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The Journal of Neurophysiology Vol. 82 No. 2 August 1999, pp. 754-767
Copyright ©1999 by the American Physiological Society
Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Saito, Yasuhiko and Tadashi Isa. Electrophysiological and Morphological Properties of Neurons in the Rat Superior Colliculus. I. Neurons in the Intermediate Layer. J. Neurophysiol. 82: 754-767, 1999. To begin characterizing the neural elements underlying the dynamic properties of local circuits in the mammalian superior colliculus (SC), electrophysiological and morphological properties of individual neurons in the intermediate layer [stratum griseum intermediale (SGI)] were investigated using whole cell patch-clamp recording and intracellular staining with biocytin in slice preparations from young (17-22 days old) and adult rats (7-8 wk old). Voltage responses to depolarizing current pulses of 223 neurons recorded in young rats were classified into six subclasses: regular-spiking neurons (n = 113), interspike intervals during depolarizing current pulses were constant; late-spiking neurons (n = 48), initiation of repetitive firing was delayed markedly from the onset of depolarizing pulses because of a transient hyperpolarization caused by A-like currents; burst-spiking neurons (n = 29), transient burst firing due to low-threshold Ca2+ channels were observed at the firing threshold level; fast-spiking neurons (n = 19), constant repetitive firings at frequencies >100 Hz were observed for the duration of the depolarizing pulse; neurons with marked spike frequency adaptation (n = 11), interspike intervals more than doubled due to spike frequency adaptation during depolarizing pulses; and neurons with rapid spike inactivation (n = 3), spike amplitude rapidly reduced, width increased during depolarizing pulses, and spiking was terminated after generating a few spikes. In response to hyperpolarizing current pulses, two different types of inward rectification were observed; time-dependent inward rectification by hyperpolarization-activated current (Ih; n = 29) and time-independent inward rectification (n = 111). Morphological analysis showed that neurons expressing time-dependent inward rectification by Ih had large somata, extended divergent dendrites dorsally into the superficial layers, and projected axons ventrally and sometimes dorsally, all characteristic features of wide-field vertical cells. Other neurons exhibited heterogeneous morphological properties, such as multipolar, fusiform, horizontal, or pyramidal-shaped cells. In adult rats, a total of 44 neurons showed similar electrophysiological properties except for the last type. These results indicate that the local circuits of the SC include neurons with at least five different firing properties and two different rectification properties; each with distinct electrophysiological and morphological characteristics that may be correlated with the functional output of the SC.
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The role of the mammalian superior colliculus (SC)
in visually guided behaviors, such as saccadic eye movements and
orientation, has long been an area of intense investigation (for
review, see Sparks 1986
; Wurtz and Albano
1980). Anatomically, the SC consists of several layers, each
with distinct neuronal organization and specific input-output
relationships. Optic fibers project to the SC through the optic layer
(the stratum opticum, SO). The stratum griseum superficiale (SGS)
receives visual input from the retina and the primary visual cortex.
The intermediate and deep layers (the stratum griseum intermediale, SGI
and the stratum griseum profundum, SGP) receive various nonvisual
sensory and cortical inputs. These layers send descending motor
commands to the brain stem reticular formation and the spinal cord and
ascending signals to the thalamus (Huerta and Harting
1982). The distribution of neurons related to control of
saccadic eye movements extends ventrally from the border between the
optic and intermediate layers to the deep layer (Moschovakis et
al. 1988b; Wurtz and Goldberg 1972).
In contrast to the abundance of anatomic studies of the SC
input-output, very little is known about the organization of its local
circuits and how visual information is processed in the SC to generate
motor commands. Moreover, although the morphological properties of
individual collicular neurons have been investigated in numerous
anatomic studies, the electrophysiological properties of the
morphologically identified cells have not (Hall and Lee 1993; Langer and Lund 1974; Ma et al.
