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1Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, Kentucky 40292; and 2Department of Cell Biology and Anatomy, Louisiana Health Sciences Center, New Orleans, Louisiana 70112
Submitted 23 December 2002; accepted in final form 28 February 2003
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ABSTRACT |
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INTRODUCTION |
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).
Although anatomical distinctions between these nuclei are well established,
there has been little attention given to the possibility that cells in these
nuclei possess different functional properties.
Much is known about the electrophysiological properties and firing
characteristics of first-order neurons, such as thalamocortical (relay) cells
in the dorsal lateral geniculate nucleus (LGN). These cells transmit retinal
signals to the visual cortex by means of single spike (tonic) or burst firing
response modes (McCormick and Feeser
1990; Sherman
2001; Steriade and
Llinás 1988). Tonic firing prevails at depolarized membrane
levels and ensures a relatively accurate transfer of retinal signals. Burst
firing, a high-frequency barrage of action potentials that ride the peak of a
low-threshold Ca2+ spike, occurs at more hyperpolarized
levels and introduces a highly nonlinear form of signaling. Burst and tonic
modes play a key role in thalamic signaling and underscore how first-order
relay neurons actively modulate the gain and efficacy of signal transmission.
However, few studies have explored the firing modes and intrinsic membrane
properties of higher-order relay cells (Hu
1993; Monckton and McCormick
2002; Zhu and Heggelund 2001). To examine the electrophysiological
properties of cells in a higher-order thalamic nucleus, we made in vitro
intracellular recordings of relay cells in the rat lateral posterior nucleus
(LPN).
The LPN receives visual input from the retinorecipient zone of the superior
colliculus as well as the visual cortex
(Li and Bickford 2001;
Li et al. 2003;
Mason and Groos 1981;
Takahashi 1985). The LPN is
considered a higher-order nucleus because it is innervated by two different
types of cortical terminals that originate in layers V and VI
(Bourassa and Deschênes
1995; Guillery
1995; Li et al.
2003). It has been proposed that higher-order thalamic neurons are
distinct from first order thalamic neurons because their response properties
may be driven by cortical rather than subcortical inputs
(Guillery 1995).
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METHODS |
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Examples of thalamic slices containing the LPN and our basic experimental
approach are shown in Fig. 1.
We used coronal or parasaggittal slices to obtain intracellular recordings
from neurons within the LPN. Sharp-tipped electrodes made of borosilicate
glass (Sutter Instruments, Novato, CA) and filled with 4 M KAC or a 2%
solution of biocytin dissolved in 2 M KAC were used to record intracellular
voltage responses. Electrodes were pulled horizontally (P97, Sutter
Instruments) to a final impedance of 60–120 M
. Intracellular
responses were collected in current-clamp mode with a high-impedance amplifier
(Axoclamp 2B, Axon Instruments, Union City, CA) using techniques described
elsewhere (Guido et al. 1997,
1998). Neuronal activity was
digitized at 10 kHz (Instrutech VR10B, Port Washington, NY) and stored
directly on computer. Current and voltage data were acquired and analyzed
using pulse and pulsefit (HEKA, Port Washington, NY) software programs.
Adjustments in membrane potential were controlled by injecting DC current
through the recording electrode. Current-voltage relations were examined at
different membrane potentials by injecting a series of square wave current
pulses (±1 nA, 0.01- to 0.1-nA steps, 300–700 ms) to reach steady
state. The voltage responses to these current steps were also used to
determine the presence and operating range of voltage gated conductances and
to explore the repetitive firing characteristics of LPN cells. In some
instances, the K+ channel blockers apamin (250–500 µM)
tetraethylammonium (TEA; 10 mM) or 4-aminopiridine (4-AP, 500 µM to 1 mM)
were applied locally into the interface recording chamber. In other
experiments, NiCl2 (1–2 mM) or CsCl (2 mM) were added to the
bath.
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During intracellular recording, some LPN neurons (n = 51) were
filled with biocytin by passing alternating positive and negative current
pulses (±1 nA, 30 ms, 100–300 pulses) through the recording
electrode. Slices containing biocytin filled cells were placed in a fixative
solution of 4% paraformaldehyde in 0.1 M phosphate buffer (PB) for 48 h and
processed using the ABC method (Guido et
al. 1997; Horikawa and
Armstrong 1988). Labeled cells were photographed and drawn using a
camera lucida attachment. Soma sizes were measured using a digitizing tablet
and SigmaScan software (SPSS, Chicago, IL).
