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The Journal of Neuroscience, 2002, 22:RC197:1-5
RAPID COMMUNICATION
Hippocampal Pyramidal Cell-Interneuron Spike Transmission Is
Frequency Dependent and Responsible for Place Modulation of Interneuron
Discharge
Lisa
Marshall,
Darrell A.
Henze,
Hajime
Hirase,
Xavier
Leinekugel,
George
Dragoi, and
György
Buzsáki
Center for Molecular and Behavioral Neuroscience, Rutgers, The
State University of New Jersey, Newark, New Jersey 07102
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ABSTRACT |
The interplay between principal cells and interneurons plays an
important role in timing the activity of individual cells. We
investigated the influence of single hippocampal CA1 pyramidal cells on
putative interneurons. The activity of CA1 pyramidal cells was
controlled intracellularly by current injection, and the activity of
neighboring interneurons was recorded extracellularly in the
urethane-anesthetized rat. Spike transmission probability between
monosynaptically connected pyramidal cell-interneuron pairs was
frequency dependent and highest between 5 and 25 Hz. In the awake
animal, interneurons were found that had place-modulated firing rates,
with place maps similar to their presynaptic pyramidal neuron. Thus,
single pyramidal neurons can effectively determine the firing patterns
of their interneuron targets.
Key words:
hippocampus; spike transmission; interneuron; depression; place cells; temporal coding
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INTRODUCTION |
Hippocampal
interneurons are suggested to play an essential role in timing the
occurrence of pyramidal cell activity by imposing a coordinated
oscillatory "context" for the "content" carried by networks of
principal cells (Buzsáki and Chrobak, 1995 ; Cobb et al., 1995;
Whittington et al., 1995; Freund and Buzsáki, 1996; Geiger et
al., 1997; Fricker and Miles, 2000). In addition to such a global role,
interneurons may play a critical role in sculpting the activity of
their local network. A single interneuron is estimated to contact
several hundred pyramidal cells (Sik et al., 1995). In the opposite
direction, interneurons are under the control of both local and distal
afferent excitation, but the relative impact of the various inputs to
interneurons is less investigated. Both in vitro and
in vivo studies suggest that the pyramidal cell-interneuron synapse is particularly efficient (Miles 1990; Gulyas et al., 1993;
Csicsvari et al., 1998; Cohen and Miles, 2000). Recently, extracellular
recordings in behaving rats revealed a high spike transmission
probability between pyramidal cells and putative basket cells in the
CA1 pyramidal layer, using a cross-correlation analysis. These
observations suggested that even a single CA1 pyramidal cell can exert
an impact on network activity by way of its target interneurons.
However, in the study of Csicsvari et al. (1998), it could not be ruled
out that some unrecorded presynaptic pyramidal cells also contributed
to the short-latency discharge of the recorded postsynaptic
interneuron. Therefore, in the present study we investigated the
probability of spike transmission in pyramidal cell-interneuron pairs
by controlling spike occurrence of pyramidal neurons with intracellular
current injection. After finding that an individual CA1 pyramidal cell can monosynaptically discharge a neighboring interneuron, we addressed the issue of whether behavioral correlates of the pyramidal cell (O'Keefe and Nadel, 1978) are also reflected in the firing patterns of
its postsynaptic interneuron.
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MATERIALS AND METHODS |
Acute experiments. Forty-five male rats
(350-450 gm) of the strain Sprague Dawley were anesthetized with
urethane (1.5 gm/kg) and placed in a stereotaxic apparatus for surgery
and recording. Constant body temperature was maintained by an animal
heat pad. Paired extracellular and intracellular recordings were
obtained by the procedure described by Henze et al. (2000). In brief,
extracellular and intracellular electrodes were mounted on manipulators
of a stereotaxic apparatus (Kopf Instruments, Tujunga, CA). The
manipulator of the extracellular tetrode (Gray et al., 1995) was
mounted at a 10° angle from the vertical plane (Henze et al., 2000).