1990; Norita 1980; Sterling 1971). Moschovakis and colleagues (Moschovakis and
Karabelas 1985; Moschovakis et al. 1988a,b)
studied the morphological characteristics of saccade-related neurons
using intracellular staining with horseradish peroxidase in alert and
anesthetized squirrel monkeys. The cells stained in their studies,
however, appeared to be limited to a population of large-sized
tectofugal neurons. Lopez-Barneo and Llinás (1988)
studied membrane properties of a population of neurons in the
intermediate layer of the SC. They described a specific group of
neurons that exhibited inward rectification at hyperpolarized membrane
potentials and have divergent dendritic trees that extend into the SGS.
Their description, however, was limited to this group of neurons and
did not include information about their axonal projections.
To determine how information is processed in the local circuits of the
SC, it is essential to characterize the membrane properties and
anatomic connectivity of individual neurons composing the circuits.
Furthermore it is also important to characterize the specific
conductances that determine the membrane properties of individual
neurons (Llinás 1988). In the present study, we
studied the electrophysiological properties of randomly selected
neurons in the movement-related layer (SGI) using whole cell
patch-clamp recording technique. At the same time we studied the
morphological characteristics of recorded cells by staining with
biocytin (Horikawa and Armstrong 1988). The present
results indicate that there are at least five subclasses of neurons
with distinct firing properties in the local circuits of the SGI and
each subclass is differentiated further according to rectification
properties in response to hyperpolarization. The difference in their
electrophysiological property, especially the rectification property,
was reflected in their morphological characteristics. These results,
together with our studies on the signal transmission in the local
circuits of the SC (Isa et al. 1998), may reveal the
fundamental aspects about the dynamic properties of the SC local circuits.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Slice preparations
Thin slices of the SC were prepared from young (17-22 days old) and adult (7-8 wk old) Wistar rats. The body weight of adult rats ranged from 180 to 270 g. In most cases, the brains were removed after decapitation under ether anesthesia. In some adult rats, the procedure was performed after transcardial perfusion of ice-cold sucrose-Ringer solution. After removal, the brains were submerged immediately in ice-cold sucrose-Ringer solution and bubbled with 95% O2-5% CO2 for 5-10 min. The sucrose-Ringer solution contained (mM): 234 sucrose, 2.5 KCl, 1.25 NaH2PO4, 10 MgSO4, 0.5 CaCl2, 26 NaHCO3, and 11 glucose. Frontal slices 200- to 300-µm thick (mostly 250 µm) were cut using a Microslicer (DTK-2000, Dosaka EM, Kyoto, Japan). They then were incubated in standard Ringer solution at room temperature for >1 h before recording. The standard Ringer solution contained (mM): 125 NaCl, 2.5 KCl, 2 CaCl2, 1 MgCl2, 26 NaHCO3, 1.25 NaH2PO4, and 25 glucose, and was bubbled continuously with 95% O2-5% CO2 (pH 7.4). After incubation, slices to be used for recording were placed individually in a recording chamber on an upright microscope (Axioskop FS, Zeiss, Germany) and continuously superfused with standard Ringer solution at a rate of 3-5 ml/min using 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 recording (Edwards et al. 1989;
Hamill et al. 1981) was performed in randomly selected
neurons in the SGI under visual control of the patch pipettes. Patch
pipettes were prepared from borosilicate glass capillaries (GC150TF-15,
Clark Electromedical Instruments, Pangbourne, UK) with a micropipette
puller (P-97, Sutter Instrument, Novato, CA). The pipettes were filled
with an internal solution containing (mM): 140 K-gluconate, 20 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. The osmolarity of the internal solution was
280-290 mOsm/l. The liquid junction potential of the patch pipette
solution and standard Ringer solution was estimated to be 
10 mV. The
measured membrane potentials were offset by this value to reflect the
actual membrane potential. The resistance of the electrodes was
2.5-7.0 M
in the bath solution, and the series resistance during
recording was 10-25 M. The electrophysiological properties of the
recorded cells were investigated in current clamp mode using an EPC-7
patch-clamp amplifier (List, Darmstadt, Germany). Depolarizing and
hyperpolarizing current pulses were given routinely to the cells with a
duration of 400 ms at 20- to 80-pA steps from two different levels of
the membrane potential (55 to 70 mV, and 75 to 90 mV) set by
varying the intensity of constantly injected current. The neurons were
classified according to their firing responses under these conditions.