To stain cells in the LPN that contained gamma amino butyric acid (GABA), two rats were deeply anesthetized with pentobarbital sodium (30 mg/kg) and perfused through the heart with tyrode solution followed by a fixative solution of 4% paraformaldehyde and 1% glutaraldehyde in PB. The brain was removed and 50-µm-thick sections were cut with a vibratome. The sections were incubated overnight in a 1:4,000 dilution of a rabbit-anti-GABA antibody (Sigma Chemical, St. Louis, MO). The next day the sections were incubated in a biotinylated goat-anti rabbit antibody for 1 h, ABC for 1 h, and reacted with nickel enhanced diaminobenzidine. GABA stained somata were drawn and measured as described in the preceding text.
To illustrate the boundaries of the LPN, two rats were perfused with tyrode solution followed by a fixative solution of 4% paraformaldehyde in PB. The brain was removed and 50-µm-thick sections were cut on a vibratome. The sections were incubated overnight in a 1:3,000 dilution of a mouse-anti-parvalbumin antibody (Sigma). The next day the sections were incubated in a biotinylated goat-anti mouse antibody for 1 h, ABC for 1 h, and reacted with nickel enhanced diaminobenzidine.
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RESULTS |
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).
Biocytin-labeled cells in the LPN also had multipolar dendritic arbors
consistent with those of class A thalamocortical cells
(Grossman et al. 1973;
Webster and Rowe 1984). Taken
together, these results indicate our recordings were made from thalamic relay
cells.
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Intrinsic membrane properties of LPN cells
The voltage responses to square-wave current pulses were used to explore
the passive and active membrane properties of LPN relay neurons. Examples are
shown in Figs. 2,
3,
4,
5. Measurements of these
responses revealed that input resistance (55 ± 19M; n =
94), resting membrane potential (–60 ± 4 mV; n = 67),
and spike amplitude (64 ± 7mV; n = 80) are similar to those of
LGN relay neurons (Williams et al.
1996). An examination of I-V relations also indicated
substantial nonlinearities in the voltage responses to current pulses
(Fig. 2E). Indeed, LPN
cells possessed many of the same voltage-gated conductances found in
first-order relay neurons (McCormick
1992; Williams et al.
1996). This included delayed firing in response to depolarizing
current pulses (Fig.
2D, a), and a hyperpolarization-activated depolarization
(Fig. 2D, b) and
rebound burst firing (Fig.
2D, c) in response to hyperpolarizing current pulses.
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All recorded LPN cells displayed a low-threshold (LT) T-type Ca2+ conductance. Activation gave rise to a large triangular depolarization and burst firing at hyperpolarized membrane potentials. Passive membrane repolarization on termination of a hyperpolarizing current pulse of sufficient strength and duration evoked large "rebound" LT spikes and burst firing. These events were also activated by a depolarization from a steady hyperpolarized state (see Fig. 5). LT spikes could be blocked by bath application of Ni2+ (n = 3, data not shown), indicating they are mediated by a T-type Ca2+ channel (IT) (Hernandex-Cruz and Pape 1989).
LPN neurons (54/55) also displayed a hyperpolarization-activated
depolarization. As shown in Fig. 3,
A and B, hyperpolarizing current pulses produced
a strong inward rectifying response. This "depolarizing sag" was
blocked by bath application of Cs+ (n = 3), thus
indicating LPN cells possess the mixed cation conductance
IH (McCormick and Pape
1990).
Many LPN neurons (33/47) showed a substantial delay in action potential
firing in response to a depolarizing current step
(Fig. 3, C–F).
These delays were voltage dependent and brought about by an outward
rectification during strong membrane depolarization.
Figure 3E shows the
latency (L) in firing varied with the intensity of injected current and could
be fitted to an exponential decay curve (r = 0.93). These delays in
firing were abolished by the local application of 4-AP (n = 4;
Fig. 3F), suggesting
they are mediated by the transient K+ conductance,
IA (McCormick
1991).
