Laboratoire de Neurophysiologie, Département de Physiologie, Faculté de Médecine, Université Laval, Québec G1K 7P4, Canada
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ABSTRACT |
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Martina, Marzia,
Sébastien Royer, and
Denis Paré.
Physiological Properties of Central Medial and Central Lateral
Amygdala Neurons.
J. Neurophysiol. 82: 1843-1854, 1999.
Mounting evidence implicates the central (CE)
nucleus of the amygdala in the mediation of classically conditioned
fear responses. However, little data are available regarding the
intrinsic membrane properties of CE amygdala neurons. Here, we
characterized the physiological properties of CE medial
(CEM) and CE lateral (CEL) amygdala neurons
using whole cell recordings in brain slices maintained in vitro.
Several classes of CE neurons were distinguished on the basis of their
physiological properties. Most CEM cells (95%), here
termed "late-firing neurons," displayed a marked voltage- and
time-dependent outward rectification in the depolarizing direction. This phenomenon was associated with a conspicuous delay between the
onset of depolarizing current pulses and the first action potential.
During this delay, the membrane potential
(Vm) depolarized slowly, the steepness of
this depolarizing ramp increasing as the prepulse
Vm was hyperpolarized from 60 to
90 mV.
Low extracellular concentrations of 4-aminopyridine (30 µM)
reversibly abolished the outward rectification and the delay to firing.
Late-firing CEM neurons displayed a continuum of repetitive
firing properties with cells generating single spikes at one pole and
high-frequency (
90 Hz) spike bursts at the other. In contrast, only
56% of CEL cells displayed the late-firing behavior
prevalent among CEM neurons. Moreover, these
CEL neurons only generated single spikes in response to
membrane depolarization. A second major class of CEL cells (38%) lacked the characteristic delay to firing observed in
CEM cells, generated single spikes in response to membrane
depolarization, and displayed various degrees of inward rectification
in the hyperpolarizing direction. In both regions of the CE nucleus,
two additional cell types were encountered infrequently (
6% of our
samples). One type of neurons, termed "low-threshold bursting
cells" had a behavior reminiscent of thalamocortical neurons. The
second type of cells, called "fast-spiking cells," generated brief
action potentials at high rates with little spike frequency adaptation
in response to depolarizing current pulses. These findings indicate
that the CE nucleus contains several types of neurons endowed with
distinct physiological properties. Moreover, these various cell types
are not distributed uniformly in the medial and lateral sector of the
CE nucleus. This heterogeneity parallels anatomic data indicating that
these subnuclei are part of different circuits.
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INTRODUCTION |
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Much evidence indicates that the amygdala
transduces the affective value of sensory events into endocrine,
visceral, and behavioral responses through divergent projections
reaching functionally diverse brain structures (Amaral et al.
1992; Davis 1992
; LeDoux 1995
).
Moreover, the amygdala appears to be the site of plastic synaptic
changes that mediate a well characterized form of fear learning termed
Pavlovian fear conditioning (LeDoux et al. 1990
; Miserendino et al. 1990
; Quirk et al.
1995
; Rogan et al. 1997
; Romanski and
LeDoux 1992a
,b
).
The central (CE) amygdaloid nucleus plays a pivotal role in this
respect as it is one of the main output structures of the amygdala.
Indeed, it is the prime source of amygdaloid projections to the brain
stem (Hopkins and Holstege 1978; Veening et al.
1984
). Moreover, lesions of the CE nucleus (Gentile et
al. 1986
; Hitchcock et al. 1989
; Iwata et
al. 1986
; Kapp et al. 1979
; Zhang et al. 1986
) or of its brain stem and hypothalamic targets
(Francis et al. 1981
; LeDoux et al. 1988
)
abolish conditioned fear responses.
Despite the important role of the CE nucleus, little is known about the
physiological properties of its neurons. So far, in vitro
electrophysiological studies have focused on the synaptic responses
(Nose et al. 1991; Rainnie et al. 1992
)
and spike after-hyperpolarizations (Scheiss et al. 1993
)
of CE neurons. In these studies, little attention was paid to possible
differences between the medial and lateral sectors of the CE nucleus
(CEM and CEL). This is an important point because the CEL and
CEM have different projection sites and contain
morphologically distinct cell types (reviewed in McDonald
1992
). For instance, the vast majority of
CEM neurons project to the brain stem, whereas
comparatively few CEL neurons do (Hopkins
and Holstege 1978
; Veening et al. 1984
). On the
input side, the CEL receives a dense projection
from the lateral amygdaloid nucleus, whereas the
CEM does not (Krettek and Price
1978
; Pitkanën et al. 1995
; Smith
and Paré 1994
). Moreover, the main cell type found in the
CEL resembles the medium spiny neurons of the
striatum (Hall 1972
), whereas CEM
cells tend to have a sparse to moderate spine density (Cassel
and Gray 1989
; Kamal and Tömböl
1975
; McDonald 1982
; Tömböl and
Szafranska-Kosmal 1972
).
