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The Journal of Neuroscience, October 15, 1998, 18(20):8496-8504
The Visuo-Motor Pathway in the Local Circuit of the Rat
Superior Colliculus
Tadashi
Isa,
Toshiaki
Endo, and
Yasuhiko
Saito
Department of Integrative Physiology, National Institute for
Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan
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ABSTRACT |
Intrinsic circuit of the superior colliculus (SC), in particular
the pathway from the optic tract (OT) to neurons in the intermediate layer (SGI), was investigated by whole-cell patch-clamp recording in
slice preparations obtained from 17- to 24-d-old rats. Stimulation of
the OT induced monosynaptic EPSPs in neurons in the superficial gray
layer (SGS) and the optic layer (SO), and disynaptic or polysynaptic EPSPs in a majority of SGI neurons. Stimulation of the SGS induced monosynaptic or oligosynaptic EPSPs in the SGI neurons. Both the monosynaptic EPSPs induced in the SGS/SO neurons by stimulation of the
OT and those induced in the SGI neurons by stimulation of the SGS were
mediated by AMPA- and NMDA-type glutamate receptors. Thus, we have
clarified the existence of the glutamatergic excitatory pathway from
the OT to the SGI neurons via SGS and SO neurons. The EPSPs in the SGI
neurons induced by stimulation of the OT or SGS were remarkably
enhanced by bicuculline, suggesting that the signal transmission in
this pathway is under strong suppression by the GABAergic system.
Key words:
superior colliculus; local circuits; slice; patch clamp; intracellular staining; rat
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INTRODUCTION |
The mammalian superior colliculus
(SC) consists of several layers with distinct organization. The
superficial layers [the stratum griseum superficiale (SGS) and the
stratum opticum (SO)] receive visual input directly from the optic
tract (OT) and indirectly from the primary visual cortex. There is a
topographic representation of the contralateral visual field in the
superficial layers (Cynader and Berman, 1972 ). The intermediate and
deep layers [the stratum griseum intermediale (SGI) and the stratum
griseum profundum (SGP)] receive nonvisual sensory inputs (Wallace and
Stein, 1996) and indirect visual inputs from higher cortical visual
areas (Harvey and Worthington, 1990; Harting et al., 1992). These
layers send descending motor commands to the brainstem and spinal cord
(Huerta and Harting, 1982). The deeper layers have a topographic
representation of vector components of saccades (Robinson, 1972). This
motor representation exists with similarly aligned multiple sensory representations. Because the spatial representations of the visual map
in the superficial layers and motor map in the deeper layers coincide
with each other, Robinson (1972) and Sprague (1975) proposed the
existence of vertical connections from the superficial to deeper
layers. However, this proposition was opposed by Edwards (1980), who on
close anatomical inspection concluded that no significant connection
exists between the two layers. Recent anatomical studies (Mooney et
al., 1988; Rhoades et al., 1989; Behan and Appel, 1992; Hall and Lee,
1993; Lee and Hall, 1995) have again suggested the existence of the
interlaminar connection. Mooney et al. (1992) suggested that
superficial layers transmit visual inputs to deeper layers in
electrophysiological experiments. Lee et al. (1997) suggested the
existence of the interlaminar connection by observing EPSCs in
SGI neurons after stimulation of the SGS in slices of the tree shrew.
However, detailed information about the synaptic organization in the
pathway is still lacking. In behavioral studies, it has been shown that
reaction times of saccades reveal several distinct peaks in
distribution. The shortest reaction time is on the order of 70 msec in
monkeys and 100 msec in humans, and these saccades are called
"express saccades" (Fischer and Boch, 1983; Fischer and Ramsperger,
1984). Fischer (1987) proposed that the presence of several peaks
reflects the existence of several distinct pathways in the central
process to generate saccade commands and that the shortest pathway is
mediated by the SC. On the basis of this proposition we hypothesized
that the signal is transmitted directly from the superficial to deeper
layers of the SC in the case of express saccades but not in the case of
regular saccades. If so, the signal transmission from superficial to
deeper layers should be significantly modulated by the behavioral
context. In the present study, we investigated the pathway from the OT
to the SGI neurons in slices of the rat SC. It will be shown that the
pathway exists and presumably is mediated by SGS or SO neurons or
both. Furthermore, as a mechanism that regulates the
transmission in the pathway, the functional significance of the
GABAergic inhibition will be discussed.