The firing responses of the recorded neurons remained stable for 10 min
after establishment of the whole cell recording configuration. All the
recordings were performed at room temperature. Data were acquired and
analyzed using a pClamp hardware/software system (Axon Instruments,
Foster City, CA). The input resistance of each neuron was calculated from the voltage change induced by a hyperpolarizing current pulse (typically 40 pA) from the membrane potential of 60 to 70 mV. The
average firing frequency was calculated from the number of spikes
during the current pulse.
Histological procedure
To visualize the recorded neurons by biocytin staining
(Horikawa and Armstrong 1988), patch pipettes were
carefully detached from the cells after recording. Slices then were
fixed with 4% paraformaldehyde in 0.12 M phosphate buffer (pH 7.4) for
2-3 days at 4°C. The slices were rinsed in 0.05 M phosphate-buffered
saline (PBS, pH 7.4) and incubated in methanol containing 0.6%
H2O2 for 30 min. After
rinsing again in PBS, the slices were incubated in the solution
containing 1% avidine-biotin peroxidase complex (Vector Laboratories,
Burlingame, CA) and 0.3% Triton-X100 for 3 h. The slices were
rinsed in PBS and 0.05 M Tris-buffered saline (TBS, pH 7.6) and then
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 or neutral red, dehydrated, and then coverslipped.
Only cells with intact somata and proximal dendrites were drawn using a camera lucida attached to a light microscope. All quantitative data were expressed as means ± SE. T-test was used for statistical analysis.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In the present study, recordings were made from 223 neurons in
slices from young rats and 44 neurons in slices from adult rats. The
neurons were recorded in the SGI. Of these, 131 neurons from young rats
and 26 from adult rats were stained successfully with biocytin and used
for morphological analysis. Recording sites covered virtually all
regions of the SC, both mediolaterally and rostrocaudally. No
distribution bias was observed for any particular subclass of neurons
in the SC. Neurons with resting membrane potentials more negative than
60 mV and that exhibited action potentials more positive than 0 mV at
their peak were used for electrophysiological analysis.
Records from young rats
VOLTAGE RESPONSES TO DEPOLARIZING CURRENT PULSES. Regular-spiking neurons. Regular-spiking neurons (Fig. 1) exhibited repetitive firing with relatively constant interspike intervals in response to depolarizing current pulses (Fig. 1, A and D). Mild spike frequency adaptation was observed in some cases; however, an interspike interval never more than doubled the preceding one. The level of the resting membrane potential did not affect the regular firing property as shown in Fig. 1, B and C. The relationship between the average firing frequency and the amplitude of the injected current was analyzed systematically in 13 cells, and linear-like correlation was observed in all the cases according to the linear regression analysis (0.986 < r < 0.997, mean ± SD; 0.992 ± 0.004, P < 0.001) as shown in Fig. 1E. Fifty-one percentage (113/223) of neurons showed this type of firing responses.
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). Late spiking was observed when the depolarizing pulse was applied from a hyperpolarized level (85 mV; Fig.
2B). When the depolarizing current pulse was applied from a
more depolarized level (62 mV), late spiking was not observed and the
firing pattern became more regular (Fig. 2C). These results
suggest that the transient hyperpolarization is due to an A-like
transient outward current, which is inactivated at depolarized membrane
potentials (Connor and Stevens 1971). This suggestion is
supported by the observation that application of 4-aminopyridine, a
blocking agent of A channels, abolished the transient hyperpolarization
and changed the firing property of late-spiking neurons to resemble
that of regular-spiking neurons (Fig. 2D) (Gustafsson
et al. 1982; Thompson 1977). Twenty-two
percentage (48/223) of neurons showed this type of firing responses.