Because the intrinsic membrane properties of neurons shape their
spontaneous activity and constrain their synaptic responsiveness (Llinás 1988), we characterized the physiological
properties of CEM and CEL
neurons using whole cell recordings in brain slices kept in vitro. This
study revealed that the CE nucleus contains multiple physiologically
defined classes of neurons that are not distributed homogeneously in
its lateral and medial sectors.
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METHODS |
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Preparation of amygdala slices
Coronal slices of the amygdala were obtained from Hartley guinea
pigs (250 g) of either sex. Prior to decapitation, the animals were
deeply anesthetized with sodium pentobarbital (40 mg/kg ip) and
ketamine (100 mg/kg ip). The brain was rapidly removed and placed in a
cold (4°C) oxygenated solution containing (in mM) 126 NaCl, 2.5 KCl,
1.25 NaH2PO4, 1 MgCl2, 2 CaCl2, 26 NaHCO3, and 10 glucose. A block containing the
amygdala was prepared and coronal sections (400 µm) were obtained
using a vibrating microtome. The slices were stored for 1 h in an
oxygenated chamber at room temperature. One slice was then transferred
to a recording chamber (submerged type) perfused with an oxygenated
physiological solution (2 ml/min). The temperature of the chamber was
gradually increased to 32°C before the recordings began.
Electrophysiological recordings
Current-clamp recordings were obtained with borosilicate
pipettes filled with a solution containing (in mM) 130 K-gluconate, 10 N-2-hydroxyethylpiperazine-N'-2-ethanesulfonic
acid, 10 KCl, 2 MgCl2, 2 ATP-Mg, and 0.2 GTP-Tris. In some experiments, Neurobiotin (0.5%) was added to the
intracellular solution. pH was adjusted to 7.2 with KOH and osmolarity
to 280-290 mOsm. With this solution, the liquid junction potential was
10 mV and the membrane potential (Vm) was corrected accordingly after
the experiments. The pipettes had resistances of 3-6 M
when filled
with the above solution. Recordings with series resistance higher than
15 M
were discarded.
Using trans-illumination of the slice (Fig. 1), the outline of the CE nucleus as well as the border between its lateral and medial sectors could be identified easily. Recordings were obtained under visual control using differential interference contrast and infrared video microscopy (IR-DIC). Recordings were carried out with an Axoclamp 2B amplifier (Axon Instruments, Foster City, CA) and a microcomputer equipped with pClamp software (Axon Instruments).
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Analyses were carried out off-line with the software IGOR (Wavemetrics, Lake Oswego, OR) and home-made software running on Macintosh microcomputers. When studying current-voltage relations, voltage measurements were performed at fixed time intervals with respect to the onset of current pulses (see Results and figure legends), unless the signal was distorted by spontaneous synaptic potentials. In such instances, the voltage was measured immediately before the synaptic event. The input resistance (Rin) was estimated in the linear portion of current-voltage plots. The membrane time constant was derived from single exponential fits to voltage responses in the linear portion of current-voltage relations.
Morphological identification of recorded cells
When recorded cells were dialyzed with Neurobiotin, the slices
were removed from the chamber and fixed for 1 to 3 days in 0.1 M
phosphate-buffered saline (pH 7.4) containing 2% paraformaldehyde and
1% glutaraldehyde. Slices were then embedded in gelatin (10%) and
sectioned on a vibrating microtome at a thickness of 60-100 µm.
Neurobiotin-filled cells were visualized by incubating the sections in
the avidin-biotin-horseradish peroxidase (HRP) solution (ABC Elite Kit,
Vector Labs, Burlingame, CA) and processed to reveal the HRP staining
(Horikawa and Armstrong 1988).
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RESULTS |
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A total of 161 CE neurons that had
Vm
60 mV and overshooting action
potentials were recorded in the present study. Of these neurons, 80 were recorded in the CEM and 81 in the
CEL. On the basis of their responses to
intracellular current injection, these neurons were subdivided in
several classes described below (see Table
1).