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MATERIALS AND METHODS |
Slice preparations. Frontal slices of the SC (400 µm thick) were prepared from young Wistar rats [postnatal day (P)
17-24]. The animals were deeply anesthetized with ether and
decapitated. The brains were quickly removed, submerged immediately in
ice-cold sucrose Ringer's solution containing (in mM): 234 sucrose, 2.5 KCl, 1.25 NaH2PO4, 10 MgSO4, 0.5 CaCl2, 26 NaHCO3, and 11 glucose, and bubbled with 95%
O2 and 5% CO2 for 5-10 min. Slices were cut with a Microslicer (DTK-2000, Dosaka EM, Kyoto, Japan). They were then
incubated in the standard Ringer's solution at room temperature for
>1 hr before recording. The standard Ringer's solution contained (in
mM): 125 NaCl, 2.5 KCl, 2 CaCl2, 1 MgCl2, 26 NaHCO3, 1.25 NaH2PO4, and 25 glucose, and was
continuously bubbled with 95% O2 and 5%
CO2, pH 7.4. After incubation, a slice was mounted
in a recording chamber on an upright microscope (Axioskop FS, Zeiss) and continuously superfused with the standard Ringer's solution at the
rate of 3-5 ml/min by a peristaltic pump (Minipuls 3, Gilson, Villiers, France).
Whole-cell patch-clamp recording. Individual neurons in the
SC were visualized with Nomarski optics with the use of a 40× water
immersion objective. Whole-cell patch-clamp recordings (Hamill et al.,
1981; Edwards et al., 1989) were obtained from neurons in the SGS, SO,
and SGI under visual control of the patch pipettes using an EPC-7
patch-clamp amplifier (List, Darmstadt, Germany). The pipettes were
filled with an internal solution containing (in mM): 150 potassium gluconate, 6 (or 10) KCl, 0.2 EGTA, 2 MgCl2, 2 Na2ATP, 10 HEPES, and 0.1 spermine, pH 7.3. To stain the recorded neurons, biocytin (5 mg/ml)
(Sigma, St. Louis, MO) was dissolved in the solution just before
recording. Because the liquid junction potential between the standard
Ringer's solution and the internal solution was estimated as  10 mV,
the actual membrane potential was corrected by this value. The
osmolarity of the internal solution was 280-290 mOsm/l. The resistance
of the electrodes was 2.5-7.0 M in the bath solution. The series
resistance during recording was 10-25 M. All recordings were
performed at a bath temperature of 28-32°C. Data were acquired using
pClamp system (Axon Instruments, Foster City CA). Electrical
stimulation of the optic tract was applied as a cathodal square-wave
pulse with a duration of 200 µsec using a concentric bipolar
electrode (Clark Electromedical Instruments, Pangbourne, UK) or a
resin-insulated tungsten needle monopolar electrode. The conduction
volley of the optic fibers was recorded by a glass capillary containing
2 M NaCl (impedance: 0.5-2 M).
6-Cyano-7-nitroquinoxaline-2,3,dione (CNQX),
D-2-amino-5-phosphonovalerate (APV) and bicuculline (Bic)
were purchased from RBI (Natick, MA), and tetrodotoxin (TTX) was
purchased from Sankyo (Tokyo, Japan). Records were filtered at a 3 kHz
bandwidth, and the sampling frequency was either 5 or 10 kHz.
Histological procedure. To visualize the recorded neurons by
staining with biocytin (Horikawa and Armstrong, 1988), the patch pipettes were carefully detached from the cells after recording. The
slices were fixed with 4% paraformaldehyde in 0.12 M
phosphate buffer, pH 7.4, for 2-3 d at 4°C. The slices were rinsed
in 0.05 M PBS, pH 7.4, and incubated in methanol containing
0.6% H2O2 for 30 min. After washes with PBS,
the slices were incubated in avidin-biotin peroxidase complex solution
(1%) (Vector Laboratories, Burlingame, CA) containing 0.3% Triton
X-100 for 3 hr. After washes with PBS and 0.05 M
Tris-buffered saline (TBS), pH 7.6, they were incubated in a TBS
solution containing 0.01% diaminobenzidine tetrahydrochloride (DAB),
1% nickel ammonium sulfate, and 0.0003% H2O2
for 30 min. All procedures for visualization of biocytin were performed
at room temperature. The slices were mounted on gelatin-coated slides,
counterstained with cresyl violet, dehydrated, and then coverslipped.
The morphological properties of stained cells were drawn using a camera
lucida attached to a light microscope.
Determining appropriate stimulus strength of the optic
tract. To investigate the input organization from the OT, the
effects of the OT stimulation were investigated in neurons located in various layers of the SC. The OT was stimulated at the most lateral part of the SC, where the optic fibers compose a bundle (Fig. 1A). To exclude the
possibility of current spread to the neural elements outside the OT, we
determined the appropriate stimulus strength by measuring the stimulus
current to induce the maximum conduction volley in the OT. As shown in
Figure 1A, the conduction volley in the OT was
measured at a point in the SO 300-500 µm medial to the stimulation
site. In the case of Figure 1B1, the OT stimulation
at 200 µA evoked a large negative volley in the SO that disappeared
after application of 1 µM TTX, leaving the stimulus
artifact (Fig. 1B2). The negative volley was
resistant to CNQX (data not shown). Subtracting the record in Figure
1B2 from that in Figure 1B1 yielded
a triphasic conduction volley by eliminating the stimulus artifact
(Fig. 1B3). The peak-to-peak amplitudes of the
conduction volley were measured at different stimulus strengths (Fig.