Guided by unit activity and evoked field potentials, the extracellular electrode was lowered into the CA1 region of the hippocampus until a
putative interneuron was recorded in or close to stratum pyramidale. On-line criteria for determining the occurrence of an interneuron unit
were the duration of the extracellular spikes (<0.8 msec), wave shape,
and firing rate (Csicsvari et al., 1998). For the off-line isolation of
interneuron spikes, a semi-automatic clustering procedure was used
(Harris et al., 2000). Once stable extracellular recording was
obtained, an intracellular sharp pipette, containing a 1 M potassium acetate solution, was lowered into
the pyramidal layer <100 µm from the recorded interneuron. After the
microelectrode was lowered, the skull hole was filled with a paraffin mixture.
Intracellular signals were recorded using an Axoclamp-2A (Axon
Instruments, Foster City, CA) under conditions of spontaneous activity
or by intracellular current injection. Current injection occurred
either as long depolarizing pulses of 40-500 msec duration (0.2-1.2
nA) or as a train of 10 short 4 msec steps. Monosynaptic pyramidal-interneuron pair connections could be observed on-line by
superimposition of extracellular putative interneuron unit activity
time-locked to the intracellular action potential (see Fig.
1B). The putative connection was verified by a
significant cross-correlation between the peak time of the pyramidal
cell action potential and negative peak of the unit activity of the putative interneuron. Cross-correlation histograms were expressed as
probability by dividing each bin by the number of reference events
(i.e., the occurrence of pyramidal cell spikes). A second, shuffled
cross-correlation histogram calculated by shifting the spike train of
the putative interneuron discharge times was subtracted from the
original to reduce the effect of random interactions. Bin values above
3 SDs from the baseline of the derived histograms were regarded as
significant (p = 0.0013; assuming normal
distribution). Probability of spike transmission was estimated as the
maximum count within 1-3 msec of the corrected cross-correlogram
(Csicsvari et al., 1998). When trains of spikes were evoked by short
current steps at defined frequencies, spike transmission probability
was calculated for all presynaptic spikes in the evoked trains after excluding the first spike. For long current steps, spike transmission probability was calculated separately for each spike position to assess
an effect on spike order.
Chronic studies. Twelve male rats of the
Long-Evans strain (300-500 gm) were implanted with eight individually
movable tetrodes. The tetrodes were inserted into the CA1 pyramidal
layer with 300 µm center spacings. The rats were tested either in a
running wheel task (Czurkó et al., 1999) or in a large
rectangular plywood box (1.2 × 1.2 × 0.5 m high) with
various objects (Hirase et al., 2001a). An infrared light-emitting
diode was attached to the head stage to track the position of the
animal (Czurkó et al., 1999). After amplification (10,000×) and
band-pass filtering (1 Hz-5 kHz), field potentials and extracellular
action potentials were digitized continuously at 20 kHz rate with a
DataMax system (16 bit resolution; RC Electronics, Santa Barbara, CA).
Interneurons and pyramidal cells were separated by a semi-automatic
clustering procedure (Harris et al., 2000). Monosynaptic connections
between pyramidal cell-interneuron pairs were quantified as described above. After completion of the experiments the rats were deeply anesthetized and perfused. The brains were sectioned and stained with
the cresyl violet method to verify electrode placements.
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RESULTS |
A single CA1 pyramidal cell can reliably drive its
target interneuron
By appropriate positioning of the extracellular and intracellular
recording electrodes in the CA1 pyramidal layer, monosynaptically connected pyramidal cell-interneuron pairs could be identified. Previous experiments indicated that the probability of such pairs is
much higher within a radius of 150 µm than at longer distances (Csicsvari et al., 1998; Cohen and Miles, 2000). In 26 of 45 experiments the intracellular and extracellular electrodes were
positioned <150 µm. In a portion of these experiments
(n = 12), an interneuron was recorded by the
extracellular electrode (Fig.
1A), in addition to
other pyramidal cells. Once the presence of the interneuron was
established, repeated attempts were made to impale a presynaptic pyramidal cell. Current- or injury-induced discharge of the pyramidal cell often drove the interneuron within <3 msec. When several pyramidal cells were impaled in succession, typically only one or none
could drive the interneuron, indicating that only a portion of the
nearby pyramidal cells innervated the same interneuron. In four
experiments, pyramidal cell-interneuron pairs were recorded for >30
min and with clearly separable interneuron spikes (see Materials and
Methods). These recordings provided a sufficient number of action
potentials to quantitatively evaluate spike transmission probability
from the presynaptic pyramidal cell to the postsynaptic interneuron in
several conditions (Fig. 1). Spike transmission probabilities ranged
between 0.02 and 0.4 (0.18 ± 0.03; mean ± SE) and were
similar for spontaneously occurring and current step-evoked spikes
(Fig. 1C). The mean latency between the peaks of the
intracellular action potential and the extracellular interneuron spike
was 1.54 msec (±0.82 msec).