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CEM neurons
LATE-FIRING NEURONS. In the vast majority of CEM neurons (95%), there was a conspicuous delay between the onset of suprathreshold depolarizing current pulses and spike discharges (Fig. 2), hence the designation "late-firing neurons." During this delay, the Vm depolarized slowly, giving rise to a ramp lasting hundreds of milliseconds.
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REPETITIVE-FIRING BEHAVIOR.
In response to depolarizing current pulses, a continuum of
repetitive-firing behaviors was observed among late-firing neurons (Fig. 2). The two examples of Fig. 2 represent the opposite poles of
this continuum, where neurons generating single spikes were prevalent
(Fig. 2A) and those generating high-frequency (90 Hz) spike bursts (Fig. 2B) were infrequent (7.5%). The bursting
and nonbursting firing patterns were not dependent on the initial membrane potential; applying suprathreshold depolarizing current pulses
from Vms ranging from
60 to
90 mV
did not transform bursting cells into nonbursting ones and vice versa.
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ORIGIN OF THE DELAY TO FIRING.
The characteristic delay observed between the onset of depolarizing
current pulses and action potentials (Fig. 2A1 and
2B1) appeared to result from a marked voltage- and
time-dependent outward rectification in the depolarizing direction.
This is shown in Fig. 2, A2 and B2, where the
voltage responses of late-firing neurons to graded series of
subthreshold current pulses applied from rest is plotted as a function
of the injected current. In these graphs, crosses and circles refer to
the voltage responses measured 220 and 1920 ms after the pulse onset,
respectively. Although the initial and late responses to negative
current pulses were nearly identical, they differed for positive
current pulses that brought the Vm
beyond
65 mV (average difference of 6.6 ± 0.68 mV for
subthreshold current pulses of maximal amplitude; Figs. 2A2
and 2B2).
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CEL neurons
Two predominant types of CEL neurons were distinguished on the basis of their responses to intracellular current injection. A first class of cells, accounting for 56% of CEL neurons, displayed the late-firing behavior, which prevails in the CEM nucleus. A second class of CEL neurons, hereafter termed "regular spiking cells," lacked the characteristic delay to firing observed in CEM cells and generated single spikes in response to membrane depolarization. This class of neurons accounted for 38% of our sample.
Within each of these cell classes, there were large variations in the amplitude, shape, and duration of spike afterhyperpolarizations as well as in the amount of inward rectification (sag) in the hyperpolarizing direction. In other words, there was no systematic relation between these physiological features (afterhyperpolarizations, sags) and the above bipartite classification. In addition, late-firing and regular spiking neurons were intermixed in the CEL. They were not differentially distributed in particular sectors of this subnucleus.
LATE-FIRING NEURONS.
An example of late-firing CEL neuron is
shown in Fig. 8A. In response
to depolarizing current pulses, these cells displayed the
characteristic time-dependent outward rectification observed in
most CEM neurons. As in CEM
cells, the importance of this rectification increased as the prepulse
Vm was hyperpolarized (cf. Fig.
8A1, at 75 mV and Fig. 8A2, at
90 mV), and it
was abolished by bath application of 4-AP (30 µM, n = 4; not shown). However, in contrast to CEM cells,
late-firing CEL neurons only generated single
spikes in response to membrane depolarization. No late-firing bursting neurons were observed in the CEL nucleus.
Although the membrane time constant of late firing neurons was
significantly shorter in the CEL than that in the
CEM (two-tailed t-test,
P < 0.05), differences in
Rin did not reach statistical
significance (see Table 1).
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REGULAR SPIKING NEURONS.
Figure 8B illustrates the behavior of a regular spiking
CEL neuron. In contrast to late-firing
CEL neurons (Fig. 8A), these cells did
not display outward rectification in the depolarizing direction (Fig.
8B3) and lacked the typical delay to firing (Fig. 8B1). These neurons generated only single spikes in response
to depolarizing current pulses and did not display spike-frequency adaptation when repetitive spiking was elicited by depolarizing current
pulses 0.12 nA. However, various degrees of spike frequency adaptation were seen when the cells were challenged with higher depolarizing currents (not shown). These neurons had a significantly higher Rin, a longer membrane time
constant and a more depolarized resting potential than late-firing
CEL cells (two-tailed t-tests, P < 0.05; see Table 1).