1C) and plotted (Fig. 1D). Figure
1D shows that the conduction volley maximized at 200 µA stimulation in this slice. This indicated that stimulation above
this strength could activate the neural elements outside the OT and
that the stimulus strength had to be set below 200 µA. The records in
Figure 1 were obtained by using a concentric bipolar electrode. The
usage of monopolar electrodes required current intensities to activate the maximal conduction volley in the OT similar to those required using
the bipolar electrode. We performed this procedure in every slice, and all the results shown in this paper were obtained using the
appropriate stimulus strength determined in this way.
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Figure 1.
Conduction volley in the optic fibers. The OT was
stimulated at the most lateral part of the SC, and the conduction
volley was recorded in the SO medial to the stimulation site
(A). Stimulation of the OT induced a conduction
volley (B1) that was completely abolished by application
of 1 µM tetrodotoxin (TTX)
(B2). Subtraction of B2 from B1 eliminated the stimulus
artifact and yielded a triphasic conduction volley (B3).
The relationship between the stimulus strength and the amplitude of the
conduction volley was investigated (C), and plots
of the amplitude of the volley against the stimulus strength revealed
that the amplitude of the volley became saturated at 200 µA stimulus
in this example (D).
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RESULTS |
Input from the OT to neurons in the SGS
The effect of the OT stimulation was investigated in 32 SGS
neurons. Among them, 16 neurons were successfully stained with biocytin. The stained neurons consisted of five piriform cells, three
narrow-field vertical cells, three stellate cells, three horizontal
cells, and two wide-field vertical cells, according to the
morphological characterization by Langer and Lund (1974).
Figure 2 shows the results recorded in a
neuron in the SGS. This neuron projected dendrites in dorsoventral
directions and appeared to be a narrow-field vertical cell (Langer and
Lund, 1974). Extensive axonal projection was observed in the ventral part of the SGS and in the SO, and some extended farther to the SGI
(Fig. 2A, thin lines). A large number of
collaterals and bouton-like swellings were observed. This neuron showed
repetitive spike firing with moderate spike frequency adaptation in
response to depolarizing current pulses. In response to hyperpolarizing
current pulses, this neuron showed inward rectification (Fig.
2B). Stimulation of the OT induced EPSPs with a fixed
latency of 3.5 msec (Fig. 2C1). When double shock stimuli
were given with an interval of 4 msec, the latencies of the EPSP
induced by the second stimulus (the onset is indicated by a vertical
broken line) were the same as those from the first (Fig.
2C2). These results suggested strongly that the EPSPs were
induced monosynaptically. The EPSPs could be induced in 26 neurons by
the OT stimulation, and the latencies ranged from 1.9 to 10.6 msec
(Fig. 2F). Among these, monosynaptic EPSPs were
observed in 21 neurons. The rise time of the monosynaptic EPSPs (the
time between 10 and 90% peak) was measured for those with clear onset
and single peak. The values ranged from 1.5 to 5.3 msec (mean ± SE = 3.2 ± 0.3 msec, n = 18). Among the
successfully stained neurons, monosynaptic EPSPs were observed in four
of five piriform, three of three narrow-field vertical, two of three
stellate, and two of three horizontal cells. Application of 10 µM Bic enhanced the late component of the EPSP with
complete recovery after washing out (Fig. 2D).
Application of 50 µM APV reduced the amplitude of the
late component, and additional application of 10 µM CNQX completely abolished the EPSPs (Fig. 2E). All of
these results indicate that various subgroups of SGS neurons receive
monosynaptic excitatory input from the OT and that the excitatory
transmission is mediated by both AMPA- and NMDA-type glutamate
receptors.
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Figure 2.
Synaptic potential induced by the OT stimulation
in an SGS neuron. The morphology of the recorded neuron, stained with
biocytin, is illustrated in A. Dendrites are drawn as
thick lines. The axon and its collaterals are drawn as
thin lines. B shows the voltage responses
of this neuron to various current pulses. The bottom
traces indicate the injected currents. Synaptic potentials
induced by single and double stimulus (at an interval of 4 msec) of the
OT are shown in C1 and C2, respectively.
The effect of bath application of 10 µM bicuculline
(Bic) is shown in D. Effects of glutamate
receptor antagonists, 10 µM CNQX, and 50 µM
APV are shown in E. F indicates
distribution of latencies of the EPSPs induced by the OT stimulation in
SGS neurons.
