1Department of Anatomy and 2Department of Neurology, Neuroscience Training Program, Wm. S. Middleton VA Hospital, University of Wisconsin, Madison, Wisconsin 53706
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ABSTRACT |
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Zhu, J. Julius, William W. Lytton, Jin-Tang Xue, and Daniel J. Uhlrich. Intrinsic oscillation in interneurons of the rat lateral geniculate nucleus. By using the whole cell patch recording technique in vitro, we examined the voltage-dependent firing patterns of 69 interneurons in the rat dorsal lateral geniculate nucleus (LGN). When held at a hyperpolarized membrane potential, all interneurons responded with a burst of action potentials. In 48 interneurons, larger current pulses produced a bursting oscillation. When relatively depolarized, some interneurons produced a tonic train of action potentials in response to a depolarizing current pulse. However, most interneurons produced only oscillations, regardless of polarization level. The oscillation was insensitive to the bath application of a combination of blockers to excitatory and inhibitory synaptic transmission, including 30 µM 6,7-dinitroquinoxaline-2,3-dione, 100 µM (±)-2-amino-5-phosphonopentanoic acid, 20 µM bicuculline, and 2 mM saclofen, suggesting an intrinsic event. The frequency of the oscillation in interneurons was dependent on the intensity of the injection current. Increasing current intensity increased the oscillation frequency. The maximal frequency of the oscillation was 5-15 Hz for most cells, with some ambiguity caused by the difficulty of precisely defining a transition from oscillatory to regular firing behavior. In contrast, the interneuron oscillation was little affected by preceding depolarizing and hyperpolarizing pulses. In addition to being elicited by depolarizing current injections, the oscillation could also be initiated by electrical stimulation of the optic tract when the interneurons were held at a depolarized membrane potential. This suggests that interneurons may be recruited into thalamic oscillations by synaptic inputs. These results indicate that interneurons may play a larger role in thalamic oscillations than was previously thought.
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INTRODUCTION |
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The brain regularly switches between sleep and wakefulness, and
the transition between these two states is accompanied by dramatic
changes in synchronized neural activity (Steriade 1997; Steriade et al. 1993
, 1994
). Electroencephalographic
(EEG) studies show that a sleeping brain is dominated by
large-amplitude, slow-frequency oscillations, whereas an aroused brain
is dominated by low-amplitude, high-frequency oscillations. The
thalamus, the primary structure relaying sensory inputs from the
periphery to the cortex in mammals, is believed to play a key role in
generating and maintaining these rhythms (Steriade et al.
1993
). In fact, changes in thalamic rhythms are a dramatic
feature of sleep-wake transitions (Steriade et al. 1990
,
1993
). The thalamus is also implicated in abnormal thalamic rhythms, such as absence seizures (Steriade et al. 1993
;
Tsakiridou et al. 1995
; von Krosigk et al.
1993
).
Three basic neuron types were described in the thalamus (Jones
1985). Thalamocortical cells are excitatory and project an axon
to cortex. Local interneurons, which reside among the thalamocortical cells in the principal relay nuclei, and cells in the adjacent thalamic
reticular nucleus (TRN) are GABAergic, and their axons are restricted
to the thalamus. Thalamocortical and TRN cells are implicated heavily
in oscillations (Steriade et al. 1993
). Thalamocortical
cells can oscillate intrinsically at low frequencies (1-4 Hz, the
frequency range of delta oscillations in the EEG). The interplay of two
conductances, the low-threshold calcium conductance, It, and the hyperpolarization-activated cation
conductance, Ih, is crucial for this oscillation
(Destexhe et al. 1993
; Leresche et al.
1991
; McCormick and Huguenard 1992
;
McCormick and Pape 1990
; Soltesz et al.
1991
). The intrinsic oscillation in thalamocortical cells
prevails at a hyperpolarized membrane potential where
It and Ih are largely
deinactivated and activated, respectively. TRN cells are also endowed
with an intrinsic oscillation (Avanzini et al. 1989
;
Bal and McCormick 1993
). When a hyperpolarizing pulse is
injected, these cells respond at pulse offset with a dampening oscillatory sequence, which consists of cyclic (7-14 Hz, the frequency range of sleep spindles in the EEG) bursts of action potentials that
progressively decrease in frequency to rhythmic single spikes. The
cellular mechanisms underlying this dampening spindle-frequency oscillation differ somewhat from those that underlie the delta oscillation in thalamocortical cells. In TRN cells, the interaction of
It with a calcium-activated, nonselective cation
conductance, Ican, and the calcium-dependent
potassium conductance, IAHP, is thought to be
the mechanism underlying the oscillation (Bal and McCormick
1993
). Spindle-frequency oscillations may also be generated by
the reciprocal connection between thalamocortical and TRN cells, with
the promotion of the intrinsic properties of these cells (Bal et
al. 1995a
,b
; Huguenard and Prince 1994
;
Warren et al. 1994
).
