 |
 Previous Article | Next Article 
The Journal of Neuroscience, October 1, 2000, 20(19):7455-7462
Parallel Streams for the Relay of Vibrissal Information through
Thalamic Barreloids
Tiphaine
Pierret,
Philippe
Lavallée, and
Martin
Deschênes
Centre de Recherche Université Laval-Robert Giffard,
Hôpital Robert Giffard, Québec G1J 2G3, Canada
 |
ABSTRACT |
This study investigated the organization of a vibrissal pathway
that arises from the interpolar division of the spinal trigeminal complex (SP5i), transits through the ventral posterior medial nucleus
(VPM), and innervates the somatosensory cortical areas in the rat.
Using Fluoro-Gold and biotinylated dextran amine, respectively, as
retrograde and anterograde tracers, the following organization plan was
disclosed. The SP5i projection arises from a population of small-sized
neurons that selectively innervate the ventral lateral part of VPM. In
cytochrome oxidase-stained material, this region does not display any
barreloid arrangement, but Fluoro-Gold injections in single barrel
columns labeled rods of cells that extend caudally into the ventral
lateral division of VPM. Thus, on the basis of retrograde labeling,
barreloids were divided into core and tail compartments, which
correspond to the rod segments running across the dorsal and ventral
lateral parts of VPM, respectively. Double-labeling experiments
revealed that SP5i afferents innervate the tail of barreloids. The
anterograde labeling of thalamocortical axons show that most "core
cells" project to a single barrel column, whereas some "tail
cells" give rise to branching axons that innervate the second
somatosensory area and the dysgranular zone of the barrel field.
Injections that straddled the transition zone between the core and tail
regions disclosed cells projecting to a single barrel column and to the surrounding dysgranular zone. These results suggest that the projection of "barreloids cells" to the granular and/or dysgranular zones relates to the class of prethalamic input(s) they receive.
Key words:
whiskers; barrels; ventral posterior medial nucleus; thalamocortical projections; trigeminothalamic afferents; spinal
trigeminal nucleus
| |
INTRODUCTION |
On each side of the rat snout, there
are five horizontal rows of whiskers that form an orderly array of
low-threshold mechanoreceptors. Each peripheral fiber innervating these
mechanoreceptors responds to only one vibrissa and, centrally, the
arrangement of the vibrissal pad is maintained in arrays of cellular
aggregates referred to as barrelettes (brainstem), barreloids
(thalamus), and barrels (cortex). Brainstem nuclei that receive
vibrissal primary afferents include the principal trigeminal nucleus
(PR5) and all subdivisions of the spinal trigeminal complex (SP5). Each
of these (sub)nuclei contributes axons to the trigeminothalamic tract,
but the main stream of ascending fibers arises from the PR5 and the
interpolar division of the SP5 (SP5i).
Anatomical studies provided clear evidence for a one-to-one
relationship between single whiskers and corresponding modules in the
PR5, in the ventral posterior medial nucleus (VPM), and in the barrel
cortex (Chmielowska et al., 1989 ; Lu and Lin, 1993; Williams et al.,
1994; Agmon et al., 1995; Veinante and Deschênes, 1999). The
organization of the SP5i-thalamo-cortical axis, however, remains poorly
understood. This axis comprises, at least, two pathways: one that
projects to the posterior group nucleus (Po) and another to VPM (Chiaia
et al., 1991a; Williams et al., 1994; Veinante et al., 2000). A central
issue concerning latter projections bears on their relationships with
the barreloid/barrel system. Traditionally, barreloids have been
identified by either cytochrome oxidase (CO) histochemistry or
retrograde labeling after deposit of a tracer into a single barrel.
Using horseradish peroxidase as a retrograde tracer, Saporta and Kruger
(1977) first reported the rod-like clustering of VPM cells that project
to the rat barrel cortex. Although injections were clearly not
restricted to the size of a single barrel, VPM rods consisted of a
sharply defined core of neurons in rostral VPM in which virtually all
neurons were labeled; caudally, rods thinned out, forming a tail in
which labeled and unlabeled cells were intermingled. Similar rod-like clusters, although narrower in size, were evidenced in mice after tracer injections restricted to a single barrel column (Hoogland et
al., 1987). The three-dimensional structure of barreloids was later examined by Land et al. (1995) using CO histochemistry. Barreloids were reported to form curved tapering cylinders, their long
axis lying normal to the VPM/Po border. Ventrolaterally, as they
approach the ventral posterior lateral nucleus (VPL), the tips of
barreloids were seen to converge midway through the rostrocaudal extent
of VPM. So defined, barreloids did not exhibit a caudal extension, a
tail, as evidenced in retrograde-labeling experiments. The mismatch
between both sets of data seems to occur in the ventrolateral and
caudal aspects of VPM in which SP5i afferents project. The present
series of experiments were undertaken to clarify the input-output
organization of this region of the rat thalamus.
