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The Journal of Neuroscience, July 15, 2000, 20(14):5300-5311
Columnar Organization of Dendrites and Axons of Single and
Synaptically Coupled Excitatory Spiny Neurons in Layer 4 of the Rat
Barrel Cortex
Joachim
Lübke1,
Veronica
Egger2,
Bert
Sakmann2, and
Dirk
Feldmeyer2
1 Anatomisches Institut I,
Albert-Ludwigs-Universität Freiburg, D-79104 Freiburg, Germany,
and 2 Max-Planck-Institut für Medizinische Forschung,
Abteilung Zellphysiologie, D-69120 Heidelberg, Germany
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ABSTRACT |
Cortical columns are the functional units of the neocortex that are
particularly prominent in the "barrel" field of the somatosensory cortex. Here we describe the morphology of two classes of synaptically coupled excitatory neurons in layer 4 of the barrel cortex, spiny stellate, and star pyramidal cells, respectively. Within a single barrel, their somata tend to be organized in clusters. The dendritic arbors are largely confined to layer 4, except for the distal part of
the apical dendrite of star pyramidal neurons that extends into layer
2/3. In contrast, the axon of both types of neurons spans the cortex
from layer 1 to layer 6. The most prominent axonal projections are
those to layers 4 and 2/3 where they are largely restricted to a single
cortical column. In layers 5 and 6, a small fraction of axon
collaterals projects also across cortical columns. Consistent with the
dense axonal projection to layers 4 and 2/3, the total number and
density of boutons per unit axonal length was also highest there.
Electron microscopy combined with GABA postimmunogold labeling revealed
that most (>90%) of the synaptic contacts were established on
dendritic spines and shafts of excitatory neurons in layers 4 and
2/3.
The largely columnar organization of dendrites and axons of both cell
types, combined with the preferential and dense projections within
cortical layers 4 and 2/3, suggests that spiny stellate and star
pyramidal neurons of layer 4 serve to amplify thalamic input and relay
excitation vertically within a single cortical column.
Key words:
barrel cortex; layer 4; spiny stellate cell; star
pyramidal neuron; cortical column; axonal projection; paired
recordings; intracellular labeling
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INTRODUCTION |
Sensory cortices display a
distinctive organization into functional modules of neuronal ensembles,
the so-called cortical columns that process signals from the periphery
(Mountcastle, 1957 ; Mountcastle and Powell, 1959; Hubel and Wiesel,
1962; for review, see Mountcastle, 1997; Rockland, 1998). One striking
example of such a modular organization is the "barrel" field in the
somatosensory cortex of rodents. In layer 4 of the barrel cortex, each
whisker hair on the animal's muzzle is topographically represented in a one-to-one relationship (Woolsey and van der Loos, 1970; Welker, 1976; for review, see Juliano and Jacobs, 1995).
In sensory cortices, layer 4 is the main input region for afferent
fibers originating in the respective thalamic relay nuclei (Hubel and
Wiesel, 1962; McGuire et al., 1984; Chiaia et al., 1991a,b; for review,
see Sherman and Guillery, 1996). Although a small fraction (~20%) of
these thalamic afferents terminate on aspinous, presumably GABAergic
interneurons (White and Rock, 1981; White et al., 1984; Benshalom and
White, 1986), their main target cells are excitatory spiny neurons in
layer 4. Most of these neurons resemble spiny stellate cells, whereas a
smaller fraction has been described as star pyramidal cells (Lund,
1984; Ahmed et al., 1994; Hirsch, 1995). Thus, these neurons are the first elements involved in intracortical signal processing (Mountcastle and Powell, 1959; Hubel and Wiesel, 1962; LeVay, 1973; Martin and
Whitteridge, 1984; McGuire et al., 1984; Douglas and Martin, 1991;
Armstrong-James et al., 1992; for review, see McCormick, 1992).
An understanding of the function of spiny neurons in layer 4 in the
microcircuitry of a cortical column requires detailed knowledge about
their anatomical organization, in particular their axonal projections
and their postsynaptic target cells. Earlier Golgi studies described
the dendritic morphology of spiny neurons in rodent barrel cortex
(Pasternak and Woolsey, 1975; Woolsey et al., 1975; Steffen, 1976;
Steffen and van der Loos, 1980; Harris and Woolsey, 1981; Simons and
Woolsey, 1984; for review, see Juliano and Jacobs, 1995) but lacked
information about the axonal projections at the single-cell level and
the target cells of these neurons. However, small extracellular
biocytin deposits revealed that most of the projections are to
supragranular layers, and relatively few direct connections exist
between hollows of neighboring barrels (Kim and Ebner, 1999).
Here we have used dual whole-cell recordings from pairs of neurons
combined with reconstruction of the biocytin-filled neurons to
quantitatively describe the dendritic arborization and in particular the axonal projections and the postsynaptic target structures of
synaptically coupled spiny neurons in layer 4 of rat barrel cortex. We
show that the dendritic arbor is largely confined to a single barrel in
layer 4 and that the axon projects vertically throughout all cortical
layers but remains predominantly within the same cortical column. In
conjunction with the functional properties of these connections
(Feldmeyer et al., 1999b), the largely columnar organization of the
axons suggests that as an ensemble, excitatory spiny neurons in layer 4 serve to amplify thalamic inputs and relay excitation to superficial
laminae within a cortical column. Therefore, spiny layer 4 neurons act
as the principal gate for the signal flow within a cortical column.
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MATERIALS AND METHODS |
Preparation of acute brain slices. All experiments
were performed in accordance with the animal welfare guidelines of the Max-Planck Society and the University of Freiburg. Wistar rats (12-22
d old) were anesthetized with halothane and decapitated, and slices
through the somatosensory cortex were cut in cold extracellular solution using a vibrating microslicer (DTK-1000, Dosaka Co. Ltd., Kyoto, Japan) and prepared according to methods described elsewhere (Agmon and Connors, 1991; Feldmeyer et al., 1999b). Slices (350-400 µm thick) were collected, incubated at 35°C in extracellular
solution for 30-60 min, and subsequently maintained at room
temperature (20-23°C) before electrical recordings were made.