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). In
response to prolonged depolarizing current pulses, solitary spikes
followed the transient burst (Fig. 3A). The transient burst
was observed only when the depolarizing current pulse was applied at a
hyperpolarized membrane potential (82 mV in Fig. 3, A and
B; 78 mV in Fig. 3C). When the current pulse
was applied at a more depolarized membrane potential (66 mV in Fig.
3, D and E; 62 mV in Fig. 3F), no
transient burst or marked afterdepolarization was observed. Rebound
depolarization and spike generation was observed after termination of
the hyperpolarizing current pulse, when the resting membrane potential
was more depolarized (Fig. 3E) but not when hyperpolarized
(Fig. 3B). These results suggest that the rebound
depolarization was due to the same conductance as that underlying the
transient burst; the membrane potential in Fig. 3, A and
B, (82 mV) was below the threshold for activation of the
conductance, whereas the membrane potential in Fig. 3, D and
E (66 mV), was above the threshold for activation of the conductance, and the conductance therefore was inactivated by constantly holding the membrane potential at that level (Fig. 3D). Thirteen percentage (29/223) of neurons showed this
type of firing.
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89 mV; Fig. 6A). Five
percentage (11/223) of neurons showed this type of firing responses.
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). Cessation of firing may have been due to inactivation of Na+ channels,
because spike generation recovered after a brief pause (10-20 ms) in
the depolarizing pulse (Fig. 7C). Furthermore although the
number of the recorded cells was too small (n = 3) for
statistical analysis, the input resistance in neurons with rapid spike
inactivation was higher and whole cell membrane capacitance was smaller
than those in other type neurons.
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VOLTAGE RESPONSES TO HYPERPOLARIZING CURRENT PULSES.
Time-dependent inward rectification. In response to
hyperpolarizing current pulses, a group of neurons showed
time-dependent inward rectification as shown in Fig.
8. The neurons in Fig. 8, A-C, showed regular-, late-, and burst-spiking properties,
respectively. In all the cases, hyperpolarizing current pulses elicited
a rapid hyperpolarization followed by a slow redepolarization or a
"voltage sag" (arrow in Fig. 8). Thus the voltage sag was
observed in a subpopulation of regular-, late-, and burst-spiking
neurons (see Table 1). Previous studies
have shown that a voltage sag is caused by a
hyperpolarization-activated current
(Ih,
If, or
Iq) that is suppressed by
Cs+ but is resistant to
Ba2+ (DiFrancesco and Ojeda 1980;
Halliwell and Adams 1982; Mayer and Westbrook
1983; Takahashi 1990; Yanagihara and
Irisawa 1980). We tested the effects of
Cs+ and Ba2+ on the
time-dependent inward rectification in 13 cells. Application of 3 mM
Cs+ in the present study had little effect on the
voltage response during the early phase of the response (50 ms) but
eliminated the voltage sag (Fig. 9,
A-E). In contrast, Ba2+ did not
affect either the early or late phase of the response (Fig. 9,
F-J). An increase in membrane conductance due to the activation of Ih at hyperpolarized
membrane potentials also accounts for the significantly low input
resistance of neurons with Ih, which
have a membrane capacitance comparable with those without Ih (t-test,
P < 0.01, Table 1). After the end of current pulses, the membrane potential exhibited a rebound depolarization (Fig. 8,
double arrows).
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; Standen and Stanfield 1978) (see also DISCUSSION).
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MORPHOLOGICAL CHARACTERISTICS.