Repetitive firing properties of LPN cells
LPN cells exhibited some repetitive firing properties that were distinct from first-order relay neurons. Examples of the firing patterns of LPN neurons are shown in Fig. 4. One group of cells (n = 71) responded to depolarizing current pulses with a steady train of action potentials and a firing frequency that varied linearly with membrane depolarization (Fig. 4A). We refer to this form of firing as a "regular spiking" (RS) mode. Firing frequency by current injection plots for RS cells have relatively steep slopes and a large linear operating range (Fig. 4C). These features can in part be attributed to the lack of spike frequency adaptation in their spike trains. Figure 4E shows the interspike intervals for RS cells remained relatively constant with the passage of each spike in a train at different levels of membrane depolarization.
Another group of LPN cells (n = 23) exhibited what we refer to as
a "clustered spiking" (CS) firing mode in which depolarizing
current pulses evoked epochs of high-frequency spike discharges
(Fig. 4B). These
intermittent clustered discharges were separate and distinct from those that
ride the peak of LT Ca2+ spikes
(Fig. 5, A and
B), and the firing rates of these clusters (
100 Hz)
were lower than the firing frequency of bursts associated with LT
Ca2+ spikes (400 Hz). Firing-frequency plots reveal
that CS cells responded in a nonlinear manner with firing rates that increased
either quadratically (Fig.
4D) or exponentially (not shown) with membrane
depolarization. This increase in firing rates resulted from an increase in the
number of clusters and/or an increase in the number of spikes within a
cluster. As illustrated in Fig.
4F, CS cells displayed a form of spike-frequency
adaptation. Although the firing frequency within the first cluster remained
relatively constant, there was an increase in the interspike interval of
subsequent clusters.
When hyperpolarized to levels more negative than –65mV, depolarizing current pulses evoked LT bursts in both RS and CS cells (Fig. 5, A and B). However, when larger (sustained) current pulses were applied to hyperpolarized RS and CS cells, their responses were distinct. In this situation, LT bursts were followed by RS or CS firing respectively (Fig. 5, C and D).
We noted two measures that were correlated with the different firing modes. First, the half-width of the action potential (duration measured at half-amplitude) was greater for CS cells (mean: 1.21 ms) than for RS cells (mean: 0.73 ms). Second, the afterhyperpolarization potential (AHP) duration for RS cells (mean: 56.72 ms) was greater than that of CS cells (mean: 15.74 ms). These differences are illustrated in Fig. 6, which plots the duration of AHPs against the half-width of action potentials for RS and CS cells.
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Further examination of the AHPs of RS and CS cells revealed heterogeneity
that could be distinguished in part by their duration and underlying
pharmacology. As illustrated in Fig. 7,
A–D,, RS cells showed the most variable AHPs. Some
RS neurons displayed a very slow AHP (Fig.
7, A–C), lasting 87.0 ± 21.2 ms (n
= 13), which corresponds to previous descriptions of a medium AHP (mAHP)
(Sah 1996;
Stocker et al. 1999). AHPs of
this length have not been reported in LGN relay neurons
(Deschênes et al. 1984;
Williams et al., 1996). As
illustrated in Fig. 7, B and
C, the AHP of some RS neurons appeared to have fast and
slow components that were separated by a small afterdepolarization. For other
RS cells, we observed a single AHP of more intermediate length (iAHP,
Fig. 7D) which lasted
38.0 ± 11.6 ms (n = 21). As indicated in
Table 1 and
Fig. 7E, CS cells had
the fastest AHP (fAHP) we observed that lasted 15.7 ± 4.9 ms
(n = 15).
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We investigated the conductances underlying these AHPs by applying various K+ channel antagonists. The results of these experiments are summarized in Fig. 7, F–H. The nonspecific K+ channel blocker, TEA significantly reduced (P < 0.001) the amplitude of the fAHP (Fig. 6F, 10.0 ± 1.7 to 7.3 ± 2.3 mV, a 27% reduction, n = 4). TEA also widened the action potential (half-width from 1.0 ± 0.2 to 2.5 ± 2.1 ms, n = 4, P < 0.001). Another nonspecific K+ channel blocker, 4-AP, was more effective in reducing the amplitude of the fAHP (8.2 ± 2.9 to 4.2 ± 1.8 mV, a 49% reduction, n = 5, P < 0.001) and did not affect action potential width (Fig. 7G). Finally, the small-conductance calcium-activated K+ channel blocker, apamin, reduced the amplitude and duration of the mAHP (111 ± 24 to 59 ± 13 ms, n = 3, P < 0.001) while leaving the width of the action potential and the amplitude of the fAHP intact (Fig. 7H). These results suggest that the variety in the duration of the AHPs recorded in LPN neurons can be attributed to the presence of several different potassium channels.