Although the contributions of thalamocortical and TRN cells to
oscillations are well studied, the role of thalamic local interneurons in these rhythms is less clear. Results from in vivo studies suggest indirectly that interneurons can oscillate (Deschânes
et al. 1984; Steriade and Deschânes 1984
;
Steriade et al. 1976
), and recent in vitro studies
indicate that thalamic interneurons are endowed with critical
oscillation-related conductances, such as It,
Ih, and Ican
(Munch et al. 1997
; Pape and McCormick
1995
; Pape et al. 1994
; Williams et al.
1996
; Zhu et al. 1999a
,b
). However, the identity of the
interneurons in the previously mentioned in vivo studies was not
confirmed, and the results of recent in vitro studies of identified
interneurons led to the conclusion that thalamic interneurons neither
generate an intrinsic oscillation nor participate in oscillations that
occur in the thalamic slice (Bal et al. 1995a
;
McCormick and Pape 1988
). Other in vitro studies described rhythmic behavior in thalamic interneurons (Williams et al. 1996
; Zhu et al. 1995
).
It is possible that earlier in vitro studies that have not observed
oscillations failed to do so because the cells were compromised by the
sharp electrode impalements, which can introduce an artificial leak
(Staley et al. 1992). In this study, we used the whole
cell recording technique, which reportedly produces less leak during recording (Staley et al. 1992
). By using this technique
in an in vitro preparation, we found and characterized an intrinsic oscillation in interneurons of the thalamic lateral geniculate nucleus
(LGN). A preliminary report of this study appeared in abstract form
(Zhu et al. 1995
).
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METHODS |
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Electrophysiology
The slice preparation was described previously (Zhu and
Uhlrich 1997). Briefly, Sprague-Dawley rats (100-300
g) were deeply anesthetized by halothane. After decapitation, the brain
was quickly removed into cold (6-8°C) physiological solution
containing (in mM) 126 NaCl, 2.5 KCl, 1.25 NaH2PO4, 26 NaHCO3, 1 MgSO4, 20 dextrose, 2 CaCl2, at pH 7.35. The
solution was continuously bubbled with 95% O2-5%
CO2. Slices containing LGN, each 500 µm thick, were cut
from the tissue blocks with a microslicer. Slices were kept in
oxygenated physiological solution for
2 h before recording. During
the recording, slices were submerged in a Plexiglas chamber and
stabilized with a fine nylon net attached to a platinum ring (Edwards et al. 1989
). The chamber was perfused with
warmed, oxygenated physiological solution, and the half time for the
bath solution exchange was ~7 s. The temperature of the bath solution
in the chamber was kept at 34.0 ± 0.5°C. Antagonists were
applied with the bath solution.
The methods for tight-seal patch recordings follow Hamill et al.
(1981), with modification for brain slices (Blanton et al. 1989
; Edwards et al. 1989
). Patch electrodes
were made from borosilicate tubing (1.2 mm OD, 0.9 mm ID) with a
horizontal puller (Sutter Instruments). Electrode resistances were 7-9
M
. The standard intracellular solution (in mM) was 120 C6H11O7K, 10 N-2-hydroxyethylpiperazine-N'-2-ethanesulfonic acid, 5 ethylene glycol-bis(
-aminoethyl
ether)-N,N,N',N'-tetraacetic acid, 2 MgCl2, 4 ATP, 0.1 GTP, 0.5 CaCl2, 10 KCl, and biocytin 0.25% at pH 7.25. To obtain whole cell recordings,
electrodes were advanced into the slice while applying 0.1-nA current
steps lasting 200 ms. When a significant increase in electrode
resistance was evident, gentle suction was applied to attain a seal
resistance of
1 G
. The patch of membrane was broken by applying
more negative pressure to obtain a whole cell configuration.