Neurons with time-dependent inward rectification by
Ih. Of the 29 neurons with time-dependent inward
rectification by Ih, 16 neurons were
successfully stained with biocytin. All extended divergent dendritic
trees dorsally (Fig. 11) that often
reached the SGS (Fig. 11, A, B, and D). These
morphological characteristics corresponded to those of wide-field
vertical cells (Langer and Lund 1974). Some of them, in
addition to extensive dorsal projection of dendrites, extended
dendrites ventrally and/or horizontally, sharing the characteristics of
multipolar cells (Fig. 11E). The axons were mostly projected
ventrally with few terminal-like structures nearby the somata (Fig. 11,
A, C, and D); however, some neurons showed
terminal-like fine collateralization and swelling of axons ventral to
the somata and/or projection of axons dorsally (Fig. 11B).
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Records from adult rats
We recorded a total of 44 neurons in slices obtained from adult rats (Table 2). Five of the six firing properties observed in young rats were found in adult rats; neurons with rapid spike inactivation were not recorded in adults.
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Among the nine neurons with time-dependent inward rectification by Ih, three neurons exhibited repetitive spike doublets in response to depolarizing pulses (Fig. 13, A and B). Such rhythmic spike doublets were never observed in the SGI in young rats.
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Twenty-six neurons from adult rats were stained successfully with biocytin. Among the nine neurons with Ih, six were stained, and all of them were wide-field vertical cells (Fig. 13, C and D). The other 20 stained neurons belonging to other subclasses consisted of 13 multipolar, 4 pyramidal-shaped, 2 fusiform, and 1 horizontal cells. Neurons recorded in adult rats tended to have higher input resistance and lower capacitance than those recorded in young rats except for neurons with Ih (Tables 1 and 2). It is, however, likely that there was a sampling bias for smaller neurons in slices because it was difficult for large cells to survive close to the surface of the slices made from adult rats.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The results of the present study indicate that when classified according to electrophysiological properties, there are at least five major types of firing responses to depolarizing pulses and two different inward rectification properties in the SGI neurons of rat SC. Thus there appears to be a wider variety of neurons in the local circuit of the SC of rat than indicated by previous studies. In addition, neurons described in previous studies can be categorized within the context of the subclasses described in the present study.
Neurons in the intermediate layer of slices of guinea pig SC have been
found to exhibit oval somata and extend divergent dendritic trees that
reached the stratum zonale (Lopez-Barneo and Llinás 1988). These neurons exhibit voltage sag in response to
hyperpolarizing current pulses, and some exhibit late-spiking property
due to an A-like current. Thus these neurons appear to correspond to wide-field vertical cells (Langer and Lund 1974) and the
regular-spiking neurons with time-dependent inward rectification by
Ih described in the present study or
the few cells that also exhibited late-spiking. Tecto-bulbo-spinal
tract neurons in cats have been found to be large multipolar cells that
exhibit marked inward rectification (Grantyn et al.
1983). These neurons appear to correspond to the regular-spiking neurons with time-independent inward rectification. The
present results showed that the time-independent inward rectification was suppressed by both Cs+ and
Ba2+. We performed voltage-clamp analyses and
observed a shift in the reversal potential of the inward rectifier
current (Cs+-sensitive current component) in
parallel to the predicted equilibrium potential for potassium when the
extracellular potassium concentration was changed (data not shown).
Previous studies have shown that inward rectifier potassium (IRK)
channels are blocked by both Cs+ and
Ba2+ (Hagiwara and Takahashi 1974;
Standen and Stanfield 1978). Thus the possibility is
raised that IRK channels contribute to the time-independent inward
rectification observed in the present study. Details of the
voltage-clamp analyses of IRK channels will be reported elsewhere
(unpublished data).