| |
MATERIALS AND METHODS |
Experiments were made in 65 adult rats (Sprague Dawley) in
accordance with the federally prescribed and university animal care and
use guidelines (Olfer et al., 1993). Surgery was performed under
ketamine (75 mg/kg) plus xylazine (5 mg/kg) anesthesia, and rats were
given analgesics (Anafen, 5 mg/kg) before being returned to their cage.
In different experiments, biotinylated dextran amine (BDA) (molecular
weight, 10,000 kDa; Molecular Probes, Eugene, OR) or Fluoro-Gold
(FG) (Fluorochrome Inc., Denver, CO) were used alone or in
combination as anterograde and retrograde tracers, respectively. The
stereotaxic coordinates of the atlas of Paxinos and Watson (1986) were
used to target the injections in SP5i or VPM, and the recording of
vibrissae-evoked responses was routinely done to ascertain the correct
placement of the injections.
All injections were made by iontophoresis by means of small-sized
micropipettes (5-30 µm). Biotinylated dextran amine (2% in 0.5 M potassium acetate) was ejected with positive current pulses of 300-1000 nA for periods ranging from 20 to 30 min.
Fluoro-Gold (2% in 0.1 M cacodylate buffer, pH 7.0) was
ejected with positive current pulses of 100-1000 nA for periods of
10-15 min. After survival periods of 1-7 d, animals were perfused
with saline followed by a fixative containing 4% paraformaldehyde and
0.5% glutaraldehyde in phosphate buffer (0.1 M, pH
7.4). Brains were post-fixed in the same fixative for 2 hr,
cryoprotected overnight in 30% sucrose, and cut at 50 µm on a
freezing microtome.
Except for the cases of double labeling, sections were usually
processed for CO histochemistry (Wong-Riley, 1979) before revealing BDA
or FG. Biotinylated dextran was revealed using the
avidin-biotin-peroxidase complex (ABC kit; Vector Laboratories,
Burlingame, CA) and the nickel-3,3'-diaminobenzidine
tetrahydrochloride (DAB) substrate (Sigma, St. Louis, MO).
Fluoro-Gold-labeled neurons were immunoreacted with an anti-Fluoro-Gold
antiserum (Chemicon, Temecula, CA). After three rinses in PBS
(0.01 M, pH 7.4) sections were incubated overnight in a
solution containing 3% normal goat serum (Vector Laboratories), 0.2%
Triton X-100, and anti-Fluoro-Gold antiserum (1:10,000). After three
rinses in PBS, sections were incubated for 1 hr in the secondary
antibody (biotinylated goat IgG; Vector Laboratories), rinsed three
times in PBS, and reacted with the ABC kit. After three rinses in
Tris-buffered saline (0.1 M, pH 7.6), peroxidase was
revealed with the nickel-DAB substrate. In double-labeling experiments, FG was first revealed using a peroxidase-labeled secondary
antibody (goat IgG; Chemicon) and DAB as a substrate (brown reaction
product). Next, sections were processed for BDA histochemistry using
the ABC kit and nickel-DAB (black reaction product). Finally, sections
were mounted on gelatin-coated slides, dehydrated in alcohols, cleared
in toluene, and coverslipped without counterstaining. Labeled material
was drawn with a camera lucida using 25 or 40× objectives.
Morphometric analysis and three-dimensional reconstructions were made
with the Neurolucida and Neurotrace software (MicroBrightField,
Colchester, VT). The somatic cross-sectional areas of retrogradely
labeled neurons were measured from tracings of the perimeters of
labeled neurons drawn with the aid of a camera lucida using a 40×
objective. The location of injection sites and projection foci was
assessed from the nuclear divisions and cytoarchitectonic features
outlined by the CO stain. In the present paper, the term "dysgranular
zone" of S1 refers to the region in and around the barrel field in
which layer 4 displays a low CO reactivity.
| |
RESULTS |
The ventral lateral part of VPM receives SP5i afferents
In Nissl-stained material, no cytoarchitectonic subdivision can be
distinguished in the rat VPM. Neither calbindin nor parvalbumin immunoreactivity, which stain matrix and rod compartments in feline and
primate VPM, reveal homologous territories in rodents. The topography
of SP5i projections, however, clearly delineates a ventrolateral region
to which we shall refer as the VPMvl. Figure 1A-C shows a series of
photomicrographs that illustrate the extent of this SP5i recipient
zone. Delimited laterally by the VPL, VPMvl is a half-crescent-shaped
region that approximately corresponds to the lower tier of VPM. It is
thicker caudally and thins out rostrolaterally. In CO-stained material,
VPMvl often displays a lighter coloration, which is better appreciated
when the enzymatic reaction is allowed to fully develop (Fig.
