczepanik AM, and Klein BG. Structural and functional characteristics of commissural neurons in the superior colliculus of the hamster. J Comp Neurol 253: 197–215, 1986.[CrossRef][Web of Science][Medline]
Robert F and Cuénod M. Electrophysiology of the intertectal commissures in the pigeon. II. Inhibitory interaction. Exp Brain Res 9: 123–136, 1969.[Web of Science][Medline]
Robinson DA. Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12: 1795–1808, 1972.[CrossRef][Web of Science][Medline]
Saito Y and Isa T. Electrophysiological and morphological properties of neurons in the rat superior colliculus. I. Neurons in the intermediate layer. J Neurophysiol 82: 754–767, 1999.
Sasaki K, Kawaguchi S, Matsuda Y, and Mizuno N. Electrophysiological studies on the cerebellocerebral projections in monkeys. Exp Brain Res 16: 75–88, 1972.[Web of Science][Medline]
Sasaki K, Stauton HP, and Dieckman G. Characteristic features of augmenting and recruiting responses in the cerebral cortex. Exp Neurol 26: 369–392, 1970.[CrossRef][Medline]
Scudder CA, Moschovakis AK, Karabelas AB, and Highstein SM. Anatomy and physiology of saccadic long-lead burst neurons recorded in the alert squirrel monkey. I. Descending projections from the mesencephalon. J Neurophysiol 76: 332–352, 1996.
Segraves MA and Goldberg ME. Functional properties of corticotectal neurons in the monkey's frontal eye field. J Neurophysiol 58: 1387–1419, 1987.
Shinoda Y, Arnold AP, and Asanuma H. Spinal branching of corticospinal axons in the cat. Exp Brain Res 26: 215–234, 1976.[Web of Science][Medline]
Shinoda Y, Ghez C, and Arnold AP. Spinal branching of rubrospinal axons in the cat. Exp Brain Res 30: 203–218, 1977.[Web of Science][Medline]
Shinoda Y, Sugiuchi Y, and Futami T. Excitatory inputs to cerebellar dentate nucleus neurons from the cerebral cortex in the cat. Exp Brain Res 67: 299–315, 1987.[Web of Science][Medline]
Shinoda Y, Yokota J, and Futami T. Morphology of physiologically identified rubrospinal axons in the spinal cord of the cat. Brain Res 242: 321–325, 1982.[CrossRef][Web of Science][Medline]
Shinoda Y and Yoshida K. Dynamic characteristics of responses to horizontal head angular acceleration in vestibuloocular pathway in the cat. J Neurophysiol 37: 653–673, 1974.
Sommer MA and Wurtz RH. Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. J Neurophysiol 83: 1979–2001, 2000.
Sparks DL and Mays LE. Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. J Neurophysiol 49: 45–63, 1983.
Sprague JM. Interaction of cortex and superior colliculus in mediation of visually guided behavior in the cat. Science 153: 1544–1547, 1966.
Stanford TR, Freedman EG, and Sparks DL. Site and parameters of microstimulation: evidence of independent effects on the properties of saccades evoked from the primate superior colliculus. J Neurophysiol 76: 3360–3380, 1996.
Stechison MT, Saint-Cyr JA, and Spence SJ. Projections from the nuclei prepositus hypoglossi and intercalatus to the superior colliculus in the cat: an anatomical study using WGA-HRP. Exp Brain Res 59: 139–150, 1985.[Web of Science][Medline]
Strassman A, Evinger C, McCrea RG, Baker RG, and Highstein SM. Anatomy and physiology of intracellularly labeled omnipause neurons in the cat and squirrel monkey. Exp Brain Res 67: 436–440, 1987.[Web of Science][Medline]
Sugiuchi Y, Izawa Y, Takahashi M, Na J, and Shinoda Y. Physiological characterization of synaptic inputs to inhibitory burst neurons from the rostral and caudal superior colliculus. J Neurophysiol 93: 697–712, 2005.
Suzuki H and Azuma M. Prefrontal neuronal activity during gazing at a light spot in the monkey. Brain Res 126: 497–508, 1977.[CrossRef][Web of Science][Medline]
Takahashi M, Sugiuchi Y, Izawa Y, and Shinoda Y. Synaptic inputs and their pathways from fixation and saccade zones of the superior colliculus to inhibitory burst neurons. Ann NY Acad Sci 1039: 209–219, 2005.[CrossRef][Web of Science][Medline]
Vincent SR, Hattori T, and McGeer EG. The nigrotectal projection: a biochemical and ultrastructural characterization. Brain Res 151: 159–164, 1978.[CrossRef][Web of Science][Medline]
Wang S and Spencer RF. Spatial organization of premotor neurons related to vertical and downward saccadic eye movements in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) in the cat. J Comp Neurol 366: 163–180, 1996.[CrossRef][Web of Science][Medline]
Yamasaki D, Krauthamer G, and Rhoades R. Organization of the intercollicular pathway in rat. Brain Res 300: 368–371, 1984.[CrossRef][Web of Science][Medline]
This article has been cited by other articles:
|
|
 |
|
  Y. Izawa, H. Suzuki, and Y. Shinoda Response Properties of Fixation Neurons and Their Location in the Frontal Eye Field in the Monkey J Neurophysiol, October 1, 2009; 102(4): 2410 - 2422. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 W. Y. Choi and D. Guitton Firing Patterns in Superior Colliculus of Head-Unrestrained Monkey during Normal and Perturbed Gaze Saccades Reveal Short-Latency Feedback and a Sluggish Rostral Shift in Activity J. Neurosci., June 3, 2009; 29(22): 7166 - 7180. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Isoda and O. Hikosaka A Neural Correlate of Motivational Conflict in the Superior Colliculus of the Macaque J Neurophysiol, September 1, 2008; 100(3): 1332 - 1342. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Takahashi, Y. Sugiuchi, and Y. Shinoda Commissural Mirror-Symmetric Excitation and Reciprocal Inhibition Between the Two Superior Colliculi and Their Roles in Vertical and Horizontal Eye Movements J Neurophysiol, November 1, 2007; 98(5): 2664 - 2682. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Izawa, Y. Sugiuchi, and Y. Shinoda Neural Organization of the Pathways From the Superior Colliculus to Trochlear Motoneurons J Neurophysiol, May 1, 2007; 97(5): 3696 - 3712. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Ding and O. Hikosaka Temporal Development of Asymmetric Reward-Induced Bias in Macaques J Neurophysiol, January 1, 2007; 97(1): 57 - 61. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. Condy, N. Wattiez, S. Rivaud-Pechoux, L. Tremblay, and B. Gaymard Antisaccade Deficit after Inactivation of the Principal Sulcus in Monkeys Cereb Cortex, January 1, 2007; 17(1): 221 - 229. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
TOP
ABSTRACT
INTRODUCTION