Current-clamp recordings were performed on an Axoclamp-2A amplifier
(Axon Instruments). The bridge balance was continuously monitored and
adjusted. The optic tract was stimulated by a concentric bipolar
electrode with single voltage pulses (200 µs, 9 V). A 10-mV liquid
junction potential was subtracted from all membrane potentials.
We selected for study only interneurons with resting membrane
potentials negative to 50 mV, input resistances >300 M
, and overshooting action potentials. Except when noted, recordings were very
stable with little change in input resistance and resting membrane
potential throughout the entire recording period. The recordings
routinely lasted 1-6 h.
Autocorrelograms and second derivative calculations were done with
NEURON (Hines and Carnevale 1997).
Histology
After each recording, the slice was fixed by immersion in 4%
paraformaldehyde in 0.1 M phosphate buffer and resectioned at 60 µm
on a freezing microtome. Sections were processed histologically with
the avidin-biotin-peroxidase method to reveal the cell morphology (Horikawa and Armstrong 1988). Cells were subsequently
drawn with the aid of a camera lucida system.
Drugs and chemicals
The following compounds were purchased from Research Biochemical
International: (±)-2-amino-5-phosphonopentanoic acid
(DL-APV), -aminomethyl-4-chloro-benzeneethanesulfonic acid (saclofen), bicuculline methbromide, 6,7-dinitroquinoxaline-2,3-dione (DNQX), picrotoxin. ATP, biocytin, GTP, and all other chemicals were purchased from Sigma.
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RESULTS |
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We studied the response of 69 interneurons in rat dorsal LGN to
current clamp. In correspondence with previous studies (Munch et
al. 1997; Pape and McCormick 1995
;
Williams et al. 1996
; Zhu and Uhlrich
1997
), we found that LGN interneurons and
thalamocortical cells exhibited very different responses; interneurons
had a higher input resistance and longer membrane time constant than
thalamocortical cells (Fig.
1A). These two properties
alone were sufficient to distinguish the two cell types (Fig.
1B). The identity of all interneurons was confirmed
morphologically (Fig. 1C).
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Previously, others have shown that return of interneurons from a
hyperpolarizing holding state can generate a calcium-mediated burst
(Pape and McCormick 1995; Williams et al.
1996
). In our hands, a depolarizing current boost consistently
elicited such a burst (Zhu et al. 1999a
). Figure
2 shows that a still greater depolarizing
current injection generated a more vigorous burst response followed by
rhythmic burst activity. Such an oscillation occurred in 48 (70%)
interneurons in our sample. This subset of cells will be the focus of
the following characterization.
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The majority of interneurons studied produced oscillations regardless
of whether the prior holding potential was a hyperpolarization or a
depolarization. The sole factor required to produce an oscillation in
most cases was a slightly depolarized potential. This result differed
from earlier reports that show tonic firing at depolarized membrane
potentials (McCormick and Pape 1988; Pape and
McCormick 1995
; Williams et al. 1996
). A few
cells showed evidence of tonic firing (Fig.
3A) coexisting with an
oscillatory mode (Fig. 3B) that could be obtained with
slightly different holding potentials or depolarizing plateaus. In most
interneurons, however, no tonic firing was seen. In three oscillating
interneurons, a large variety of protocols was used in an attempt to
elicit tonic spiking. The protocols included the use of successive
depolarizing current steps (e.g., Fig. 9), slow depolarizing ramps,
depolarizing the cells to the point of sodium spike inactivation and
then slowly hyperpolarizing. These maneuvers were designed to
inactivate It and other channels that might be
responsible for repetitive bursting. In all of these cases, the cell
response was consistently oscillatory.
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Oscillation is intrinsic
To determine whether the oscillation observed was intrinsic or due
to circuitry, we tried blocking axonal conduction with tetrodotoxin
(TTX). Bath application of TTX blocked the oscillation (n = 3; Fig.
4B), leaving only an initial
calcium spike at depolarization onset (cf. Zhu et al.
1999a). This result demonstrated either that the oscillation
resulted from circuitry or that it was dependent on the sodium channel.