Solutions. Slices were continuously superfused with
extracellular solution containing (in mM): 125 NaCl, 2.5 KCl, 25 glucose, 25 NaHCO3, 1.25 NaH2PO4, 2 CaCl2 and 1 MgCl2 bubbled
with 95% O2 and 5% CO2. The intracellular pipette
solution contained (in mM): 105 K-gluconate, 30 KCl, 10 HEPES, 10 phosphocreatine, 4 ATP-Mg, 0.3 GTP (adjusted to pH 7.3 with
KOH). The osmolarity of this solution was 300 mOsm. For subsequent
morphological analysis, 2-5 mg/ml biocytin (Sigma, München,
Germany) was routinely added to the internal solution, and neurons were
filled during 1-3 hr of recording.
Identification of synaptically connected neurons in layer 4 of
the barrel cortex. Slices of rat somatosensory cortex were placed
in the recording chamber under an upright microscope (Axioskop Carl
Zeiss Göttingen, Germany) fitted with 2.5× plan/0.075 NA and
40×-W/0.80 objectives) with the pial surface pointing to the front and the hippocampus to the right. The barrel field was visualized at low magnification under bright-field illumination and can be identified in layer 4 as evenly spaced dark structures. Barrel structures are present in five to six slices but a continuous band of
barrels is visible only in two to three slices just above the
hippocampus, fimbria-fornix, and lateral ventricle. Individual layer 4 neurons were identified at 40× magnification using
infrared-differential interference contrast (IR-DIC) microscopy as
previously described. The somata of layer 4 neurons in the barrel field
tended to be organized in clusters in the dark edges of a barrel (see
Fig. 1B,C) when compared with the
light centers.
Electrophysiological recordings. Whole-cell voltage
recordings from presynaptic and postsynaptic spiny layer 4 neurons were made as described elsewhere (Feldmeyer et al., 1999b). In brief, a
postsynaptic cell was recorded from with one pipette, and subsequently synaptic connections to this cell were searched with a second pipette
in the loose-patch configuration. When EPSPs in response to the
loose-patch stimulation were detected in the postsynaptic neuron, the
presynaptic cell was repatched with a new pipette filled with
biocytin-containing intracellular solution using the whole-cell
(voltage recording) mode. Potentials were amplified using an EPC9-2
(for dual whole-cell recording; HEKA Elektronik Lambrecht). Recordings
were filtered at 2-5 kHz, digitized at 5-10 kHz using an ITC-16
interface (Instrutech, Great Neck, NY), and stored on the hard disk of
a Macintosh or a PC.
Histological procedures. After recording and loading with
biocytin, brain slices were fixed in 100 mM
phosphate-buffered (PB) solution, pH 7.4, containing 1%
paraformaldehyde and 2.5% glutaraldehyde at 4°C for at least 24 hr.
Endogenous peroxidase was blocked by incubation of the slices in 1%
H2O2 for 15-20 min. After
several rinses in PB solution they were then transferred to a 1%
avidin-biotinylated horseradish peroxidase complex containing 0.1%
Triton X-100 (ABC-Elite Camon, Wiesbaden, Germany) and left overnight
at 4°C while shaking slightly. The next day, slices were reacted
using 3,3-diaminobenzidine (DAB; Sigma) and 0.01%
H2O2 until dendrites and
axonal arbors were clearly visible (after approximately 2-5 min).
Slices were mounted on glass slides, embedded in Moviol (Hoechst AG,
Frankfurt AM, Germany), and coverslipped.
Individual selected spiny stellate (n = 2) and star
pyramidal neurons (n = 1) were processed for electron
microscopic analysis to identify the postsynaptic target structures of
these neurons. After cryoprotection in 10% (20 min) and 20% (30 min)
sucrose, sections were freeze-thawed in liquid nitrogen. After several rinses in PB solution, sections were incubated overnight in ABC solution and reacted as described above. To enhance staining contrast, slices were post-fixed in 0.5% OsO4 (30-45
min), then dehydrated and embedded in Durcupan (Fluka, Deisenhofen,
Germany). Serial ultrathin sections through the entire axonal domain
were cut with an ultramicrotome (Leitz-Ultracut, Hamburg, Germany),
counterstained, and examined with a Philips CM 100 electron microscope
(Philips, Eindhoven, The Netherlands).
GABA postembedding immunogold labeling. The immunogold
staining procedure was performed as described by Somogyi and Hodgson (1985), using a commercially available antiserum against GABA (Sigma).
The immunostaining was performed on droplets of Millipore-filtered solutions in humid Petri dishes. Immersion in 1% periodate (10 min)
was followed by several washes in double-distilled water. Thereafter,
the grids were transferred through 2 or 5% sodium metaperiodate
(10-30 min) and rinsed several times in double-distilled water and
three times in Tris-buffered saline (TBS), pH 7.4. After preincubation
in 1% ovalbumin dissolved in TBS (30 min), the grids were incubated in
rabbit anti-GABA antiserum (1:5000, in 1% normal goat serum in TBS).
After rinsing in TBS and 50 mM Tris buffer, pH 7.4, containing 1% bovine serum and 0.5% Tween 20 (10 min), the
grids were incubated in the secondary antibody (goat anti-rabbit IgG-coated colloidal gold, 10 nm) for 2 hr (diluted 1:10, in darkness). After rinsing in 2% glutaraldehyde (10 min), the grids were washed again in double-distilled water and stained with uranyl acetate and
lead citrate. In control experiments without the primary antibody and
sections processed for GABA postimmunogold labeling, almost no or only
low background labeling was detected, whereas labeling of structures
presumed to be GABAergic exceeded the mean gold particle density of the
maximal background staining by at least four SDs.