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Input from the OT to neurons in the SO
The effects of the OT stimulation were investigated in 20 neurons
in the SO. Figure 3 shows the records
obtained in a wide-field vertical cell according to classification by
Langer and Lund (1974) (Fig. 3A). This neuron extended
dendrites divergently into the SGS and projected axons to the ventral
part of the SO and farther ventrally into the SGI. This neuron showed
regular firing in response to depolarizing current pulses and clear
voltage sag in response to hyperpolarizing pulses and rebound
depolarization after termination of the hyperpolarizing pulses (Fig.
3B). The voltage sag and the rebound depolarization in this
type of neuron were shown to be caused by hyperpolarization-activated
current (Saito and Isa, 1997). Among the 20 SO neurons recorded in the
present study, 17 neurons were regarded as wide-field vertical cells
according to the electrophysiological property (voltage sag). Ten of
these neurons were successfully stained with biocytin, in which the classification was confirmed morphologically. In the neuron shown in
Figure 3, stimulation of the OT induced EPSPs at a latency of 6.3 msec.
The onsets of the EPSPs were constant over many sweeps. When double
shock stimuli were applied with an interval of 4 msec, the EPSP
component locked to the second stimulus (indicated with a vertical
broken line) appeared to have the same latency as that induced by the
first stimulus (Fig. 3C2). These results strongly suggested
that the EPSPs were induced by monosynaptic linkage. The latency of the
EPSPs ranged from 1.3 to 17.0 msec in the 17 wide-field vertical cells
(Fig. 3F, closed columns). Among these, monosynaptic EPSPs
were observed in 16 neurons. In the remaining three neurons, which were
not regarded as wide-field vertical cells (Fig. 3F, open
columns), the OT stimulation induced EPSPs, which were not
regarded as monosynaptic because of fluctuation of latencies. The rise
time of the monosynaptic EPSPs (the time between 10 and 90% peak) in
the wide-field vertical cells was measured for those with distinct
onset and single peak. The values ranged from 3.2 to 11.0 msec
(mean ± SE = 6.6 ± 0.6 msec, n = 10),
much longer than those recorded in the SGS neurons. Application of Bic
enhanced the late component of the EPSPs (Fig. 3D2,E2). The
late component was reduced by APV (Fig. 3D3,E3) and
completely abolished after additional application of CNQX (Fig.
3D4,E4). This indicated that the EPSPs were mediated
by both AMPA- and NMDA-type glutamate receptors. An interesting
observation in these wide-field vertical cells in the SO was that when
a depolarizing current pulse was applied to the soma via the recording
pipette, the action potentials were generated at a threshold of 58 mV (Fig. 3B). In contrast, when the OT was stimulated, the
action potential was induced, overriding the slow and small EPSP, at a
threshold of approximately 74 mV when the resting membrane potential
was 76 mV (Fig. 3C1). Such spike generation insensitive to
the somatic membrane potential was investigated in more detail. The
records in Figure 4 show the synaptic
responses of a wide-field vertical cell in the SO to the OT
stimulation, when the membrane potential of the soma was set at
different levels by varying the amplitude of the constantly injected
current. Figure 4A-D shows that the action
potentials were generated from somatic membrane potentials of 66,
76, 86, and 92 mV, when the membrane potentials were held at
68, 78, 88, and 95 mV, respectively. Thus, the threshold for
the spike generation was independent of the somatic membrane potential.
As shown in Figure 4D, the M-spike (asterisk) was
sometimes induced instead of the full-sized action potential. The
amplitude of the EPSPs became slightly larger when the somatic membrane
potential was held at an extremely hyperpolarized level (95 mV in
this case) than those induced from a more depolarized level (68 mV)
(Fig. 4D, inset). Thus, the variation of the injected current somewhat affected the membrane potential at the synaptic sites
where the EPSPs were induced and also at the sites where the action
potentials were generated. However, this effect seemed minor. Figure
4E shows that the action potential generated from the
membrane potential below 90 mV was effectively blocked by application
of 5 µM CNQX and 50 µM APV in all three
neurons that were tested. Thus, the spike generation independent of the
somatic membrane potential in the wide-field vertical cells was
confirmed to be of synaptic origin but not of the antidromic origin.
Such spike generation independent of the somatic membrane potential was
observed in 13 of the 17 wide-field vertical cells in which monosynaptic EPSPs were observed after the OT stimulation. In the
remaining four wide-field vertical cells and three SO neurons that were
not identified as wide-field vertical cells, the action potentials were
generated around the membrane potential of 58 mV, overriding the peak
of EPSPs as shown in the case of Figure 4F1. These
action potentials disappeared when the membrane potentials were
hyperpolarized (to 92 mV in the cell shown in Fig.
4F2) by increasing the amplitude of the constantly
injected current.
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Figure 3.