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Figure 1.
Schematized recording procedure.
A, A tetrode for extracellular recording was inserted
into the CA1 pyramidal cell layer at an angle to record putative
interneuron(s). A sharp glass micropipette impaled a pyramidal cell
<100 µm from the interneuron. The intracellularly recorded pyramidal
cell was later revealed by biocytin staining (A).
B, Superimposed traces of the activity of a putative
interneuron (int; 800 Hz-3 kHz) and intracellularly
recorded pyramidal cell. Insets, Spike distribution of
the interneuron at high temporal resolution (0.1 msec). Note
short-latency (<2 msec) discharge of the interneuron by the
presynaptic pyramidal cell. C, Cross-correlation between
the pyramidal cell spikes (reference event) and interneuron spikes.
Spikes from the two cells were shuffled, and the shuffled values were
subtracted from the original histograms. Dotted lines
indicate 3 SDs of the mean (p < 0.002).
Note similar spike transmission probability for spikes that occurred
spontaneously in the pyramidal cell or were evoked by intracellular
current injection. D, Dependence of spike transmission
on the frequency of the presynaptic pyramidal cell spikes.  ,
Spontaneously occurring spikes;  , spikes induced by short
current steps (4 msec) at various frequencies. Spike transmission
probability was calculated for all presynaptic spikes in the evoked
trains, excluding the first spike. Note the highest spike transmission
probability at 10 Hz.
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The anatomical identity of the monosynaptically driven neurons could
not be revealed with extracellular recordings. It is known, however,
that interneurons with cell bodies in the pyramidal layer correspond to
basket cells, chandelier cells, and bistratified interneurons (Freund
and Buzsáki, 1996). In vitro experiments indicated
that the pyramidal cell synapses on these interneurons show
paired-pulse depression (Ali et al., 1998). Therefore, we investigated
the short-term use-dependent effects on spike transmission probability.
In the first test, bursts of spikes were evoked in the pyramidal cell
by long depolarizing pulses of 40-500 msec duration (Fig.
2A,B).
The pyramidal cell responded to these prolonged steps with a train of
accommodating spikes, with the largest depression of spike transmission
probability between the first and second spike (Fig.
2C,D). This suggested that either the high
frequency of the spikes (mean interval, 10.5 ± 2.22 msec) or
something more general about the second spike was responsible for the
depression. Therefore, we examined spike transmission probability
specifically as a function of the frequency of the presynaptic spikes
(n = 2 pairs). In this test, action potentials were
evoked by trains of 10 step pulses of 4 msec (one spike per step) at
various frequencies. In both neuron pairs tested, we found that the
highest probability of spike transmission occurred between 5 and 25 Hz,
with relatively low probabilities above 40 Hz or below 3 Hz (Fig.
1D). These findings indicated that the firing
patterns of the presynaptic pyramidal cell can affect the efficacy of
synaptic transmission between the pyramidal cell and interneuron.
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Figure 2.
Suppression of monosynaptic pyramidal-interneuron
spike transmission probability. A, Relationship between
long current step-induced action potentials in the pyramidal cell and
interneuron spikes. Wide band (1 Hz-3 kHz) and bandpass-filtered traces
of the extracellular traces are shown. Interneuron spikes occurred <2
msec after the first, third, and fourth pyramidal cell spikes, shown in
detail in B. C, Changes in spike
transmission probability from the 1st to 12th spike position for the
neuron pair shown in A and B. Spike
transmission probability was calculated separately for the 1st through
12th presynaptic spike. D, Average of three neuron
pairs. The mean instantaneous firing frequency of the second spike
ranged between 80 and 120 Hz for the different pyramidal cells and was
lower for subsequent spikes.
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"Place" correlates of interneurons are secondary to pyramidal
cell activity
Previous studies have shown that in addition to pyramidal cells,
interneurons can also display a reliable spatial distribution of their
spikes. However, in contrast to pyramidal cells (place cells), the
place fields of interneurons are typically large, sometimes with
multiple centers (McNaughton et al., 1983; Kubie et al., 1990). In
agreement with these previous reports, we found a significant
place-related increase of firing rates in 12 of 26 CA1 interneurons.