Morphological reconstructions of biocytin-filled synaptically
coupled neurons. Biocytin-labeled pairs of synaptically coupled neurons were examined under the light microscope at high magnification. Only pairs for which a complete physiological analysis was made and
that had no obvious truncation of their dendritic and axonal profiles
were used for qualitative and quantitative morphology. Measurements
were not corrected for shrinkage. Representative neuron pairs were
photographed at various magnifications to document dendritic
morphology, axonal projection, and location of synaptic contacts. The
outline of neurons was then drawn with the aid of a camera lucida
attached to an Olympus BX50 microscope (Olympus, Hamburg, Germany) at a
final magnification of 720×. For some pairs of neurons,
three-dimensional reconstructions were also made at 400× magnification
using the Neurolucida (Microbrightfield, Colchester, UK)
software. The reconstructions provided the basis for further quantitative morphological analysis of the following parameters: (1)
maximal horizontal field span of the dendrites and axons, (2) total
number and distribution of putative synaptic contacts per neuron, (3)
total number of boutons in cortical layers 1 to 6, and (4) number of
boutons per 100 µm of axonal segment counted separately for each
cortical layer. For all data, means ± SD were calculated.
Significance was tested using a two-tailed Student's t test.
Cytochrome oxidase histochemistry. To identify the barrel
structure in layer 4 of the somatosensory cortex, the cytochrome oxidase staining according to Wong-Riley (1979) was used on
perfusion-fixed rat brains of the same age (postnatal day 12-15) as
used for the acute slice preparations. In brief, animals were perfused
transcardially with a PB solution containing 4% paraformaldehyde.
Brains were stored overnight in the same fixative at 4°C and then
prepared as described above. After several rinses in PB solution,
free-floating 100-µm-thick vibratome sections through the barrel
field were incubated in a PB solution containing 50 mg DAB, 15-30 mg
cytochrome c, and 20 mg catalase/100 ml at 37°C for 2 hr
in the dark. The reaction was stopped when individual barrels were
clearly distinguishable from the background (see Fig.
1A). After several rinses in PB solution,
sections were mounted on glass slides, air-dried, defatted in absolute
alcohol and xylene, finally embedded in Hyper-Mount (Life Science,
Frankfurt, Germany), and coverslipped. In some experiments, cytochrome
oxidase histochemistry and labeling of single biocytin-filled neurons
(n = 15 neurons) were combined to reveal the dendritic
and axonal organization with respect to the barrel structure (see Fig.
2B, inset, D).
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RESULTS |
Cytochrome oxidase stain of the barrel cortex slices
All experiments were performed on thalamocortical slices in which
the barrel structure in layer 4 is easily recognizable. Figure
1A illustrates the
barrel structure in somatosensory cortex as revealed by cytochrome
oxidase staining that mirrors the bright-field images taken from acute
slice preparations of the barrel cortex. Combined bright-field and
IR-DIC videomicroscopy at low and high magnification, respectively,
showed that the somata of neurons appeared to be organized in
clusters of 5-15 neurons (Fig.
1B,C), with a predominant
location at the edges of individual barrels. In contrast, spiny
stellate neurons in the visual cortex display a more homogeneous
distribution throughout layer 4 (LeVay, 1973; Lund, 1984; Martin and
Whitteridge, 1984, 1988).
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Figure 1.
A, Low magnification of a
semicoronal section through the barrel field (as used for acute slices)
stained for cytochrome oxidase showing the regular distribution of
barrels in layer 4 of the somatosensory cortex. Scale bar, 500 µm.
B, Low magnification IR-DIC contrast image of layer 4 of
the barrel cortex. The box outlined in
black indicates a cluster of spiny layer 4 neurons that
is shown enlarged in C. Scale bar, 200 µm.
C, Higher magnification of a single cluster of spiny
layer 4 neurons. All neurons in the plane of focus are marked by
black asterisks. Scale bar, 10 µm.
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Multiple biocytin labeling of individual neurons in combination with
cytochrome oxidase staining (n = 15 neurons) revealed that almost the entire dendritic and axonal domain of excitatory spiny
neurons in layer 4 was confined to a single cortical column. This was
found for all spiny layer 4 neurons in the barrel field (Fig.
2A,B).
In contrast, layer 5 pyramidal neurons (n = 5) injected right below the barrels showed a completely different morphology, and
their apical dendrites showed no obvious relationship to the barrels as
defined with cytochrome oxidase staining (Fig.
2C,D).
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Figure 2.
A, Barrel cortex slice under
bright-field illumination. The white asterisk marks a
biocytin-labeled spiny stellate cell. B, Camera lucida
reconstruction of the spiny stellate cell marked by the white
asterisk in A. The somatodendritic configuration
is shown in red; the axonal collaterals are shown in
blue. The outline of the barrel is revealed by the
cytochrome oxidase staining and is shaded in light
gray. Inset, Half-tone picture of the
cytochrome oxidase and intracellular biocytin double staining of the
same barrel. Scale bar: 100 µm; inset, 40 µm. C,
Barrel cortex slice under bright-field illumination. The black
asterisks mark the position of the biocytin-labeled pyramidal
neurons shown in D. D, Row of
biocytin-labeled pyramidal neurons in upper layer 5. The somata of
these neurons are located right beneath two adjacent barrels that were
stained with cytochrome oxidase. In contrast to spiny stellate cells,
the somatodendritic configuration of these neurons shows no obvious
relation to the barrel structure. Scale bar, 200 µm.
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Morphology of synaptically coupled spiny layer 4 neurons
Excitatory layer 4 neurons were identified by their shape in
IR-DIC and their "regular" pattern of action potentials after current injection (Connors and Gutnick, 1990; Feldmeyer et al., 1999b).