Synaptic potentials induced by the OT stimulation
in an SO neuron. The morphology of the recorded neuron, stained with
biocytin, is illustrated in A. Dendrites are drawn as
thick lines. The axon and its collaterals are drawn as
thin lines. B shows the voltage responses
of this neuron to various current pulses. Here, the threshold of the
action potentials was approximately 58 mV. Synaptic potential induced
by the OT stimulation is shown in C1. Action potentials
were induced from the membrane potential of 74 mV, overriding the
EPSPs. C2 shows synaptic responses to double stimulus of
the OT at an interval of 4 msec. The onset of the EPSP induced by the
second stimulus is indicated by a vertical broken line.
Effects of 10 µM Bic and additional application of 50 µM APV and 10 µM CNQX are shown in
D1-4 (faster time sweeps) and E1-4
(slower time sweeps). F shows distribution of latencies
of the EPSPs induced by the OT stimulation in SO neurons. Closed
columns indicate the cases of wide-field vertical cells, and
open columns indicate the other cell types.
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Figure 4.
Synaptic responses and action potential generation
in a wide-field vertical cell in the SO induced by the OT stimulation
when the resting membrane potentials of the soma
(Vm) were held at different levels:
Vm = 68 mV (A), 78
mV (B), 88 mV (C), and
95 mV (D), respectively. The
asterisk in D indicates an M-spike. The
inset in D indicates superimposition of
EPSPs without the action potentials taken from records in
A and D. E1 and
E2 indicate the effect of 5 µM CNQX and 50 µM APV on the action potential generated from the somatic
membrane potential below 90 mV. F1 and
F2 indicate the example of records in wide-field
vertical cells in which the action potentials were generated from
normal threshold level (58 mV in this case) overriding the EPSPs
evoked by the OT stimulation (F1), and action potentials
disappeared when the membrane potential was hyperpolarized by
increasing the intensity of constantly injected hyperpolarizing current
(F2). G, Morphological characteristics of
a wide-field vertical cell in the SO. Photomicrographs (G1,
G2) and camera lucida drawing (G3) of a
wide-field vertical cell whose axon was originated from a proximal
dendrite (arrows). a and d
in G2 indicate axon and dendrite, respectively.
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A most probable explanation of such observation is that these
wide-field vertical cells received the synaptic input from the OT on
their distal dendrites, which led to induction of EPSPs with long rise
time when recorded in the soma because of long electrotonic length
(Rall, 1964). Because the extremely hyperpolarized somatic membrane
potential did not affect the spike generation, we speculated that the
EPSPs elicited in the dendrites might have induced nonlinear dendritic
spikes, which directly activated the initial segment of the axon
bypassing the soma, and generated the action potentials. This
speculation is substantiated by the fact that in 7 of the 10 morphologically identified wide-field vertical cells, the axons were
originated from a proximal portion of a dendrite, which is illustrated
in photomicrographs and camera lucida drawings in Figure 4G
(arrows). In the remaining three cells, we could not determine whether
the axons were originated from the soma or a dendrite. This
morphological property of wide-field vertical cells has already been
illustrated [Langer and Lund (1974), their Plate 8].
Furthermore, we investigated the morphology of 14 wide-field vertical
cells, which we stained in our previous study without investigating the
synaptic input (Saito and Isa, 1997), and could confirm that the axon
was originated from a dendrite in eight cases. However, it should be
noted that this is not the case for all the wide-field vertical cells,
because in 3 of the 14 cases, we confirmed that the axons originated
directly from the soma. In the remaining three cases, the location of
the axon hillock could not be confirmed. According to these
speculations, in the four wide-field vertical cells in which the action
potential was generated at the normal threshold level (shown in Fig.
4F1), the EPSPs might have been induced in the
dendrites that did not possess the axon or the axon was originated from
the soma in those cells. However, the morphological evidence for these
speculations has not been obtained yet.
Input from the OT to neurons in the SGI
The effect of the OT stimulation was investigated in 32 SGI
neurons, and among them, 21 neurons were successfully stained with
biocytin. They consisted of seven fusiform cells, four pyramidal cells,
eight multipolar cells, one stellate cell, and one wide-field vertical
cell according to the classification of Ma et al. (1990) and Langer and
Lund (1974).
Figure 5 shows the results obtained from
a multipolar cell in the SGI. In response to depolarizing current
pulses, this neuron responded with repetitive firing with fairly
constant intervals, whereas in response to hyperpolarizing current
pulses, it showed inward rectification. This neuron had multipolar
dendrites (thick lines) and dense axonal projections and terminations
near the soma (thin lines). Stimulation of the OT induced EPSPs at
latencies of 5.6-11.4 msec (Fig. 5C,D1). The onsets
of the EPSPs fluctuated, suggesting that the EPSPs were induced by
disynaptic or polysynaptic linkage. Application of Bic remarkably
enhanced the late phase of the EPSPs, and the duration of EPSPs induced
by a single stimulus often exceeded 500 msec (Fig.
5D2). At the critical stimulus strength (17 µA in
this case), the amplitude and duration of the EPSPs varied markedly
from sweep to sweep, suggesting the existence of some nonlinear
activating mechanism in the pathway to the SGI neurons (Fig.