To distinguish between these possibilities, we blocked both excitatory
and inhibitory synaptic transmission with 30 µM DNQX, 100 µM
DL-APV, 20 µM bicuculline, and 2 mM saclofen. This
combined blockade of non-N-methyl-D-aspartate
(non-NMDA) glutamatergic, NMDA,
-aminobutyric acid-A
(GABAA) and GABAB receptors did not eliminate
the oscillation (n = 4; Fig. 4B). In two of the four cells, 10 µM picrotoxin, a more potent GABAA
receptor blocker, was also included with no effect. These results
suggest that the bursting oscillation in thalamic interneurons was
intrinsic and dependent on sodium channels.
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Although the oscillation was generated intrinsically, it could be
initiated through synaptic activation of the optic tract in cells held
just below firing threshold (Fig.
5B). At a slightly depolarized
membrane potential, optic tract stimulation evoked a large IPSP (cf.
Zhu et al. 1999a), followed by an oscillation similar to
that elicited by current injection (Fig. 5A).
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Basic properties of the bursting oscillation in interneurons
Figure 6 illustrates the oscillatory
responses of four representative interneurons to a series of
depolarizing current pulses. In general, the firing pattern showed two
components: a robust initial burst comparable to that described
previously (cf. Zhu et al. 1999a), followed by
repetitive bursting. Sometimes the initial response was not a single
burst but was instead two or more bursts in quick succession (Fig. 6,
B, middle, and D, top). The
sustained oscillation generally showed regularly recurring multispike
bursts with two to five action potentials at a 25- to 150-Hz intraburst
frequency. In two cells repetitive bursts had 10-16 action potentials
(not shown). In some cells the definition of the firing pattern to
large depolarizing currents was ambiguous, with only a small difference
between the intraburst interspike intervals and the interburst
interspike intervals (compare Fig. 6A, top and
bottom). In other cases, the firing pattern was quite regular (Fig. 6B, middle and top).
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The character of the oscillation depended on the intensity of the sustaining depolarizing current. Increasing the depolarizing current increased the duration of the initial burst and decreased the subsequent interburst intervals, resulting in higher-frequency oscillations. We used the first peak of the autocorrelogram to determine its frequency at different current injections (e.g., Fig. 6D, right). Results of this analysis are summarized for seven cells in Fig. 7. Interneurons that showed clear burst oscillations at all current injections (Fig. 6D) yielded a relatively shallow current-frequency slope. In contrast, interneurons that displayed nonburst firing at depolarized levels yielded a steeper current-frequency relationship.
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Inspection of the nonburst firing seen at high current injections suggested the possibility of two different firing patterns. In some instances, the hyperpolarization trajectory of the interspike intervals was similar to the sharp intraburst trajectory at lower current injections. In other cases, these trajectories seemed more similar to the dull interburst trajectory seen with lower depolarizing current. We therefore hypothesized that the former, sharp trajectories were associated with increased burst duration such that the burst was continued throughout the period of depolarization, whereas the latter, dull trajectories represented a reduction in burst duration to the point where each "burst" was only a single spike. This latter situation would then represent a continuation of burst oscillation dynamics, which may be denoted "single-spike oscillation" (Fig. 6B, middle and top).
To quantify the difference between these firing patterns, we measured
the sharpness of interspike hyperpolarizations by calculating the
average positive second derivative (Fig.
8). Sharp intervals have relatively large
second derivatives compared with rounded intervals, which have
relatively small second derivatives. At low depolarizations (Fig. 8,
bottom inset traces), the characteristic bursting
oscillation generally showed a bimodal distribution of intervals, dull
long trajectories from interbursts, and sharp, brief trajectories from
the intraburst intervals (Fig. 8, B-F, ). In
some cases, the distribution appeared to be trimodal, with evidence of
longer- and shorter-duration interspike intervals within the burst,
with corresponding dull and sharp trajectories (Fig. 8A).
When a higher depolarizing current was injected into the cell
(top inset traces), the interburst interval decreased in
duration. For most cells (e.g., Fig. 8, A, B,
D, and E), the distribution of intervals within
the burst remained similar in duration and sharpness to the
distribution produced at lower current injections. However, in several
cases, higher current levels gave interspike trajectories that were
uniformly dull, with second derivatives comparable to those of
interburst intervals at the lower activation levels (Fig. 8,
C and F). The small second derivative values of
these interspike intervals, similar to those of an interburst interval,
allows us to define these firing patterns as single spike oscillations.
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The pattern of oscillation depended on the intensity of the
depolarization during the oscillation, not on the holding potential before initiating the oscillation (Fig.