The results of the present study also indicate that the
morphological properties of the neurons, particularly the dendritic arborization, correlate with the presence of
Ih in the neuron. Wide-field vertical
cells expressed Ih and exhibited
time-dependent inward rectification in response to hyperpolarizing
current pulses. In response to depolarizing pulses, these neurons
primarily responded as regular-spiking cells; however, some of these
neurons exhibited late or burst spiking. The morphology of the
wide-field vertical cells in the SGI suggests that they receive direct
or indirect visual information from the optic tract in the SGS and SO
on their dendrites and transmit it to deeper layers, that is, the SGI
and SGP. If so, these neurons are involved in the signal transmission in the direct visuomotor pathway in the SC (the optic
tract-SGS/SO
SGI) (Isa et al. 1998). In contrast,
multipolar, pyramidal, fusiform, and horizontal cells did not exhibit
Ih, but many of them exhibited time-independent inward rectification due to activation of presumably IRK channels. In response to depolarizing pulses, these neurons showed
heterogeneous firing properties; they responded either as regular-,
late-, burst-, or fast-spiking neurons or neurons with marked spike
frequency adaptation. Further analysis of these neurons focusing on
additional characteristics, such as their projection pattern (output
neurons or interneurons) or postsynaptic effects (excitatory or
inhibitory), may give rise to a more distinct classification.
Neurons with firing properties similar to those described in the
present study also have been described in other regions of the CNS.
Regular-spiking neurons have been described primarily in the neocortex
(Connors and Gutnick 1990; McCormick et al.
1985), although the regular-spiking neurons recorded in the
present study exhibited milder spike frequency adaptation than
neocortical neurons. Those in the neocortex appeared to be more similar
to the neurons with marked spike frequency adaptation described in the
present study. Regular-spiking neurons with time-dependent inward
rectification by Ih have been
described in the thalamus (McCormick and Pape 1990) and
striatum (Jiang and North 1991; Kawaguchi
1993). Late-spiking neurons have been described in vagal motor
nucleus (Yarom et al. 1985), pedunculopontine tegmental
nucleus (Kang and Kitai 1990), nucleus tractus
solitarius in the medulla (Dekin et al. 1987), neocortex
(Kawaguchi 1995), and cochlear nucleus (Fujino et
al. 1997). Fast-spiking neurons have been described in the
neocortex (Connors and Gutnick 1990; McCormick et
al. 1985) and hippocampus (Han et al. 1993;
Kawaguchi and Hama 1988; Kawaguchi et al.
1987; Schwartzkroin and Mathers 1978).
Burst-spiking neurons with low-threshold Ca2+
channels have been described in the neocortex (Connors and
Gutnick 1990; McCormick et al. 1985), thalamus
(Jahnsen and Llinás 1984), and pedunculopontine
tegmental nucleus (Kang and Kitai 1990). The properties
of the neurons described in the present study illustrate that the
diversity of electrophysiologically distinct neurons present in the SGI
of the SC is comparable with other regions of the CNS.
Development of the SC local circuits
In the present study, 17- to 22-postnatal-day-old rats were mainly
used, because in general visually controlled patch-clamp experiments
become extremely difficult in slice preparations from older animals.
Developmental studies of the SC indicate that although calbindin-D28k-containing neurons exhibit adult-like distribution by
the end of the first postnatal week (Dreher et al. 1996)
and SC neurons exhibit adult-like dendritic trees 15 days postnatal, dendritic growth continues beyond 30 days (Warton and Jones
1985). Thus it is likely that the SC circuits were still in the
course of development in the rats used in the present study. Data from adult rats (7-8 wk old) demonstrated the presence of five subclasses of the firing responses in young rats; only neurons with rapid spike
inactivation were not observed. Although the sample size was limited,
the morphological characteristics of immature cell-like appearance
suggested that these neurons might be in the course of development or
cell death that is normally occurring in the developing SC
(Warton and Jones 1984). In adult rats, neurons exhibiting time-dependent inward rectification caused by
Ih were exclusively wide-field
vertical cells, and thus correlation between morphological and
electrophysiological properties was preserved. In adult rats, there
appeared to be a larger proportion of burst- and fast-spiking neurons
than in young rats. This may reflect developmental processes; however,
it is also possible that this result was due to a sampling bias. In
addition, some of neurons with time-dependent inward rectification by
Ih in adult rats exhibited a unique
electrophysiological property not observed in young rats; repetitive
spike doublets were observed. Such doublets of spikes also have been
observed in SO neurons by Lo et al. (1998), who showed
that SO neurons express voltage sag by
Ih and repetitive doublets of spikes
by intracellular recordings in adult rat SC slices. These neurons were
mostly wide-field vertical cells and looked quite analogous to the SGI
neurons with Ih recorded in the
present study. This firing property may contribute to the oscillatory
activity in SC circuits (Anderson and O'Steen 1975; Mandl 1993).