Rare types of CEM and CEL neurons
Other types of CE neurons were encountered too infrequently
(6%) to allow meaningful quantitative analyses. One class of cells,
observed in both sectors of the CE nucleus, generated very brief action
potentials and was able to sustain high firing rates with little or no
spike frequency adaptation, hence the designation "fast-spiking
neurons." A second class of CE neurons, also encountered in both
sectors of the CE nucleus, had a behavior reminiscent of dorsal
thalamic relay neurons (Deschênes et al. 1982
;
Llinás and Jahnsen 1982
). Hereafter, they will be
referred to as "low-threshold bursting neurons."
It should be emphasized that the low percentage of fast-spiking and low-threshold bursting cells was obtained despite the fact that a deliberate attempt was made to record from somatic profiles with atypical shapes and/or diameters.
FAST-SPIKING NEURONS.
Three fast-spiking neurons were recorded in the
CEM (Fig.
9B) and one in the
CEL (Fig. 9A). These neurons were
characterized by a very high Rin
(ranging from 467 to 700 M), generated brief action potentials
(ranging from 0.5 to 0.6 ms at half-amplitude), and large spike
afterhyperpolarizations (range of 16 to 28 mV). A distinguishing
feature of fast-spiking neurons was their ability to sustain firing
rates as high as 100 Hz without spike frequency adaptation. However,
during current-evoked spike trains, fast-spiking CEM neurons always exhibited short pauses in
firing during which a low-amplitude Vm
oscillation occurred (Fig. 9B). This phenomenon was not
observed in the fast-spiking CEL cell.
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LOW-THRESHOLD BURSTING NEURONS.
Four low-threshold bursting neurons were recorded in the
CEL and one in the CEM. At
the break of hyperpolarizing current pulses applied from rest, these
neurons generated rebound spike bursts whose latency decreased as the
amplitude of the current pulses was increased (Fig.
10A2). The rebound spike
bursts rode on a slow depolarizing potential (13.8 ± 2.40 mV) of
variable duration (182 ± 79.2 ms; compare the cells depicted in
Fig. 10, A1 and B1). The intraburst frequency
varied markedly from cell to cell (from 50 to 200 Hz), but in all
cases, the duration of successive interspike intervals increased as the
burst progressed. Spike bursts with similar features could be elicited
by depolarizing current pulses applied at
Vms negative to 65 mV (data not
shown), but pulses of similar amplitudes elicited accommodating trains
of action potentials at depolarized
Vms (Fig. 10B1, top trace).
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Morphological properties of CE neurons
Intracellular injections of Neurobiotin were performed in 30 CE neurons belonging to the major physiologically defined cell classes described above. Twenty-one of these cells were recovered (CEM, 13 late-firing; CEL, 6 late-firing, and 2 regular spiking cells). The dendrites of all these cells remained within the confines of the nucleus where their soma was located.
Late-firing CEM neurons (Fig. 11, A1-A3) had an ovoid cell body (long axis, 24.1 ± 0.90 µM), collateralized axons bearing varicosities, and dendrites with a sparse to moderate spine density. Typically, they had two to three main dendritic trunks from which emerged a few secondary dendritic branches that rarely divided more than once. No consistent differences were found between the morphological properties of bursting (n = 4; Fig. 11, A2 and A3) and nonbursting (n = 9; Fig. 11A1) late-firing CEM cells.
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Compared with CEM cells, CEL neurons (Fig. 11, B1-B3) tended to have a more angular and smaller (long axis, 19.3 ± 1.02 µM; P < 0.05) soma from which emerged three to five primary dendrites. Most of these proximal dendritic segments branched several times within a short distance of the cell body (Fig. 11B1). The dendrites of late-firing CEL neurons, particularly their distal segments, were densely covered with spines. Local axonal ramifications of CEL neurons could be seen rarely, in contrast to CEM cells. In our admittedly limited sample of CEL neurons, no striking morphological difference was observed between late-firing (Fig. 11, B1-B2) and regular spiking (Fig. 11, B3) CEL cells.
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DISCUSSION |
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In the present study, the physiological and morphological properties of CE amygdala neurons were correlated using whole cell recordings and intracellular Neurobiotin injection in vitro. It was found that the CE nucleus contains several physiologically defined cell classes that are not distributed homogeneously in its lateral and medial sectors.
The most common type of CE neurons (95% of CEM
and 56% of CEL cells) were late-firing cells.