The field sizes represented by interneurons were several times larger
than those of the pyramidal cells. Because of the high spike
transmission probability between some pyramidal cell-interneuron pairs
and the behavior dependence of the efficacy of the synaptic
transmission (Csicsvari et al., 1998), we hypothesized that place
correlates of interneurons are brought about by the activity of their
presynaptic place cells. Three of the 12 interneurons with place
correlates were postsynaptic to a simultaneously recorded place cell.
An example is shown in Figure 3. In this
experiment two pyramidal cells, recorded from the same tetrode, had
adjacent place correlates (P1, P2). One of the
place cells was monosynaptically connected to a simultaneously recorded
interneuron, as shown by the sharp short-latency (<3 msec) peak in the
cross-correlograms (Fig. 3A). Although the interneuron had
multiple place fields, one of its place correlates was identical with
the place field of its presynaptic pyramidal cell (Fig. 3B).
The spatial extent of the field represented by the interneuron was
somewhat larger than that of its presynaptic place cell. However, the
peak firing of the interneuron and pyramidal cell coincided. Spatial
overlap of the peak firing of monosynaptically connected place
cell-interneuron pairs was similar in the remaining two cases in which
interneurons possessed place correlates.
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Figure 3.
Spatial correlates of interneurons are
attributable to their monosynaptic activation by presynaptic place
cells. A, Autocorrelograms of two neighboring place
cells (P1 and P2; blue and
green, respectively) and an interneuron
(int; red) and their respective
cross-correlograms (orange, light blue).
The large peak at  2 msec (arrow) indicates
monosynaptic connection between P1 and the interneuron.
B, Color-coded firing rate place maps of the three
neurons shown in A in a larger square
box. The rectangular box is added to highlight
the place fields of P1 and P2. Note
similar spatial discharge of the interneuron and its presynaptic
pyramidal cell (P1; i.e., right,
bottom corner of rectangle).
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DISCUSSION |
The present study examined the impact of presynaptic activity of
CA1 pyramidal cells on their postsynaptic interneuron targets. We found
that a single presynaptic pyramidal cell alone can discharge a putative
postsynaptic interneuron. The high spike transmission probability
between pyramidal cell-interneuron pairs was expressed at the
behavioral level by the similar place-related firing of the interneuron
and the presynaptic pyramidal cell.
Our findings confirm and extend previous in vitro studies
demonstrating the high reliability of synaptic transmission between principal cells and interneurons (Gulyas et al., 1993; Geiger et al.,
1997; Ali et al., 1998; Fricker and Miles, 2000; Galarreta and Hestrin,
2001). Although principal cells contact basket cells and other
interneurons typically by a single release site, transmission failures
are rare (Gulyas et al., 1993). In the awake rat, presynaptic spikes in
pyramidal cells often resulted in a monosynaptic discharge of target
interneurons (Csicsvari et al., 1998). However, in that study the
contribution of other simultaneously active cells could not be
excluded. In the present study, intracellular stimulation of a single
pyramidal cell reliably discharged the target interneuron. The
discharge probability of the postsynaptic neuron in response to
spontaneously occurring presynaptic spikes and current-induced spikes
was comparable. In addition, the postsynaptic spikes showed very little
time jitter. Therefore, these findings conclusively demonstrate that
single pyramidal cells can discharge postsynaptic interneurons with
high reliability in the intact brain. It should be noted here that the
spike transmission probability method may underestimate the number of
pyramidal-interneuron connections because pairs with low spike
transmission probabilities would be classified as nonconnected. Thus,
the variability of spike transmission from pyramidal to interneurons
can be quite large.
The identity of our extracellularly recorded interneurons remains to be
elucidated. Because the recorded cell bodies were encountered in the
pyramidal cell layer, they may represent basket cells, chandelier
cells, or a subgroup of bistratified interneurons (Freund and Buzsaki,
1996). Glutamatergic synapses onto neurons in these classes have been
shown to display use-dependent modulation. We also observed a robust
depression in spike transmission mainly from the first to the second
presynaptic spike, similar to recordings from pyramidal
cell-interneuron pairs in the slice preparation (Ali et al., 1998).