5E). The EPSPs were observed in 24 of the 32 SGI neurons, and the latencies of the EPSPs ranged from 3.4 to 47.4 msec
(Fig. 5F, closed columns). In two neurons, a small
EPSP component with short latency (<5 msec) occurred with fixed onset,
and the possibility of monosynaptic EPSPs could not be excluded.
However, they appeared to be minor among the present material. These
results indicated the existence of disynaptic or polysynaptic
excitatory pathways from the OT to SGI neurons and that the
transmission in the pathway is under strong suppression by GABAergic
neurons.
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Figure 5.
Synaptic potentials induced by the OT stimulation
in an SGI neuron. The morphology of the recorded neuron, stained with
biocytin, is illustrated in A. Dendrites are drawn as
thick lines. The axon and its collaterals are drawn as
thin lines. B shows the voltage responses
of this neuron to various current pulses. C shows the
synaptic responses of this neuron to the OT stimulation (50 µA) in
the control solution. D shows effects of application of
10 µM Bic (D1, Control;
D2, after application of Bic).
E shows the synaptic responses to the critical stimulus
strength (17 µA) for induction of long-lasting responses under the
application of 10 µM Bic. F shows
distribution of latencies of the EPSPs induced by the OT stimulation in
SGI neurons. Open columns in F indicate
the EPSPs recorded in the slice preparation with a transection shown in
Figure 6A.
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The OT-SGS/SO-SGI pathway
To further exclude the possibility of current spread to the
structures outside the OT, a transection was made to the slice just
medial to the stimulation site to spare the SGS and SO (Fig. 6A). Thirteen SGI
neurons were recorded in seven slices with such manipulation. In this
type of preparation, EPSPs could be induced in 11 SGI neurons by the OT
stimulation at virtually the same latencies (Figs. 5F, open
columns, 6C) at the submaximal stimulus strength for
the conduction volley in the OT (Fig. 6B). The
threshold for inducing EPSPs was 10-100 µA in these neurons (below
50 µA in nine neurons). In contrast to these preparations, the SGS
and SO were selectively cut, and the OT was stimulated lateral to the
transection in four slices (Fig. 6D). In these
slices, seven SGI neurons were recorded. In the neuron shown in Figure
6E,F, the OT stimulation at 500 µA did not induce
the conduction volley of the OT recorded medial to the transection or
the EPSPs in the SGI neurons. However, when the stimulus intensity was
increased to 1 mA, the conduction volley and the EPSPs started to
appear simultaneously. The threshold for inducing EPSPs was 400 µA-1 mA in four of the seven tested cells and above 1 mA in the remaining three cells after transection of the SGS and the SO. These results indicated that the current spread across the transection could occur
when the stimulus intensity was increased above 400 µA, but this
intensity was much higher than those that induced EPSPs in SGI neurons
in slices with transections sparing the SGS and SO (described above).
These results indicated that the EPSPs in the SGI neurons were induced
by the stimulation of the OT, and the possibility of current spread to
the structures outside the OT was excluded.
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Figure 6.
To exclude the possibility of current spread to
the structures outside the OT, two types of transection were made to
the slice as shown in A and D. In
A, a transection was made to spare the SGS and SO.
B shows the conduction volley in the OT recorded in the
SO at various stimulation strengths in the preparation shown in
A. Synaptic potentials under application of 10 µM Bic at each stimulus strength are illustrated in
C. In D, the SGS and SO were selectively
transected, and the OT was stimulated lateral to the transection.
Recordings of the conduction volley in the OT and synaptic potentials
in the SGI neurons were made medial to the transection.
E and F indicate the conduction volley in
the OT and the EPSPs in the SGI neurons under application of 10 µM Bic in the preparation shown in D,
respectively. Note that an extremely strong stimulus (1 mA) was
necessary to induce the conduction volley and the EPSPs.
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Synaptic transmission from SGS to SGI neurons
The effects of stimulation of the SGS were investigated in seven
SGI neurons located ventral to the stimulation site (Fig. 7A). Stimulation of the SGS
induced EPSPs in the SGI neurons (Fig. 7B) in the standard
Ringer's solution in five of seven cells tested. The thresholds for
inducing EPSPs were often below 10 µA. The latencies of the EPSPs
ranged from 3.8 to 20.0 msec (n = 5). When the latency
was short, the onsets of the EPSPs were constant from sweep to sweep
(Fig. 7B3). Thus, the minimal synaptic linkage was estimated
as monosynaptic. These EPSPs were much enhanced by application of Bic
(Fig. 7C2). The late component of the EPSPs was largely
abolished by application of APV (Fig. 7C3), and the remaining fast component was abolished by additional application of
CNQX (Fig. 7C4). In the remaining two SGI neurons,
stimulation of the SGS did not induce EPSPs in the standard Ringer's
solution, but long-latency EPSPs (14.3 msec in this case) could be
observed after application of Bic, suggesting lack of monosynaptic
linkage but existence of a polysynaptic pathway from the SGS to these SGI neurons (Fig. 7D1,D2). In these cases, additional
application of APV completely abolished the polysynaptic EPSPs (Fig.