These neurons displayed a pronounced time- and voltage-dependent
outward rectification in the depolarizing direction that was associated
with a long delay to firing. In response to depolarization, late-firing
CEM cells generated repetitive single spikes or
high-frequency spike bursts. In contrast, only nonbursting late-firing
cells were seen in the CEL. On the other hand,
the CEL contained a second major class of cells
(38% of our sample) that lacked the characteristic delay to firing
observed in late-firing neurons and generated repetitive single spikes on membrane depolarization. Finally, two rare types of neurons, collectively representing 6% of our samples, were observed in both
sectors of the CE nucleus: cells that had a behavior reminiscent of
thalamocortical neurons ("low-threshold bursting cells") and fast-spiking neurons, which had a high
Rin, a fast time constant, and the
ability to sustain high firing rates without spike frequency adaptation.
Technical considerations
Filling recorded neurons with Neurobiotin precluded the use of the
perforated-patch method. As a result, the intrinsic membrane properties
of CE neurons might have been altered by exchanges between the
intracellular compartment and the pipette solution. However, the
electroresponsiveness and Vm of CE
neurons remained stable over time, implying that potential artifacts
introduced by the intracellular dialysis were immediate or too subtle
for detection. Similar conclusions were reached in a recent analysis of
the electrophysiological properties of hilar neurons
(Lübke et al. 1998). Consequently, we ascribe the
more polarized Vm of CE neurons
described here, in comparison to previous studies using conventional
intracellular recordings (Nose et al. 1991
;
Scheiss et al. 1993
), to the damage caused to the
membrane by the sharp micropipettes.
Another potentially confounding factor is the relatively young age of the animals used this study (2-4 wk old). Consequently, it is possible that the physiological properties of CE neurons change with maturation. Juvenile rather than adult animals were used because myelination increases with age, making it difficult to visualize neurons with IR-DIC.
Relationship between physiological and morphological features
Various parcellations of the CE nucleus have been proposed using
Nissl and Golgi staining as well as peptide immunoreactivity (Brodal 1947; Cassel and Gray 1989
;
Krettek and Price 1978
; McDonald 1982
;
Wray and Hoffman 1983
). However, considering that there is disagreement regarding this issue and since we could only
distinguish a lateral and a medial sector of the CE nucleus in
transilluminated slices, we used this classical bipartite parcellation
(Brodal 1947
; Krettek and Price 1978
).
Golgi studies (reviewed in McDonald 1992) have revealed
that the CEM and CEL each
contain one predominant morphological cell type (Hall
1972
; Kamal and Tömböl 1975
;
McDonald 1982
; Tömböl and
Szafranska-Kosmal 1972
). In the CEM, most
cells have an oval cell body, a collateralized and varicose axon, and
three to four poorly branched primary dendrites with a sparse to
moderate spine density. In the CEL, the
predominant cell type is termed "medium spiny neuron," in reference
to the main class of cells found in the striatum (Hall
1972
). These cells have a smaller soma than CEM neurons, a high-density of dendritic spines,
and multiple primary dendrites with numerous branching points. These
morphological features correspond well to those of the
Neurobiotin-filled CEM and
CEL cells recovered in the present study.
These considerations imply that morphologically uniform populations of CE cells can exhibit different physiological properties. For instance, CEL neurons with the typical medium spiny appearance could belong to the late-firing or regular spiking cell classes. Similarly, bursting and nonbursting late-firing CEM cells had similar morphological features. Conversely, our findings also show that morphologically different populations of CE cells can be endowed with similar physiological properties. The clearest example of this are the late-firing neurons of the CEL and CEM, which had distinct morphological properties but similar electroresponsive characteristics.
This equivocal relation between the physiological and morphological
properties of CE amygdala neurons parallels the results of
immunohistochemical studies (Cassel and Gray 1989),
where it was found that there is no obvious morphological difference
among medium spiny CEL neurons containing
different neuropeptides. Conversely, the same neuropeptides were
observed in different morphological types of CE neurons.
The lack of systematic association between morphological features and
electroresponsive behavior was also noted in other structures of the
CNS. In the cerebral cortex for instance, it was observed that aspiny
local-circuit neurons could display regular spiking, intrinsically
bursting, or fast-spiking discharge patterns (Thomson et al.
1996). Others noted that some physiologically identified corticothalamic neurons could behave like conventional cortical fast-spiking cells (Steriade et al. 1998
), a behavior
traditionally assumed to be expressed only by aspiny local-circuit
neurons (McCormick et al. 1985
).