In conclusion, the comparison of data obtained from rats of different ages suggests that developmental changes may still be occurring 17- to 22-days postnatal; however, most of the properties observed in neurons from young rats were stable and observed in adult rats.
Functional significance of firing characteristics in relation to dynamic properties of the SC local circuits
Among the subclasses of SGI neurons, the regular-spiking neurons
composed the largest population (Tables 1 and 2). Regular-spiking neurons recorded in the present study exhibited more regular firings and milder spike frequency adaptation than those described in the
neocortex (Connors and Gutnick 1990; McCormick et
al. 1985). Such firing property may have significance in the
generation of discrete motor commands to control precise movements. In
addition, the SC circuits contain other subclasses of neurons that
exhibited marked nonlinear input-output relationships. Among these
subclasses, burst-spiking neurons may be suited for the detection of
changes in sensory events because they are strongly activated,
particularly when the neuron is excited at more hyperpolarized membrane
potentials, due to the activation and inactivation properties of
low-threshold Ca2+ channels. Late-spiking neurons
exhibited voltage-dependent change in firing property; repetitive
firing was suppressed at hyperpolarized membrane potentials but release
from the suppression occurred in a depolarization-dependent manner.
These properties may enable these neurons to discharge a large number
of spikes in response to excitatory input only when the cell is
concurrently depolarized.
The present study also provides evidence for the presence of specific
ionic conductances in each subclass of neurons. Inward rectification in
several subclasses of neurons appears to be due either to IRK channels
or Ih. The characteristic firing of
late-spiking neurons appears to be due to A-like transient outward
currents. Although not specifically investigated in this study,
Ca2+-activated K+ channels
may have a significant role in the firing property of neurons with
marked spike frequency adaptation (Blatz and Magleby 1987; Sah 1996). The channels mediating the
characteristic electrophysiological properties of each subclass of
neurons are known to be significantly modulated by several
neurotransmitter systems, such as acetylcholine and enkephalin (see
Nicoll et al. 1990). Then a question may arise as to
whether the classification of neurons made in the present study is
exclusive or not. We recently found that regular-spiking neurons in the
SGI express fast inactivating transient outward currents (A channels),
the amplitude of which is smaller than those in late-spiking neurons
(Saito and Isa 1998). Thus some aspects of the
classification made in the present study may be a matter of quantity of
a particular ionic conductance. Therefore the firing properties in some
cases can be modulated significantly by change in amplitude of a
particular ionic conductance that determines the firing properties
under physiological conditions, e.g., by action of neurotransmitters.
Further studies of the transmitter systems innervating the SC are needed to determine their role in modulating the signal transmission in the local circuits and possibly give rise to interesting hypotheses as to how SC modulation may effect changes in the behavioral response of the animal.
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ACKNOWLEDGMENTS |
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The authors thank Prof. Seiji Ozawa and Drs. Wen-Jie Song, Hiroshi Aizawa, and Yasushi Kobayashi for comments on the manuscript and helpful discussions, and M. Seo for technical assistance.
This study was supported by grants from the Ministry of Education, Science, Sports, and Culture of Japan (Grants 08279207, 08458266, and 09268238) and by grants from the Japan Science and Technology Corporation and Uehara Memorial Foundation.