Spiny layer 4 neurons, i.e., spiny stellate and star pyramidal cells, were easily distinguished by their spherical to ovoid somata and
the absence of a prominent apical dendrite (Fig. 1C). In
addition, their somata appeared to be larger than those of GABAergic
aspiny stellate layer 4 interneurons ( 10 vs  10 µm) but smaller
than that of GABAergic interneurons with fusiform somata (>20 µm). Monosynaptic connections between spiny layer 4 neurons were reliable and characterized by a low coefficient of variation and a low failure
rate of unitary EPSPs (Feldmeyer et al., 1999b).
From the sample of synaptically connected pairs of spiny neurons in
layer 4 (n = 131), ~80% were identified as spiny
stellate neurons and the remainder as star pyramidal neurons. However, often no clear distinction between the two cell types was possible because of the variability in the morphology and length of the apical
dendrite. Representative examples of pairs of coupled spiny stellate
(nine cell pairs) and star pyramidal neurons (two cell pairs) were
selected for further analysis.
Spiny stellate cells
Spiny stellate cell dendrites in the barrel cortex have a
characteristic asymmetric orientation (Figs. 2B,
3A,
4, 5), in
contrast to spiny stellate cells in layer 4 of the visual cortex that
generally display a multipolar, almost radially symmetric dendritic
field (LeVay, 1973; Lund, 1984; Martin and Whitteridge, 1984; 1988; but
see Katz et al., 1989; Kossel et al., 1995). Three to six thick primary
dendrites emerged from the spherical to ovoid somata that gave rise to
several secondary, tertiary, and higher-order dendrites. These
dendrites formed an asymmetric dendritic field of various size
(Table 1) that was confined to a single
barrel and always oriented toward its center (Figs.
2B, 3A, 4). Higher-order dendrites were
densely covered with spines (Fig. 5). Spiny stellate cells that were
synaptically coupled to each other as described here resembled those
designated as class I spiny neurons in the barrel cortex by Woolsey and
coworkers (Pasternak and Woolsey, 1975; Simons and Woolsey, 1984).
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Figure 3.
Low-magnification light microscope image of a
synaptically coupled pair of spiny stellate cells
(A) and star pyramidal neurons
(B) filled with biocytin showing the location,
dendritic configuration, and columnar axonal projection of both
neurons. Note that the characteristic asymmetric dendritic
configuration of spiny stellate cells is confined to layer 4, whereas
the axons of the presynaptic and postsynaptic neuron project throughout
the cortex from layer 1 to the white matter with extensive arborization
in layers 2/3 and 4. In contrast, dendrites of star pyramidal neurons
have no asymmetric distribution. They are largely confined to layer 4, with the exception of the apical dendrites that terminate in middle to
upper layer 2/3. The axons have a projection similar to that of spiny
stellate cell axons but tend to show clustering (black
asterisks) in layer 2/3. Scale bar, 100 µm.
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Figure 4.
Camera lucida reconstruction of the pair
of spiny stellate cells shown in Figure 3A. For clarity,
the presynaptic and postsynaptic neurons were separated. The dendritic
configuration of the neurons is drawn in red and
black for presynaptic and postsynaptic neurons,
respectively. The axonal arborization is drawn in blue
(presynaptic neuron) and green (postsynaptic neuron).
The gray shading delineates the barrel structure. Note
the dense projection of axon collaterals in layer 2/3. Scale bar, 100 µm.
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Figure 5.
Camera lucida reconstruction of the same pair of
spiny stellate cells as shown in Figures 3A and 4. A, The projecting neuron (cell 1) with its dendritic
arbor in red and the axon in blue.
B, The target neuron (cell 2) with its dendritic arbor
in black and the axon in green. Putative
autaptic contacts between axon and dendrites of the presynaptic cell
are marked with blue triangles. C,
Dendritic arbor of cell 2 (target neuron) and axonal projections of
cell 1 (projection neuron). Blue dots indicate putative
synaptic contacts between the presynaptic axon and the dendrites of the
postsynaptic spiny stellate cell as identified by high-power light
microscopic examination. The soma of the presynaptic cell is shown in
red. Autaptic contacts are not marked in
C. Scale bar, 100 µm.
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The axonal collaterals of spiny stellate cells project throughout all
cortical laminae from layer 1 to the white matter (Figs. 3A,
4) and remain largely confined to a single cortical column. The main
axon emerges from the soma and descends toward the white matter, giving
rise to numerous collaterals. Most of these collaterals branch off in
layer 4 and ascend toward layer 2/3. In layers 5 and 6, a few long
horizontal collaterals (length 500-800 µm) were observed that may
project to adjacent cortical columns. The densest axonal projection was
found in layers 4 and 2/3 where the axons show a high degree of
collateralization. In these layers most of the axonal collaterals were
confined to a single cortical column (Fig. 4). Their orientation is
predominantly vertical in layers 2/3 and 4, whereas in layers 5 and 6 they follow a slightly descending horizontal course (Figs.
3A, 4).
Putative synaptic contacts (two to five) (Feldmeyer et al.,
1999b) were distributed over the entire dendritic tree but
preferentially located on tertiary dendrites and relatively close to
the soma (Fig. 5C). In addition, potential autaptic contacts
were identified that displayed a similar dendritic distribution as the synapses.
To estimate the number of postsynaptic target neurons contacted by a
single spiny stellate cell, the total number of synaptic boutons was
counted separately for each cortical layer (Table 2). More than 75% of all synaptic
boutons were found in layers 4 and 2/3, with the highest density in
layer 2/3; the remaining 25% of synaptic boutons were found in layers
5 and 6 (Table 2). This result suggests that the main target cells of
spiny stellate cell axons are spiny neurons in layer 4 and pyramidal
neurons in 2/3, implying that the flow of excitation is preferentially directed from layer 4 to layer 2/3. This view is further substantiated by the fact that the number of synaptic boutons per 100 µm axonal segment was significantly higher (p > 0.01) in
layers 2/3 and 4 than in the other layers (Table
3). Although we cannot exclude the
possibility that boutons may also synapse on apical oblique dendrites
of infragranular pyramidal neurons, the preferential termination of
spiny stellate boutons appears to be on neurons in these layers.