Identity of the different physiologically defined cell classes
Even though we did not identify the projection site of late-firing
CEM neurons, it is likely that most of them have
brain stem projections. Indeed, it was reported that virtually all
CEM neurons are retrogradely labeled after large
retrograde tracer injections in the brain stem (Hopkins and
Holstege 1978). On the other hand, little can be said about the
projection site of CEL cells. This is due to the
fact that late-firing and regular spiking CEL
cells were intermingled and did not appear to be concentrated in
particular regions of the CEL, thus preventing
correlations with the results of tract tracing studies. As to the
identity of fast-spiking and low-threshold bursting neurons found in
both subnuclei, they might correspond to the rare intensely GABA
immunoreactive cells found in both sectors of the CE nucleus
(McDonald and Augustine 1993
; Nitecka and Ben-Ari
1987
; Paré and Smith 1993a
). However, this
idea awaits experimental confirmation.
Late-firing neurons are endowed with a slowly inactivating K+ conductance
Several factors suggest that late-firing neurons are endowed with
a slowly inactivating K+ conductance similar to
that previously described in striatal (Bargas et al.
1989; Nisenbaum et al. 1994
), hippocampal
(Storm 1988
), thalamic (McCormick 1991
),
and cortical (Hammond and Crépel 1992
) neurons. In
voltage clamp analyses (Gabel and Nisenbaum 1998
; McCormick 1991
; Storm
1988
), it was observed that this conductance activates around
65 mV, has relatively rapid activation kinetics, inactivates slowly,
requires hyperpolarization beyond
100 mV for full deinactivation, and
is sensitive to low µM concentrations of 4-AP.
These features are consistent with our current clamp observations.
First, late-firing neurons exhibited a marked outward rectification in
the depolarizing direction that increased as the prepulse
Vm was hyperpolarized. Second,
application of long depolarizing steps to near firing threshold gave
rise to long depolarizing ramps, suggesting that the underlying
conductance inactivated slowly. Last, the outward rectification and
depolarizing ramps were sensitive to low µM concentrations of 4-AP.
However, in contrast with previous descriptions in other cell types,
this current did not seem to undergo cumulative inactivation when
repetitive depolarizing current pulses were applied unless interpulse
intervals shorter than 1.5 s were used. Finally, it should be
noted that low 4-AP concentrations did not abolish the early component
of the outward rectification, suggesting that late-firing neurons are
also endowed with a fast A-type K+ conductance
(Rudy 1988; Storm 1988
).
The presence of these K+ currents is likely to
have important consequences for the activity of late-firing neurons. As
a result, depolarizing voltage transients caused by excitatory synaptic inputs will be attenuated. Moreover, in response to a sustained barrage
of excitatory synaptic inputs, the Vm
rise will be delayed. Of course, the magnitude of these alterations
will be dependent on the Vm prior to
the occurrence of the synaptic events, as the inactivation of the 4-AP
sensitive conductance is steeply voltage-dependent and recovers slowly
(McCormick 1991; Nisenbaum et al. 1994
;
Storm 1988
).
These considerations imply that the slowly inactivating
K+ conductance should tend to reduce the
spontaneous and synaptically evoked discharges of late-firing CE
neurons. Consistent with this, physiologically identified brain stem
projecting CE neurons were reported to have extremely low spontaneous
firing rates in conscious animals (Collins and Paré
1999; Pascoe and Kapp 1985
). However, inhibitory
synaptic inputs might also play an important role in this respect
(Collins and Paré 1999
; Nose et al.
1991
; Paré and Smith 1993b
; Sun et
al. 1994
).
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CONCLUSIONS |
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In summary, our results indicate that the CE nucleus contains several physiologically defined cells classes. These different types of neurons are not distributed homogeneously in the lateral and medial sectors of the CE nucleus, thus paralleling their involvement in distinct circuits. The distinctive physiological properties of the various types of CEM and CEL neurons are likely to be major determinants of their activity in the intact brain.
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ACKNOWLEDGMENTS |
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We thank D. R. Collins and E. J. Lang for comments on an earlier version of this manuscript and P. Giguère and D. Drolet for technical support.
This research was supported by the Medical Research Council of Canada.
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FOOTNOTES |
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Address reprint requests to D. Paré.
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 April 12, 1999; accepted in final form June 1, 1999.
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REFERENCES |
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