1D). That VPMvl is distinct from the dorsal aspect of
the nucleus is further indicated by the distribution of retrogradely
labeled trigeminothalamic cells after FG injections restricted to
either parts of the nucleus (Fig. 2).
Injections in dorsal VPM, with minimal spread to VPMvl, produces heavy
retrograde labeling in PR5 barrelettes but very sparse labeling in
SP5i. Conversely, injections centered in VPMvl label neurons
principally in SP5i and a smaller population of cells in the PR5.
View larger version (162K):
[in this window]
[in a new window]
|
Figure 1.
Distribution of SP5i terminal fields in
the rat VPM. A-C show, in CO-stained sections, the
topography of BDA-labeled SP5i terminal fields at different frontal
planes (rostral to caudal in A-C). Note
the segregation of terminal fields in VPMvl. In tissue processed
only for CO histochemistry (D), VPMvl displays
lighter staining than the dorsal part of the nucleus.
Asterisks outline the frontier between VPM and VPL.
Scale bar in A also applies to B and
C.
|
|
View larger version (72K):
[in this window]
[in a new window]
|
Figure 2.
Distribution of retrogradely labeled
trigeminothalamic cells after FG injections in different parts of the
somatosensory thalamus. Injections sites in dorsal VPM, VPMvl, and Po
are shown in A-C, with the corresponding maps of
retrogradely labeled cells below. Each map represents
the counts of five consecutive sections. sp5, Spinal
trigeminal tract; SP5o, oral division of the spinal
trigeminal complex; VC, ventral cochlear nucleus;
7n, tract of the facial nerve.
|
|
Small-sized SP5i neurons project to VPMvl
In a previous study (Veinante et al., 2000), we reported that two
types of SP5i fibers convey vibrissal information to the thalamus:
thick, fast-conducting fibers that project to Po and thin,
slow-conducting axons that project to VPM. The two groups of axons were
supposed to arise, respectively, from the large and small cells
identified previously in SP5i by Phelan and Falls (1991). To test this
hypothesis, we measured the cross-sectional area of SP5i cell bodies
retrogradely labeled after FG deposits restricted to dorsal Po or VPMvl
(Figs. 2B,C). The histograms of Figure 3 show that indeed the two
populations of neurons differ in size. Cells projecting to Po exhibit
larger somata than those projecting to VPMvl (mean ± SD
cross-sectional area, 396 ± 153 vs 153 ± 64 µm2). This difference is statistically
significant (Student's t test, p < 0.001),
thus confirming the distinct cellular origin of SP5i projections to
VPMvl and Po.
View larger version (60K):
[in this window]
[in a new window]
|
Figure 3.
Comparative distributions of the cross-sectional
areas of cell somata of SP5i neurons that project to VPMvl
(black bars) and Po (white bars).
Insets A and B show
FG-labeled cells projecting to VPMvl and Po, respectively. Injection
sites in Po and VPMvl are shown in Figure 2.
|
|
The core-tail structure of thalamic barreloids
To determine whether VPMvl relay neurons project to the barrel
cortex and whether they are part of thalamic barreloids, small FG
injections were made in layer 4 of physiologically identified barrel
columns. The use of fine micropipettes (10 µm) and low-intensity currents (100-200 nA) reduced tracer diffusion to neighbor barrels, but spread to the supragranular layers over the injected barrel was
unavoidable. Of 25 attempts to inject a single barrel column, eight
cases were successful. These include barrel columns representing whiskers B2, B4, C2, C3, D2, D3, and E3. Fluoro-Gold injections restricted to a single barrel column label sharply defined arrays of
cells in dorsal VPM (Fig. 4). Like the
barreloids outlined by CO staining (Land et al., 1995), arrays are
~100 µm wide and extend from the VPM/Po border toward VPL. In some
sections, especially after the injection of barrel columns in C and D
rows, CO light septa are seen flanking the rod of cells. These compact
clusters of neurons form the core of barreloids. On reaching VPMvl,
rods bend caudalward, forming a long string of cells in the posterior part of the nucleus (Fig. 4C,F). In this
tail region, arrays differ from the rostral zone by displaying a lower
cell density and less precise borders. The three-dimensional structure
of barreloids B2 and D3 is shown in Figure
5 in which the core and tail regions are
highlighted in different gray tones. It must be stressed
that, in the absence of anterograde labeling, no sharp border can be drawn between the dorsal part of VPM and VPMvl. Thus, the transition between the core and tail of barreloids was assumed to occur where the
rod of cells bent horizontally in the caudal direction. This transition
occurs gradually in barreloids representing whiskers in D and E rows
but manifests by a sharper bend in barreloids of the A and B rows (see
sagittal representations in Fig. 5). Injections that spread to two
adjacent barrel columns label cell clusters approximately twice as wide
but with a similar three-dimensional structure. Thus, these results
show that each barrel column receives input from an array of thalamic
neurons which, in dorsal VPM and VPMvl, form the core and tail of
barreloids, respectively.