Star pyramidal neurons
The second class of synaptically coupled excitatory neurons
resembled those designated as star pyramidal cells (Lund, 1984; for
review, see Lund, 1988). These neurons constitute a smaller fraction
(~20%) of the spiny neurons in layer 4 of the barrel cortex. Somata
and dendritic domains of star pyramidal neurons were also exclusively
located within layer 4, with the exception of the prominent apical
dendrite. Its distal part often ascends to layer 2/3, but without
forming a terminal tuft (Figs. 3B,
6). In contrast to spiny stellate cells,
star pyramidal cells never showed an asymmetry of the dendritic arbor
(Figs. 3B, 6). Three to seven primary basal dendrites emerge
from the spherical to ovoid soma that give rise to secondary, tertiary,
and higher-order basal dendrites of various lengths. Most of the
dendrites were restricted to a single barrel. The thick apical
dendrite emerges from the upper pole of the soma and ascends through
layer 4, giving rise to several oblique apical dendrites (Figs.
3B, 6). The number and distribution of synaptic and autaptic
contacts were similar to those of spiny stellate cells (see also
Feldmeyer et al., 1999b, their Table 2).
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Figure 6.
Camera lucida reconstruction of the pair of star
pyramidal cells shown in Figure 3B. For clarity, the
presynaptic and postsynaptic neurons were separated. The dendritic
configuration of the neurons is drawn in red and
black for presynaptic and postsynaptic neurons,
respectively. The axonal arborization is drawn in blue
(presynaptic neuron) and green (postsynaptic neuron).
The gray shading delineates the barrel structure. Scale
bar, 100 µm.
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The axons of star pyramidal cells projected also into all cortical
layers (1-6) but spared the white matter (Figs. 3B, 6). As
shown for spiny stellate cells, axonal collaterals were largely confined to a single cortical column. The main axon emerges either directly from the soma or from one of the primary basal dendrites and
descends toward the white matter. In some neurons the main axon was
seen to loop back toward layer 4 after reaching layer 6. The main axon
gives rise to numerous collaterals ascending vertically toward layer 1. Only a few but long collaterals (up to 700 µm) were observed to
descend to layers 5 and 6 (Figs. 3B, 6). Again, the most
dense axonal projection was established in layers 4 and 2/3, but the
density of collaterals and the degree in branching of the axonal
collaterals were lower when compared with the axonal arborization of
spiny stellate cells (compare Figs. 4 and 6). In layer 4, axonal
collaterals are largely confined to a single barrel, whereas in upper
layer 2/3 they fan out so that a few appear to project to adjacent
cortical columns (Figs. 3B, 6). In upper layer 2/3 axonal
collaterals were often organized in clusters, as described for
pyramidal cells of cortical laminae 2/3 and 5 (Fig. 3B) (see
also Gilbert and Wiesel, 1979). The total number of synaptic boutons on
the axons of star pyramidal cells was significantly lower than that of
spiny stellate cells (Table 2). This may be related to the lower number
of axonal collaterals, because the number of boutons per 100 µm
axonal segment was similar to that of spiny stellate cells
(p > 0.01) (Table 3). Again, most of the
synaptic boutons (~70%) were found in layers 4 and 2/3, with the
highest density in layer 2/3 (Table 2). The number of synaptic boutons
per 100 µm axonal segment was also significantly higher
(p > 0.01) in layers 2/3 than in layers 4 and 5 (Table 3). As observed for spiny stellate cells, star pyramidal neurons establish synaptic contacts predominantly with neurons in superficial layers 4 and 2/3 of the barrel cortex or superficial dendritic segments
of infragranular pyramidal neurons traversing through these layers.
This notion is supported by paired recordings between spiny layer 4 neurons and layer 2/3 pyramidal cells of the barrel cortex (Feldmeyer
et al., 1999a).
Postsynaptic target structures of excitatory spiny neurons in layer
4 of the barrel cortex
The number of axonal collaterals as well as the density of
synaptic boutons was highest in layers 4 and 2/3, suggesting that the
main stream of excitation via spiny layer 4 neurons is directed to
these layers. Synaptic contacts established by the axons of biocytin-labeled spiny neurons (n = 3) in layer 4 of
the barrel cortex with postsynaptic target structures in layers 4 and
2/3 were examined in serial ultrathin sections. Of the total number of
boutons investigated (n = 200; 75 in layer 4 and 125 in
layer 2/3), the vast majority of the target structures in layers 4 and 2/3 were excitatory spiny neurons. This could explain the high probability in electrophysiological experiments of finding connected pairs of excitatory spiny neurons in layer 4 or between layers 4 and
2/3 (Feldmeyer et al., 1999a,b). In layer 4, most of the synaptic
contacts (n = 55) were found on small caliber dendritic shafts (Fig. 7C,D)
and a smaller fraction (n = 20) on dendritic spines
(Fig. 7A) of other spiny neurons. In layer 2/3, synaptic contacts were formed with either small caliber dendritic shafts (n = 57) (Fig. 7F) or spines (n = 63) (Fig. 7E,G) of putative basal
dendrites of layer 2/3 pyramidal neurons (n = 120) and
on a smaller fraction with thick caliber apical dendrites
(n = 5) of either layer 2/3 or layer 5 pyramidal
neurons (Fig. 7H).
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Figure 7.
Electron microscopy of synaptic contacts
established by spiny stellate neurons on different postsynaptic target
structures in layers 4 (A-D) and 2/3
(E-H) as revealed from serial ultrathin sectioning
through the entire axonal domain. Boutons (b) of
synaptic contacts established by the axon of a biocytin-labeled spiny
stellate neuron on (A) a spine
(s) or (B-D) small
caliber dendritic shafts (d) of excitatory
neurons, presumably other spiny stellate neurons (E-H).