Distribution and morphology of recorded LPN neurons
We then examined the firing characteristics of LPN neurons in relation to
their location in LPN. In the rodent LPN, rostral regions receive input from
the cortex and caudal regions receive input from the superior colliculus
(Li and Bickford 2001;
Li et al. 2003;
Mason and Groos 1981;
Takahashi 1985). In
experiments carried out in coronal slices, we noted that RS cells tended to be
located in more caudal levels of the LPN, whereas CS cells seemed to be
located in more rostral regions. However, this trend was difficult to quantify
in brains cut in the coronal plane. To confirm that RS and CS cells are
segregated in the LPN, we did experiments in slices cut in the parasaggittal
plane. A typical experiment is illustrated in
Fig. 8. We found that CS cells
were located exclusively in the rostral LPN
(Fig. 8, red symbols), whereas
RS cells were dispersed throughout the rostrocaudal extent of the LPN
(Fig. 8, yellow and green
symbols). On closer examination, we found that cells firing in the RS mode
could be further subdivided by correlating their rostral-caudal location with
the duration of their AHPs. RS cells with a medium AHP (>60 ms;
RSm, n = 32) were located only in the caudal LPN
(Fig. 8, green symbols), while
RS cells with an intermediate AHP (<60 ms; RSi, n = 39)
were more dispersed throughout the LPN
(Fig. 8, yellow symbols).
With cells divided into three categories, we re-examined their membrane
properties and these are summarized in
Table 1. The AHPs for
RSi, RSm, and CS cells differed significantly from each
other (t-test, P < 0.001). The half-width of the action
potential also differed between both groups of RS cells and CS cells
(t-test, P < 0.001). However, there were no significant
differences in the resting membrane potential, input resistance, or amplitude
of action potentials among any of the groups. Moreover, all cells exhibited
IT and IH and the majority of cells
within each group displayed IA (54–79%, see
Table 1 and
Fig. 3, C and
E). We also failed to detect any consistent correlation
between the firing characteristics and morphology of LPN neurons.
Figure 8 provides examples of
camera lucida drawings of a biocytin filled CS
(Fig. 8A),
RSi (Fig.
8B), and RSm
(Fig. 8C) cell. While
there is an inherent variability in dendritic morphology among these cells,
they are indistinguishable from class A thalamocortical relay cells
(Grossman et al. 1973).
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DISCUSSION |
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). It
has previously been shown that the synaptic targets of TRN terminals are
similar in first- and higher-order nuclei
(Wang et al. 2001). These
results taken together with the present report suggest that higher-order
thalamic relay neurons can engage in rhythmic events similar to those
described in first-order nuclei, and thus contribute to the widespread
distribution of thalamic oscillatory activity.
Despite these similarities, we did note that the repetitive firing
characteristics of higher-order LPN relay neurons differed from first-order
LGN relay neurons. We found that cells in the LPN fired linearly in a RS mode
or nonlinearly with epochs of high-frequency bursts in a CS mode. The bursting
associated with the CS mode differs from the conventional LT
Ca2+ mediated burst mode of thalamic relay neurons.
While both forms of bursting are highly nonlinear, their temporal patterning
and voltage dependency differ substantially
(McCormick and Feeser
1990).
The RS mode of LPN relay neurons also differs from the tonic mode of LGN
neurons. Firing frequency by current injection plots for regular spiking cells
are steeper and exhibit a much larger linear operating range
(McCormick and Feeser 1990;
Zhan et al. 1999). The tonic
firing of LGN neurons also shows substantial spike frequency adaptation
(Smith et al. 2001;
Zhan et al. 1999), a feature
that was not apparent in the regular spiking of LPN neurons. These differences
may be attributed to the relative strength and density of various
K+ conductances involved in the regulation of the f- and mAHPs of
thalamic relay cells.
Previous studies have noted that LGN interneurons display longer AHPs than
LGN relay cells (Williams et al.