View larger version (95K):
[in this window]
[in a new window]
|
Figure 4.
Retrograde labeling in the rat VPM after FG
injections in barrel column C2. Tangential sections in A
and D show the cortical injection sites.
B and C show, respectively, the core and
tail of barreloid C2 in coronally cut sections. The core and tail of
the same barreloid, as they appear in horizontal sections, are shown in
E and F, respectively. A,
Anterior; L, lateral; P, posterior.
|
|
View larger version (30K):
[in this window]
[in a new window]
|
Figure 5.
Three-dimensional structure of thalamic
barreloids as revealed by the retrograde transport of FG injected in
barrel columns D3 (A) and B2
(B). Horizontal, frontal, and sagittal views are
shown from left to right. The
black and gray dots represent,
respectively, neurons within the core and tail of barreloids. The
transition between the core and tail was assumed to occur at the dorsal
VPM/VPMvl border. A, Anterior; D, dorsal;
M, medial; P, posterior.
|
|
SP5i afferents innervate the tail of barreloids
Direct evidence that SP5i afferents innervate the tail of
barreloids was provided by double-labeling experiments (five cases) in
which BDA and FG were injected, respectively, in SP5i and
physiologically identified barrel columns. A clear overlap of
anterograde axonal and retrograde cellular labeling was observed in two
experiments. Figure 6 shows the
distribution of SP5i axons with respect to the core and tail of
barreloids C2/C3. In the core region, no anterograde labeling is
observed, although labeled fibers are present in VPMvl, beneath the
cluster of stained somata (Fig. 6C). In sections passing
through the tail of the same barreloids, however, numerous darkly
stained fibers and terminations are seen among the brown-labeled somata
(Fig. 6D). Failure to observe overlap in the other
experiments likely relates to the small size of the SP5i injections,
because in those cases projection foci were seen next to the clusters
of retrogradely labeled cells.
View larger version (133K):
[in this window]
[in a new window]
|
Figure 6.
Selective innervation of the tail of
barreloids by SP5i afferents. The injection sites of BDA in SP5i and of
FG in barrel columns C2/C3 are shown in A and
B, respectively. Dark blue SP5i fibers in
C are seen beneath the rod of
brown-labeled somata forming the core of barreloids. In
the tail region (D), dark blue
fibers and terminals are seen among the cluster of FG-labeled
cells.
|
|
Thalamocortical projections from the core and tail
of barreloids
The selective innervation of the tail of barreloids by SP5i
afferents raises the issue of a differential projection from the core
and tail subdivisions on the barrel cortex. This question was addressed
by making BDA injections in dorsal VPM and VPMvl, respectively. As
expected, injections in the dorsal VPM (four cases) label fibers that
project massively to the CO-reactive barrels and innervate more
sparsely the upper layer 6 of the same barrel columns (Fig.
7A,B).
In contrast, injections restricted to the VPMvl (eight cases)
highlighted projections across a broader expanse of the neocortex,
which includes the second somatic sensory area (S2), the insular
region, and the dysgranular zone of the primary somatic sensory area
(S1) (Figs. 7C,D,
8B). The most robust projection foci are observed in layers 4 and 6 of S2, whereas the
concurrent anterograde labeling in S1 is principally concentrated in
layers 3, 4, and 6. Injections that straddled the transition zone
between dorsal VPM and VPMvl (three cases) led to a mixed pattern of
anterograde labeling consisting of dense projection foci in the barrel
columns and a lighter projection to the surrounding dysgranular zone
and S2.
View larger version (172K):
[in this window]
[in a new window]
|
Figure 7.