The observation that higher frequencies (>25 Hz) of presynaptic
activity are not as efficient as lower frequencies at driving
interneurons is likely to be the reason for the robust depression of
spike transmission from the first to the second spikes in a
step-induced burst. The depression of spike transmission at higher
frequencies is consistent with previous in vitro studies examining synaptic transmission (Thomson and Bannister, 1999; Waldeck
et al., 2000). However, additional factors may also be involved (Manor
et al., 1997; Borst and Sakmann, 1999; Frerking et al., 2001) because
the efficacy of pyramidal cell-interneuron spike transmission was
highest in the 5-25 Hz range and decreased again at lower frequencies.
Thus, spike transmission is not a simple function of interspike
interval, but each synapse may have some preferred frequency range
[frequency filtering (Markram et al., 1998)].
The frequency tunability of the pyramidal cell-interneuron synapse may
be an efficient mechanism to temporarily redistribute communication in
active neuronal ensembles (Abbott et al., 1997; Tsodyks et al., 2000).
In the hippocampus, such active groups may correspond to place cell
assemblies (Wilson and McNaughton, 1993). The frequency of place cells
corresponds to the range in which the pyramidal cell-interneuron spike
transmission probability was highest (5-25 Hz). Thus, an active place
cell can enhance its access to its target interneurons through
frequency-tuned synapses, compared with other presynaptic pyramidal
cells that discharge at a low frequency. This hypothesis can help
explain the previous (McNaughton et al., 1983; Kubie et al., 1990) and present observations that the firing rates of several interneurons were
not distributed homogenously over the visited places. Our finding that
the peak firing rates of some interneurons coincided with the place
field of the presynaptic pyramidal cell provides support for such a
mechanism. Although hundreds of pyramidal cells are presynaptic to a
single interneuron, only a small portion is active at any one time
(Harris et al., 2000). Furthermore, place cells, representing the same
part of the environment, are not clustered but are randomly distributed
in the CA1 pyramidal layer (Redish et al., 2001). Importantly, most
presynaptic partners of interneurons are local (Csicsvari et al., 1998;
Hirase et al., 2001b). Therefore, if pyramidal cells in the vicinity of
the recording electrode do not cover the explored area homogeneously,
this inhomogeneity will be reflected by the activity of their target interneuron(s).
It has been reported that timing of spikes within the theta cycle
varies systematically as the rat traverses the place field of the
recorded pyramidal cell (O'Keefe and Recce, 1993). This "phase
precession" has important implications in the nature of neuronal
coding (Jensen and Lisman, 1996; Skaggs et al., 1996; Tsodyks et al.,
1996; Wallenstein and Hasselmo, 1997). The present findings suggest
that phase advancement may not be unique to principal cells. Some
interneurons, strongly coupled to their presynaptic pyramidal neuron,
may undergo the same degree of theta phase precession as their master
place cell. The implication of this prediction is that a subset of
neurons can coherently "step out" from the population and form an
assembly different in both discharge rate and timing from the remaining population.
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FOOTNOTES |
Received July 10, 2001; revised Oct. 12, 2001; accepted Oct. 16, 2001.
This work was supported by the Deutsche Forschungsgemeinschaft (LM/
2053/2) and National Institutes of Health (54671; 34994; P41-RR09754; 2403). We thank E. Borok for her skillful technical assistance.
Correspondence should be addressed to György Buzsáki,
Center for Molecular and Behavioral Neuroscience, Rutgers University, 197 University Avenue, Newark, NJ 07102. E-mail:
buzsaki{at}axon.rutgers.edu.
L. Marshall's present address: Medical University Lübeck,
Clinical Research Group, H23a Ratzeburger Allee 160, 23538, Lübeck, Germany.
This article is published in
The Journal of Neuroscience, Rapid Communications Section,
which publishes brief, peer-reviewed papers online, not in print. Rapid
Communications are posted online approximately one month earlier than
they would appear if printed. They are listed in the Table of Contents
of the next open issue of JNeurosci. Cite this article as:
JNeurosci, 2002, 22:RC197 (1-5). The
publication date is the date of posting online at
www.jneurosci.org.
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ABSTRACT
INTRODUCTION