9). Varying the conditioning pulse did
alter the frequency of action potentials in the initial burst, as shown
previously (Zhu et al. 1999a). However, the conditioning pulse had little effect on the sustained oscillation. The pattern of
oscillation was generally the same even when preceded by a depolarizing
pulse (Fig. 9, top 2 traces). Varying the duration of the
preceding conditioning pulse also had no effect on the sustained
oscillation (not shown).
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The cells are illustrated oscillating for a short-duration, stopping after the termination of the depolarizing current. We tested other interneurons with longer depolarizing pulses (2 min, n = 3; 20 min, n = 1; not shown) and found that the oscillation lasted as long as the depolarizing current was present.
Role of input resistance
In some cells, we observed that the burst oscillation was lost over the course of the recording (n = 3, Fig. 10). In these cases, the transition appeared to be associated with a substantial loss of input resistance and a depolarization of 7-12 mV in RMP. Despite these signs of injury, we were able to see consistent single-spike responses for another 30-60 min. Hypothesizing that the reduction in resistance resulted from a partial loss of the gigaseal between the patch pipette and cell membrane, we broke the gigaseal and produced a comparable drop in input resistance in two other cells by lightly vibrating the electrode manipulator. These two cells also lost the capacity to oscillate and subsequently exhibited single-firing behavior.
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The previous result suggests that the ability to oscillate depends on
the input resistance of the cell. Thus we compared the input
resistances of the 48 cells that could sustain a burst oscillation with
21 cells that could not. The average input resistance in the former
group (643.1 ± 216.0 M) was higher than that in the latter
group (553.5 ± 163.8 M
; t-test, P < 0.05). However, input resistance is not a strong predictor of firing
behavior because we observed robust oscillations in cells whose input
resistances spanned the entire range in our sample.
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DISCUSSION |
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Oscillations in LGN interneurons
We have shown that local interneurons in the LGN can intrinsically
generate a low-frequency oscillation. The idea that interneurons can
oscillate is consistent with early studies by Steriade and colleagues
(Deschênes et al. 1984; Steriade and
Deschênes 1984
). In these previous in vivo studies,
putative thalamic interneurons were identified by their prolonged, slow
frequency burst firing after synaptic stimulation, a unique response
that was not observed in the larger sample of putative thalamocortical
cells (Burke and Sefton 1966
; Deschênes et
al. 1984
). The authors also showed that interneurons were
involved in both spontaneous and stimulus-evoked spindle oscillations
in vivo (Deschênes et al. 1984
; Steriade and Deschênes 1984
). In the previous studies, the
frequency of action potentials in each burst of the oscillation was
lower than that in thalamocortical cells, which is consistent with the
low intraburst frequency reported in this study (see also Zhu et
al. 1999a
). In addition, previous work also demonstrated that
the bursting phase of the oscillation in interneurons was opposite of
that in thalamocortical cells (Deschênes et al.
1984
), consistent with the interaction between inhibitory and
excitatory cell types (Andersen and Andersson 1968
).
Finally, both in vivo and in vitro studies reported spontaneous
oscillatory inhibitory postsynaptic potential (IPSP) sequences at
spindle frequency in thalamocortical cells (Pape and McCormick
1995
; Steriade et al. 1985
). These IPSP sequences persist after the TRN was disconnected anatomically from the
thalamocortical cells, suggesting that these events are generated by
the local interneurons (Steriade et al. 1985
).
Previous studies (Bal et al. 1995a;
McCormick and Pape 1988
), concluded that geniculate
interneurons are unable to generate oscillations. A few factors may
contribute to the difference with our results. First, we used the whole
cell technique, whereas the previous studies used sharp electrodes.
Impalement by sharp electrodes typically results in a decrease in input
resistance, especially in small neurons (Staley et al.
1992
). After impalement, the currents that originally were
large enough to support a bursting oscillation may no longer be
sufficient because of a decrease in input resistance. Furthermore, the
leak introduced by sharp electrodes will make it more difficult to see
dendritic activity. It is possible that the oscillations that we
recorded are being generated out in the dendrites and were thereby
inaccessible to sharp electrode recording. In this context, we note the
recent study of Williams et al. (1996)
, who also reported an intrinsic 10-Hz oscillation in LGN interneurons. Although they used sharp electrodes and reported input resistances below those of the current study, their resistances were considerably higher than those of other
studies that used sharp electrodes.