7D3), suggesting that the activation of NMDA receptors was
essential for bringing the membrane potential of intercalated neurons
above the firing threshold level. All these results have suggested that excitatory synaptic transmission from the SGS to SGI neurons is mediated by both AMPA- and NMDA-type glutamate receptors, and among
them, NMDA receptors make a significant contribution.
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Figure 7.
Effect of stimulation of the SGS on an SGI neuron.
Experimental arrangement is shown in A. B
shows the EPSPs induced by the OT stimulation at different stimulus
strengths in the control solution. The effect of 10 µM
Bic on the EPSP (compare C1 and C2) and
of additional application of 50 µM APV
(C3) and of 50 µM APV plus 10 µM CNQX (C4). D
shows records from another SGI neuron. The OT stimulation did not
induce EPSPs in the control solution (D1); however, it
induced long-latency EPSPs under application of 10 µM Bic
(D2), which was completely abolished by application of
50 µM APV (D3).
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DISCUSSION |
This study presented electrophysiological evidence confirming the
existence of the excitatory pathway from the OT to SGI neurons via
neurons in the SGS and SO in rats. The excitatory synaptic transmission
in this pathway is mediated by both AMPA- and NMDA-type glutamate
receptors and is under strong suppression by the GABAergic system. We
believe that this basic circuit demonstrated in the present study using
young rats (P17-24) will remain in adult animals; however, we
have to keep in mind that the synaptogenesis in the SC reaches its peak
at P14 and continues until P30 (Warton and McCart, 1989), and
accordingly development of the SC is not completed in the animals we
used.
Optic fiber input to the SGS neurons
Visual synaptic transmission in the SGS has been studied by Binns
and Salt (1994) in anesthetized cats by a combination of extracellular
unit recording and iontophoretic application of neurotransmitter
antagonists. These authors observed that both NMDA- and non-NMDA-type
glutamate receptors contribute to visual synaptic transmission in the
SGS. In the present study, we used the SC slices obtained from
rats, and the appropriate stimulus strength for selective activation of
the OT was determined by measuring the stimulus strength that induces
the maximal conduction volley in the OT. This experimental preparation
enabled detailed analysis of the synaptic organization of the OT-SGS
synapses using the whole-cell patch-clamp technique. Furthermore,
combining intracellular staining with biocytin enabled us to identify
recorded cells. Previous morphological studies have revealed
that SGS neurons are composed of several subclasses (Sterling, 1971;
Langer and Lund, 1974; Norita, 1980). In the present study, we recorded
from at least five subclasses of neurons, and those that received
monosynaptic excitation included piriform cells, stellate cells, and
narrow-field vertical and horizontal cells.
Visual synaptic input to wide-field vertical cells in the SO
The present results showed that wide-field vertical cells in the
SO receive monosynaptic excitatory input from the optic tract on their
dendrites. We found that the spike generation of the wide-field
vertical cells is insensitive to the somatic membrane potential and
considered two possible explanations. (1) As described in Results, the
EPSP induced in the distal dendrites evoked a dendritic spike that
directly triggered the spike generation at the initial segment of the
axon originated from one of the dendrites, bypassing the soma. (2) The
OT axons made synapses on the axon of the wide-field vertical cell.
Morphological examinations are necessary to obtain a final conclusion.
Furthermore, generation of dendritic spikes or synaptic contact on the
axon should be examined by direct recording from dendrites or axons or
both. If possibility (1) is correct, it suggests that all the dendrites extended from the wide-field vertical cells are not equivalent, but
rather the one that carries the axon has a dominant effect on
generation of action potential over the others. Such a phenomenon has
also been observed in dopaminergic neurons in the substantia nigra
(Hausser et al., 1995). Thus, extensive projection of dendrites from
the wide-field vertical cells may suggest that these neurons possess a
wide visual receptive field; however, inputs on individual dendrites
are not equivalent, and the magnitude of visual response of these
neurons may vary depending on which dendrite received the input.
Connection from the OT to the SGI
The present study showed that stimulation of the OT induced
disynaptic or polysynaptic EPSPs in SGI neurons. Thus, the excitatory pathway from the OT to SGI neurons exists in the local circuit of the
SC. Morphological analysis and electrophysiological recordings from
SGS/SO neurons revealed possible neuronal elements comprising the
pathway. Intracellular staining with biocytin revealed that most SGS
neurons projected abundant axon collaterals and terminal bouton-like
structures in the ventral part of the SGS and the SO, but the number of
bouton-like structures decreased in the SGI. On the other hand, the
wide-field vertical cells in the SO extended divergent dendritic trees
into the SGS and projected axons and terminal bouton-like structures in
the ventral part of the SO and in the SGI. Therefore, wide-field
vertical cells in the SO can mediate indirect (via SGS neurons) visual
input to neurons in the SGI neurons. These neurons can also mediate direct visual input to the SGI neurons, because they receive
monosynaptic excitatory input from the OT on their dendrites.