Synaptic contacts established by the axon of a biocytin-labeled spiny
stellate neuron on (E, G) spines,
(F) a small caliber dendritic shaft of basal
dendrites, and (H) an apical dendrite
(ad) of presumed pyramidal neurons in layer 2/3. Scale
bar, 0.5 µm.
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In addition, on every third grid, GABA postembedding immunogold
labeling was performed to further identify GABAergic target structures
of biocytin-labeled excitatory spiny cell axons. In the sample
investigated (n = 60 sections), no biocytin-labeled boutons were found that synapsed on GABAergic profiles. However, in the
same sample, GABAergic structures such as synapses, dendritic profiles,
and somata that were not contacted by biocytin-labeled boutons could be
easily identified (data not shown). Again, this finding suggests that
the main target structures of excitatory spiny neurons are other
excitatory spiny neurons in layer 4 and pyramidal neurons in layer
2/3.
| |
DISCUSSION |
The dendritic geometry, the axonal projections, and the
postsynaptic target structures of excitatory spiny neurons in layer 4 of the barrel cortex provide the morphological basis for their functional role in the microcircuitry of a cortical column. We have
sharpened the morphological picture of the excitatory microcircuits by
using dual recording from synaptically connected pairs and subsequent
characterization of the morphology of the spiny layer 4 neurons.
The results show that the dendritic arbor of synaptically coupled spiny
layer 4 neurons is largely confined to a single barrel in layer 4 and
that both synaptic and autaptic contacts were exclusively found within
a barrel in layer 4, whereas their axon collaterals project throughout
all cortical layers. The axonal collaterals were also largely confined
to a single cortical column in the granular and supragranular layers.
However, a few horizontal collaterals in layers 2/3, 5, and 6 project
to adjacent cortical columns. The total number of synaptic boutons and
their density per unit length of axon were highest in layers 2/3 and 4. These morphological findings suggest that the main target neurons of a
spiny neuron in layer 4 are other excitatory spiny neurons in layer 4 of the same barrel and pyramidal neurons in layer 2/3 of the same
cortical column (Feldmeyer et al., 1999a,b), and probably to a lesser
extent pyramidal neurons in infragranular layers 5 and 6.
Axonal projection pattern and dendritic morphology of spiny layer
4 neurons
The axonal projection of spiny layer 4 neurons in the barrel
cortex is highly organized with respect to the structure of a cortical
column. In a quantitative Golgi study, Harris and Woolsey (1983) have
shown that the main axonal trunk of class I neurons (corresponding to
spiny layer 4 neurons) is directed toward the white matter, with
recurrent collaterals projecting back into the barrels. Axonal
projections to infragranular and supragranular layers were not
reported, which may be attributable in part to the different plane of
sectioning and incomplete staining of axonal collaterals by the Golgi
method. Whole-cell recording in combination with intracellular biocytin
labeling in the oblique coronal slice (Agmon and Connors, 1991) made it
possible to describe the axonal projections of spiny layer 4 neurons in
more detail.
The axonal projections of spiny layer 4 neurons in the visual cortex
are well documented, in contrast to the barrel cortex (Martin and
Whitteridge, 1984; Lund, 1988; Burkhalter, 1989; Ahmed et al., 1994).
Spiny stellate and star pyramidal cells show a multitude of axonal
projection patterns. Axons can either be more locally organized or
display a patchy and extensive (2.5 mm lateral spread) tangential
projection (Martin and Whitteridge, 1984, their Figures 8-10). This
variability in projection patterns in layer 4 could be explained by the
different information processing pathways for somatic/visceral and
visual information as well as by different organization at the level of
cortical layer 4 (barrels vs ocular dominance columns).
The dendritic arborization pattern of spiny neurons in layer 4 has been
studied in detail previously (Pasternak and Woolsey, 1975; Woolsey et
al., 1975; Steffen, 1976; Steffen and van der Loos, 1980; Harris and
Woolsey, 1981; Simons and Woolsey, 1984). Asymmetry of the dendritic
arborization has been noted for some but not all spiny layer 4 neurons
(class I neuron). In this study, nearly all spiny stellate cells
(~95%) that were investigated showed a clear asymmetry, whereas star
pyramidal neurons with a characteristic main apical trunk display a
radially symmetric distribution of their basal dendrites. This
classification was possible because the oblique coronal plane of
sectioning allowed discrimination of spiny stellate and star pyramidal
neurons in contrast to the tangential plane used in Golgi studies
(Pasternak and Woolsey, 1975; Woolsey et al., 1975; Steffen, 1976;
Simons and Woolsey, 1984). Because the axonal and the dendritic field span of a spiny stellate cell show a strong overlap and cover one-third
to two-thirds of a barrel (~200-400 µm in diameter), the strong
asymmetry of the dendritic field could result in segregation of the
inputs within an individual barrel. This appears to be unlikely for
star pyramidal cells with a more radially symmetric dendritic field. In
addition, these neurons may receive additional synaptic input via their
apical dendrites.
Flow of excitation in the barrel cortex
Granular layer
The target structures of thalamic afferents arising from the
ventroposterior medial nucleus are excitatory spiny neurons and different GABAergic interneurons in layer 4 (White et al., 1984; Benshalom and White, 1986). Apart from thalamic input, these neurons receive excitation from intracortical sources, namely other spiny layer
4 neurons and layer 6 pyramidal neurons (Benshalom and White, 1986).