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FOOTNOTES |
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Address reprint requests to T. Isa.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 29 July 1997; accepted in final form 13 April 1999.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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T. Sooksawate, K. Isa, and T. Isa Cholinergic Responses in Crossed Tecto-Reticular Neurons of Rat Superior Colliculus J Neurophysiol, November 1, 2008; 100(5): 2702 - 2711. [Abstract] [Full Text] [PDF]
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J. D. Cohen, A. Hirata, and M. A. Castro-Alamancos Vibrissa Sensation in Superior Colliculus: Wide-Field Sensitivity and State-Dependent Cortical Feedback J. Neurosci., October 29, 2008; 28(44): 11205 - 11220. [Abstract] [Full Text] [PDF]
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T. Endo, E. Tarusawa, T. Notomi, K. Kaneda, M. Hirabayashi, R. Shigemoto, and T. Isa Dendritic Ih Ensures High-Fidelity Dendritic Spike Responses of Motion-Sensitive Neurons in Rat Superior Colliculus J Neurophysiol, May 1, 2008; 99(5): 2066 - 2076. [Abstract] [Full Text] [PDF]
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X. Li, B. Kim, and M. A. Basso Transient Pauses in Delay-Period Activity of Superior Colliculus Neurons J Neurophysiol, April 1, 2006; 95(4): 2252 - 2264. [Abstract] [Full Text] [PDF]
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M. Takahashi, Y. Sugiuchi, Y. Izawa, and Y. Shinoda Commissural Excitation and Inhibition by the Superior Colliculus in Tectoreticular Neurons Projecting to Omnipause Neuron and Inhibitory Burst Neuron Regions J Neurophysiol, September 1, 2005; 94(3): 1707 - 1726. [Abstract] [Full Text] [PDF]
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Y. Saito and T. Isa Organization of Interlaminar Interactions in the Rat Superior Colliculus J Neurophysiol, May 1, 2005; 93(5): 2898 - 2907. [Abstract] [Full Text] [PDF]
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Y. Saito and T. Isa Laminar Specific Distribution of Lateral Excitatory Connections in the Rat Superior Colliculus J Neurophysiol, December 1, 2004; 92(6): 3500 - 3510. [Abstract] [Full Text] [PDF]
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Y. Saito and T. Isa Local Excitatory Network and NMDA Receptor Activation Generate a Synchronous and Bursting Command from the Superior Colliculus J. Neurosci., July 2, 2003; 23(13): 5854 - 5864. [Abstract] [Full Text] [PDF]
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 R. Ruscheweyh and J. Sandkuhler Lamina-specific membrane and discharge properties of rat spinal dorsal horn neurones in vitro J. Physiol., May 15, 2002; 541(1): 231 - 244. [Abstract] [Full Text] [PDF]
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H. Luksch, H. J. Karten, D. Kleinfeld, and R. Wessel Chattering and Differential Signal Processing in Identified Motion-Sensitive Neurons of Parallel Visual Pathways in the Chick Tectum J. Neurosci., August 15, 2001; 21(16): 6440 - 6446. [Abstract] [Full Text] [PDF]
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Y. Saito and T. Isa Voltage-gated transient outward currents in neurons with different firing patterns in rat superior colliculus J. Physiol., October 1, 2000; 528(1): 91 - 105. [Abstract] [Full Text] [PDF]
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B. Santoro, S. Chen, A. Luthi, P. Pavlidis, G. P. Shumyatsky, G. R. Tibbs, and S. A. Siegelbaum Molecular and Functional Heterogeneity of Hyperpolarization-Activated Pacemaker Channels in the Mouse CNS J. Neurosci., July 15, 2000; 20(14): 5264 - 5275. [Abstract] [Full Text] [PDF]
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in B)], were measured and plotted.
F-I: effect of extracellular application of 1 mM
Ba2+. Details as in B-E.