Furthermore, some of the SGI neurons extended dendrites into the SO and
sometimes farther dorsally to the SGS (Lopez-Barneo and Llinás,
1988; Mooney et al., 1988; Hall and Lee, 1993; Saito and Isa, 1997).
This morphological evidence has suggested that SGI neurons receive
indirect visual input from SGS neurons mainly on their dendrites.
Although some SGI neurons could receive direct input from the OT on
their dendrites in the SGS/SO (Mooney et al., 1988), the direct
connection from the OT to SGI neurons appeared to be minor because
monosynaptic EPSPs were observed only in a small population of SGI
neurons in the present study.
It is not clear which type of SGS neurons is excitatory or inhibitory.
We have shown that various types of SGS neurons receive monosynaptic
excitatory input from the OT. Although Mize (1992) showed that
GABAergic neurons in the SGS include horizontal, stellate, and piriform
cells, it is not yet clear whether all neurons of these subclasses are
inhibitory. Thus, until it is revealed which subclass of the SGS
neurons with excitation from the OT is excitatory, it will not be clear
which subclass of SGS neuron mediates the excitatory synaptic
transmission from the OT to the SO and SGI neurons.
Regulation of signal transmission from the SGS/SO to the SGI
Freeman and Singer (1983) analyzed the synaptic input from the OT
to the SC by current source density analysis in anesthetized cats.
These authors showed that the synaptic current was induced mainly in
the SGS, but no large synaptic currents appeared to be induced in the
SGI. This suggested that the neural connection from the SGS or SO to
the SGI is not strong enough to elicit large synaptic currents in SGI
neurons in intact cats. However, the present study clarified that the
synaptic transmission from the OT to the SGI neurons is under strong
regulation by GABAergic system, because application of bicuculline
predominantly enhanced the EPSPs recorded in the SGI neurons (Fig.
5D). The importance of GABAergic input in controlling the
output from the SC has been shown by Hikosaka and Wurtz (1985), who
reported that injection of bicuculline remarkably increased the
occurrence of express saccades.
Thus, a possible explanation of the mechanisms to generate express
saccades is that the signal transmission from the SGS/SO to the SGI
neurons is suppressed in cases of regular saccades; however, the
transmission becomes facilitated, for example, in cases of express
saccades, possibly by disinhibition from GABAergic neurons.
Nonlinear activation mechanisms of SGI neurons
A unique property of the neural circuit in the SC is that the
output from the circuit has a nonlinear relationship with its input.
Induction of saccadic eye movements has an all-or-none relationship
with the stimulus strength of the SC (Robinson, 1972; Schiller and
Stryker, 1972). The present study showed that the EPSPs induced by the
OT stimulation were remarkably enhanced by application of bicuculline.
The enhanced EPSPs often lasted >500 msec. Such a phenomenon was not
observed in SGS/SO neurons and appeared to be a unique property of the
SGI neurons. These results suggested the existence of some nonlinear
regenerative property in the pathway to the SGI. The present study
showed that NMDA-type glutamate receptors play an important role in
mediating the signal transmission to the SGI neurons (Fig.
7E). NMDA-type glutamate receptors have negative slope
conductance below 30 mV of membrane potential. In this voltage range,
the more the cell is depolarized, the larger the current that passes
through the NMDA-receptor channels; thus the regenerative process can
be switched on. In addition, intrinsic properties of individual neurons
comprising the local circuit may contribute to the nonlinear property
of the circuit (Saito and Isa, 1997). The actual contribution of these
elements should be examined experimentally either in vivo or
in vitro.
| |
FOOTNOTES |
Received May 20, 1998; revised Aug. 3, 1998; accepted Aug. 5, 1998.
We express sincere thanks to Drs. Hiroshi Aizawa and Yasushi Kobayashi
for comments on this manuscript, Professor S. Ozawa for valuable
discussion, and Ms. Michi Seo, Junko Yamamoto, and Chika Kamada for
excellent technical assistance. This study was supported by grants from
the Ministry of Education, Science, Sports and Culture of Japan
(Project No. 08458266, 08279207, and 09268238), Japan Science and
Technology Corporation, Daiko Foundation, Naito Memorial Foundation,
and Uehara Memorial Foundation.
Correspondence should be addressed to Dr. Tadashi Isa, Department of
Integrative Physiology, National Institute for Physiological Sciences,
Myodaiji, Okazaki 444-8585, Japan.
| |
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Top
Abstract
Introduction