However, the contribution of thalamocortical versus intracortical projections to the excitatory drive of spiny layer 4 neurons is still a
matter of debate. It has been demonstrated that thalamocortical afferents to spiny layer 4 neurons in the barrel cortex are
characterized by a high reliability, whereas intracortical connections
are supposedly of low reliability (Gil et al., 1999). However, synaptic
transmission between individual spiny layer 4 neurons has a low failure
rate, a low coefficient of variation, and a high connectivity
(Feldmeyer et al., 1999b). This suggests that intracortical inputs
serve to enhance even weak thalamic activity; the main excitatory drive thus appears to be generated intracortically (Douglas et al., 1995;
Stratford et al., 1996; Feldmeyer et al., 1999b). Evidence supporting
this hypothesis comes from Ahmed et al. (1994) who reported a more than
fourfold preponderance of intracortical over thalamocortical inputs to
spiny stellate neurons of cat visual cortex. Furthermore, Stratford et
al. (1996) and Tarczy-Hornoch et al. (1999) found that both
thalamocortical and intracortical (spiny stellate-spiny stellate
connections) have a high reliability similar to those found in the
somatosensory cortex.
Supragranular layers
Spiny layer 4 neurons subsequently relay excitation to layer 2/3
but because of the largely columnar organization of the axons of these
neurons it remains restricted to neurons within the same cortical
column (Feldmeyer et al., 1999a,b). This finding is further supported
by optical recordings of voltage-sensitive dyes, which have shown that
excitatory activity evoked by stimulation of thalamocortical afferents
is largely restricted to a single barrel whereas in layer 2/3 it
spreads across cortical columns (Laaris et al., 2000). It may be
speculated that in layer 2/3 excitation arriving from layer 4 is
distributed by pyramidal cell axons throughout the primary
somatosensory cortex in vertical and horizontal directions (for review,
see DeFelipe and Farinas, 1992). In supragranular layers, the spread of
excitation may be no longer confined to a cortical column but mostly
lateral to adjacent or even more distant cortical columns (Fig.
8). Furthermore, excitatory activity is
probably not restricted to one hemisphere but also relayed by the
commissural axons of layer 2/3 pyramidal neurons via the corpus
callosum to the other hemisphere (DeFelipe and Farinas, 1992). This may
help to correlate and balance sensory input from the ipsilateral and
the contralateral whisker pad. Obviously this spread of excitation
depends mostly on the functional properties of spiny stellate and
pyramidal cells that will filter excitation, depending on the
frequency-dependent transmission properties (i.e., short-term
plasticity) and spatial and temporal coincidence of synaptic activity
in these neurons (Egger et al., 1999). This may represent the
initial step in the cortical integration of afferent sensory signals
from several whiskers. This proposal is supported by in vivo
2-deoxyglucose mapping and imaging studies showing that the tangential
spread of excitation occurs indeed at the level of layer 2/3 (McCasland
and Woolsey, 1988; Kleinfeld and Delaney, 1996; Woolsey et al., 1996).
Finally, layer 2/3 pyramidal cells can excite layer 5 pyramidal cells,
the principal output neurons of the neocortex (Thomson and Bannister,
1998; Reyes and Sakmann, 1999).
View larger version (38K):
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|
Figure 8.
Simplified schematic diagram of the flow of
excitation within a cortical column. At the level of layer 4, individual barrels are shown in dark gray. A functional
cortical column is superimposed in light gray.
Excitatory input coming from thalamic relay nuclei is relayed and
amplified in layer 4 by excitatory spiny neurons with strong synaptic
connections as indicated by the thick arrow. No
distinction was made between spiny stellate and star pyramidal neurons
because they have similar axonal projection patterns. Through the
vertical axonal collaterals of these neurons that have a preferential
projection toward superficial layers, excitation is then transmitted to
layer 2/3 pyramidal neurons and finally distributed throughout the
barrel cortex via the long-range tangential axons of layer 2/3
pyramidal cells. Thickness of arrows
indicates the preferential projections of the axons, in particular for
the spiny layer 4 neurons. Note that there are only weak tangential
projections to adjacent barrels. To reduce complexity, cortical
inhibition mechanisms and thalamic input to layers 5 and 6 have been
omitted.
|
|
Infragranular layers
In analogy to the visual cortex, spiny layer 4 neurons may also
establish synaptic contacts with layer 6 pyramidal neurons and in turn
may receive synapses from these neurons (Gilbert and Wiesel, 1979;
Martin and Whitteridge, 1984; McGuire et al., 1984; Benshalom and
White, 1986; Ahmed et al., 1994; Stratford et al., 1996; Tarczy-Hornoch
et al., 1999). The axonal projection of spiny layer 4 neurons toward
layer 6 makes it likely that such a feed-forward loop exists also in
the somatosensory cortex and may also serve to control the flow of excitation.
Inhibitory neurons
The flow of excitation within a cortical column is controlled by a
very heterogeneous population of GABAergic interneurons in each layer
(Somogyi et al., 1998; Gupta et al., 2000). Based on the location of
GABAergic synapses with excitatory principal neurons, interneurons have
different functions, e.g., feedback-feedforward inhibition and
suppression of dendritic Ca2+ spikes
(Miles et al., 1996; Larkum et al., 1999). Several classes of GABAergic
interneurons in the neocortex have been identified to date (Jones,
1993; Kawaguchi and Kubota, 1993, 1996, 1997; Deuchars and Thomson,
1995; Kawaguchi, 1995; Thomson et al., 1996; Tamás et al., 1997,
1998; Reyes et al., 1998; Gupta et al., 2000), and electrophysiological
recordings have demonstrated the existence of synaptic contacts between
spiny layer 4 neurons and layer 4 interneurons (V. Egger, D. Feldmeyer,
and B. Sakmann, unpublished results). However, their specific function
in the columnar microcircuitry is still unclear. Recent evidence
indicates that certain types of GABAergic interneurons are coupled via
gap junctions (Galarreta and Hestrin, 1999; Gibson et al., 1999). This
may support concerted activity of these neurons; however, it is still
unknown which effects this may have on the flow of excitation in a
cortical column.
| |
FOOTNOTES |
Received Nov. 24, 1999; revised April 28, 2000; accepted April 29, 2000.