It is possible that we may have recorded from a different
population of interneurons from those in previous studies because at
least two populations of interneurons are present in the thalamus (Bal et al. 1995a; Famiglietti 1970
;
Gabbott and Bacon 1994
). However, we evaluated a large
number of interneurons and found nothing that would permit us to
dichotomize them physiologically or anatomically. Although the finding
of lower input resistance in cells that did not oscillate might suggest
that these belong to a different category, the appearance of this
firing pattern late in the recording of cells that previously
oscillated makes this unlikely. It is also possible that the
oscillation we observed might have resulted from the washout effect by
patch electrodes (Pusch and Neher 1988
). However, this
also seems unlikely: in many interneurons, the oscillation was found
immediately after the whole cell configuration was formed, before the
washout could occur. In some of these recordings, the access resistance
could be as high as 100 M
, although for most cells it was <20 M
.
Mechanism of oscillation in LGN interneurons
The nature of the interneuron oscillation appears to be
quite distinct from that of thalamocortical neurons. Although
thalamocortical cells oscillate at relatively hyperpolarized levels, a
depolarizing boost is necessary for the interneuron oscillation. Such a
depolarization would largely inactivate It and
would preclude activation of Ih, the two
channels critical to the thalamocortical oscillation (McCormick and Pape 1990).
Instead we suggest that the interneuron oscillation is more like that
seen in thalamic reticular neurons, which also oscillate at relatively
depolarized levels. Indeed, we recently showed that interneurons
possess Ican (Zhu et al. 1999a),
which is believed important in the TRN oscillation (Destexhe et
al. 1994
). The long-lasting inward current of
Ican may augment the depolarized state on which the bursts occur. Alternatively, the ability of TTX to eliminate the
oscillation suggests that this sustaining inward current might be a
persistent sodium channel. Other interpretations are possible and will
need to be explored further.
Functional significance of the intrinsic oscillation in interneurons
Thalamic oscillations appear to be involved in both normal
thalamic rhythms, such as those associated with sleep, and abnormal rhythms, such as absence seizures (Steriade et al. 1993;
Tsakiridou et al. 1995
; von Krosigk et al.
1993
). Recent studies demonstrated that both thalamocortical
and TRN cells are endowed with intrinsic rhythms that oscillate at
delta and spindle frequencies, respectively (Bal and McCormick
1993
; Leresche et al. 1991
; McCormick and
Pape 1990
; Soltesz et al. 1991
). Synaptic
connections between thalamocortical and TRN cells also support a delta
or spindle rhythm (Bal et al. 1995a
;
1995b
; Huguenard and Prince 1994
;
Warren et al. 1994
). It was therefore suggested that
these two cell types are responsible for generating and promoting these
thalamic rhythms (Steriade et al. 1993
; von
Krosigk et al. 1993
).
We found that thalamic interneurons also generate an intrinsic
oscillation across a frequency range that includes the delta and
spindle rhythms. Because interneurons are connected synaptically to
both thalamocortical cells and reticular cells (Ahlsén et al. 1985; Crunelli et al. 1988
; Liu et
al. 1995
; Paré et al. 1991
) and inhibitory
potentials can readily entrain postsynaptic firing (Andersen and
Andersson 1968
; Cobb et al. 1995
; Lytton and Sejnowski 1991
; Whittington et al. 1995
), we
suggest that interneurons also play a role in promoting and
synchronizing thalamic oscillations. This idea is consistent with in
vivo studies that showed bursting oscillations in thalamic interneurons
(Deschênes et al. 1984
; Steriade and
Deschênes 1984
). Further study will be needed to fully
explore the complex interactions of interneurons with thalamocortical
and TRN cells during thalamic oscillations.
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ACKNOWLEDGMENTS |
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This research was supported by the National Eye Institute (D. J. Uhlrich), the National Institute of Neurological Disease and Stroke (W. W. Lytton), and by the Office of Research and Development, Medical Research Service of the Department of Veterans Affairs (W. W. Lytton).
Present address of J. J. Zhu: Dept. of Cell Physiology, Max-Planck-Institute for Medical Research, Jahnstr. 29, Heidelberg D-69120, Germany.
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FOOTNOTES |
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Address for reprint requests: D. J. Uhlrich, Dept. of Anatomy, University of Wisconsin, 1300 University Ave., Madison, WI 53706.
Received 12 December 1997; accepted in final form 6 October 1998.
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REFERENCES |
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