1996). The AHPs of interneurons are similar in some ways to the
AHPs of the RS cells. However, in the LPN we did not observe the slow voltage
ramp that occurs prior to the start of each action potential. In addition, the
duration of action potentials for LPN cells was greater than those of
interneurons. Similarly, the responses of LPN CS cells are reminiscent of the
responses of "fast spiking" cortical interneurons (Kawaguichi
1995; McCormick et al. 1985).
However, the width of the action potentials of CS cells is wider than that of
parvalbumin-containing fast-spiking interneurons
(Galarreta and Hestrin 2002)
and no neurons in the LPN stain for parvalbumin (see
Fig. 1).
The response profile of CS cells in the rodent LPN more closely resembles
the firing mode of relay cells in the dorsolateral nucleus of the avian
thalamus (Luo and Perkel
2002). In addition, responses similar to CS LPN neurons have been
recorded in relay cells located within the shell region of the cat
ventroposterior lateral nucleus (VPL)
(Turner et al. 1997). Because
responses similar to CS cells have not been recorded in well-characterized
first-order thalamic nuclei such as the rat LGN
(Crunelli et al. 1987;
Williams et al. 1996) or
ventrobasal complex (Velazquez and Carlen
1996), it raises the possibility that the rat LPN and the shell
region of the cat VPL share properties distinct from first order nuclei. Some
areas of the primate VPL are innervated by two types of cortical terminals
(Darian-Smith et al. 1999) and
thus might be considered higher order
(Guillery 1995). However, this
information is unavailable for the cat VPL. At this point, we can confidently
state that within the rat visual thalamus, the firing properties of
higher-order relay neurons are distinct from those of first-order relay
neurons. Whether this distinction will hold true for thalamic nuclei
representing other sensory modalities, or indeed whether the
first-order/higher-order distinction applies to all thalamic regions, requires
further investigation.
We are also confident that the LPN cell responses that we observed were
recorded from relay cells rather than interneurons. First, all of our
biocytin-filled cells were larger than GABAergic interneurons. Second, their
dendritic morphology was consistent with that of first order thalamocortical
cells. Finally, we previously noted that GABAergic interneurons in the LPN are
much sparser than in the LGN, and are virtually absent in the rostral LPN
(Li et al. 2003).
This lack of interneurons in the rostral LPN is worth noting because this
is the region where CS cells are concentrated. The rostral LPN also receives
dense input from the visual cortex (Li et
al. 2003; Mason and Groos
1981; Takahashi
1985). This includes inputs from cortical layer V cells that do
not project to first-order thalamic nuclei but do provide large
"driver-like" inputs to higher-order nuclei
(Guillery and Sherman 2002)
such as the LPN (Bourassa and
Deschênes 1995; Li et
al. 2003). Higher-order nuclei of the visual thalamus project
densely to cortical layer I (Abramson and
Chalupa 1985), where the apical dendrites of layer V cells end in
tufts (Klein et al. 1986).
Thus the high-frequency bursts of CS cells could be particularly effective in
activating layer V cells (Swadlow and
Gusev 2001; Thomson
2000). It is possible that the response characteristics of CS
cells are important for strengthening and maintaining cortico-thalamo-cortical
signals through the rostral LPN.
In contrast, RS cells are located in more caudal levels of the LPN. In
particular, RS cells with the slowest AHPs (RSm cells) are
clustered in the most caudal LPN. This region of the LPN receives input from
the retinorecipient zones of the superior colliculus
(Li and Bickford 2001;
Mason and Groos 1981;
Takahashi 1985). In fact, the
firing characteristics of RSm cells are similar to the firing
characteristics of tectothalamic cells (Lo
et al. 1998). Such firing may be important for the accurate
transfer of these signals through the caudal LPN to the cortex and/or striatum
(Takada 1992). Thus in the
LPN, RS and CS cells may be driven by subcortical and cortical inputs,
respectively, and the distinct temporal properties of their response modes may
be a necessary component of circuits that are unique to higher-order
nuclei.
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ACKNOWLEDGMENTS |
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This work was supported by National Institutes of Health Grants NS-35377 to M. Bickford and EY-012716 to W. Guido and by Sigma Xi to J. Li.
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FOOTNOTES |
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Address for reprint requests: W. Guido, Dept. of Cell Biology and Anatomy, 1901 Perdido St., New Orleans LA 70461 (E-mail: wguido{at}lsuhsc.edu).
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