This work was supported by the Deutsche Forschungsgemeinschaft (SFB
505/C6) and the Max-Planck-Society. We thank Dr. Imre Vida and Arnd
Roth for critically reading an earlier version of this manuscript. We
are also grateful to B. Joch, S. Nestel, M. Winter, and I. Dehof for
excellent technical assistance.
Correspondence should be addressed to Dr. Joachim Lübke,
Anatomisches Institut der Albert-Ludwigs-Universität Freiburg, Albertstraße 17, D-79104 Freiburg, Germany. E-mail:
luebkejo{at}uni-freiburg.de.
| |
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D. L. Barbour and E. M. Callaway
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M. Helmstaedter, J. F. Staiger, B. Sakmann, and D. Feldmeyer
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D. J. Wallace and B. Sakmann
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K. D. Alloway
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A. Frick, D. Feldmeyer, M. Helmstaedter, and B. Sakmann
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P. Krieger, T. Kuner, and B. Sakmann
Synaptic Connections between Layer 5B Pyramidal Neurons in Mouse Somatosensory Cortex Are Independent of Apical Dendrite Bundling
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T. Inoue and K. Imoto
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R. M. Bruno and B. Sakmann
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Morphology, Electrophysiology and Functional Input Connectivity of Pyramidal Neurons Characterizes a Genuine Layer Va in the Primary Somatosensory Cortex
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D. Feldmeyer, A. Roth, and B. Sakmann
Monosynaptic Connections between Pairs of Spiny Stellate Cells in Layer 4 and Pyramidal Cells in Layer 5A Indicate That Lemniscal and Paralemniscal Afferent Pathways Converge in the Infragranular Somatosensory Cortex
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A. I. Cowan and C. Stricker
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M. Zhang and K. D. Alloway
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H. N. Liu, T. Kurotani, M. Ren, K. Yamada, Y. Yoshimura, and Y. Komatsu
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C. P. Pluto, R. D. Lane, and R. W. Rhoades
Local GABA Receptor Blockade Reveals Hindlimb Responses in the SI Forelimb-Stump Representation of Neonatally Amputated Rats
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J. F. Staiger, I. Flagmeyer, D. Schubert, K. Zilles, R. Kotter, and H. J. Luhmann
Functional Diversity of Layer IV Spiny Neurons in Rat Somatosensory Cortex: Quantitative Morphology of Electrophysiologically Characterized and Biocytin Labeled Cells
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C. Wirth and H.-R. Luscher
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T. Nevian and B. Sakmann
Single Spine Ca2+ Signals Evoked by Coincident EPSPs and Backpropagating Action Potentials in Spiny Stellate Cells of Layer 4 in the Juvenile Rat Somatosensory Barrel Cortex
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K. M. M. Kaiser, J. Lubke, Y. Zilberter, and B. Sakmann
Postsynaptic Calcium Influx at Single Synaptic Contacts between Pyramidal Neurons and Bitufted Interneurons in Layer 2/3 of Rat Neocortex Is Enhanced by Backpropagating Action Potentials
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M. F. Casanova, D. Buxhoeveden, and J. Gomez
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R. M. Bruno, V. Khatri, P. W. Land, and D. J. Simons
Thalamocortical Angular Tuning Domains within Individual Barrels of Rat Somatosensory Cortex
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J. Lubke, A. Roth, D. Feldmeyer, and B. Sakmann
Morphometric Analysis of the Columnar Innervation Domain of Neurons Connecting Layer 4 and Layer 2/3 of Juvenile Rat Barrel Cortex
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K. J. Bender, J. Rangel, and D. E. Feldman
Development of Columnar Topography in the Excitatory Layer 4 to Layer 2/3 Projection in Rat Barrel Cortex
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J. Waters, M. Larkum, B. Sakmann, and F. Helmchen
Supralinear Ca2+ Influx into Dendritic Tufts of Layer 2/3 Neocortical Pyramidal Neurons In Vitro and In Vivo
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K. Fox, N. Wright, H. Wallace, and S. Glazewski
The Origin of Cortical Surround Receptive Fields Studied in the Barrel Cortex
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D. Schubert, R. Kotter, K. Zilles, H. J. Luhmann, and J. F. Staiger
Cell Type-Specific Circuits of Cortical Layer IV Spiny Neurons
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C. C. H. Petersen, A. Grinvald, and B. Sakmann
Spatiotemporal Dynamics of Sensory Responses in Layer 2/3 of Rat Barrel Cortex Measured In Vivo by Voltage-Sensitive Dye Imaging Combined with Whole-Cell Voltage Recordings and Neuron Reconstructions
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V. Rema, M. Armstrong-James, and F. F. Ebner
Experience-Dependent Plasticity Is Impaired in Adult Rat Barrel Cortex after Whiskers Are Unused in Early Postnatal Life
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G. Radnikow, D. Feldmeyer, and J. Lubke
Axonal Projection, Input and Output Synapses, and Synaptic Physiology of Cajal-Retzius Cells in the Developing Rat Neocortex
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M. Brecht and B. Sakmann
-Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex
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C. C. H. Petersen
Short-Term Dynamics of Synaptic Transmission Within the Excitatory Neuronal Network of Rat Layer 4 Barrel Cortex
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N. Laaris and A. Keller
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A. Laurent, J.-M. Goaillard, O. Cases, C. Lebrand, P. Gaspar, and N. Ropert
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D. Feldmeyer, J. Lubke, R A. Silver, and B. Sakmann
Synaptic connections between layer 4 spiny neurone- layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column
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M. Brecht and B. Sakmann
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C. C. H. Petersen and B. Sakmann
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X. Jin, P. H. Mathers, G. Szabo, Z. Katarova, and A. Agmon
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D. Schubert, J. F. Staiger, N. Cho, R. Kotter, K. Zilles, and H. J. Luhmann
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TOP
ABSTRACT
INTRODUCTION