Thalamocortical projections arising
from the dorsal part of VPM and from VPMvl. Biotinylated dextran
injections in dorsal VPM (A) label fibers that
terminate in the barrels (B), whereas injections
in VPMvl (C) produce terminal labeling in
interbarrel regions (D). Scale bars:
C, 500 µm; D, 250 µm.
|
|
View larger version (29K):
[in this window]
[in a new window]
|
Figure 8.
Camera lucida reconstructions of thalamocortical
fibers arising from the dorsal part of VPM and from VPMvl. The
"standard" type of barrel-specific fiber, which was labeled after
BDA injections in dorsal VPM, is shown in A.
B shows the areal distribution of thalamocortical axons
labeled after BDA injection in VPMvl. Four consecutive sections were
used for the reconstruction. Branching axons that project to the
dysgranular zone of S1 and to S2 are shown in C. A fiber
that innervates both a barrel and the surrounding dysgranular zone is
shown in D (see Results). Shaded patches
represent cortical barrels. CPu, Caudate putamen;
GP, globus pallidus; Rf, rhinal
fissure.
|
|
Although injections of the size shown in Figure 7 label too many fibers
to allow the complete reconstruction of but a few axonal arbors, at
least three types of thalamocortical axons were clearly recognizable in
our material. The "standard" type of thalamocortical axon that
projects to a single barrel column was observed after injections
restricted to dorsal VPM (Fig. 8A). By far, this type of axon seems to constitute the most prevalent thalamic input to the
barrels. The second type of fiber consists of VPMvl axons that project
to both S2 and the dysgranular zone of S1. The sparsity of these fibers
in S1 allowed the complete reconstruction of 20 local axonal arbors
which, in backward reconstructions, were all seen to stem from parent
fibers that also projected to S2 (Fig. 8C). Injections that
straddled the dorsal VPM/VPMvl border also provided clear evidence for
a third type of fiber that innervates both a single barrel column and
the surrounding dysgranular zone (Fig. 8D). This last
type of fiber was intermingled with, and often hidden by, the numerous
barrel-specific projecting axons. The one shown in Figure
8D was sufficiently isolated from the rest of the
projection focus to be fully reconstructed, but close examination of
the material and several cases of partial reconstruction suggest that
many axons of this type arise from the transition zone between dorsal
VPM and VPMvl.
| |
DISCUSSION |
The present study provides evidence for a stream of vibrissal
information that arises from a population of small-sized SP5i neurons,
transits through the ventral lateral part of VPM, and innervates the
barrel cortex and S2. This stream parallels the PR5-thalamo-cortical
pathway, but differs from the latter on several aspects.
The PR5 and SP5i projection systems
In the vibrissal sensory system, first-order afferents have
single-whisker receptive fields and project on corresponding
barrelettes in the PR5 and SP5i by means of axons that branch
repeatedly throughout the trigeminal column (Hayashi, 1980, 1985;
Jacquin et al., 1986b). The vast majority of PR5 cells that project to
VPM have narrow, barrelette-bounded dendritic trees, which makes them
responsive to the displacement of a single vibrissa (Shipley, 1974;
Jacquin et al., 1988; Henderson and Jacquin, 1995; Veinante and
Deschênes, 1999) In contrast, thalamic-projecting SP5i cells
distribute dendrites across multiple barrelettes and thereby manifest a
multi-whisker responsiveness (Woolston et al., 1982; Jacquin et
al., 1986, 1989). The ascending SP5i multi-whisker stream is composed
of at least two distinct subsystems: one that arises from small-sized
neurons that project to VPMvl and another that arises from large
multipolar neurons that project to Po (Veinante et al., 2000). For the
sake of the present discussion, this latter subsystem shall not be considered further.
The whisker-like patterning of the terminal fields of PR5 axons in the
rat VPM has been well documented at both the ensemble level and a
single-cell level (Williams et al., 1994; Veinante and Deschênes,
1999). These fibers project principally to the dorsal part of the
nucleus, forming bushy terminal fields whose size corresponds to that
of the barreloids highlighted by CO staining (Williams et al., 1994;
Land et al., 1995; Veinante et al., 1999). In VPMvl, the CO stain
lightens, septal divisions disappear and, as a whole, the SP5i
projection does not exhibit any clear whisker-like arrangement. Yet,
single SP5i axons form narrow bushy arbors whose size and orientation
suggest an intriguing continuity with the tip of the barreloids
(Veinante et al., 2000).
A more global and comprehensive organizational plan emerges, however,
when the thalamocortical projections to a single barrel column are
examined by retrograde labeling. Each barrel column is seen to receive
input from a rod of cells that extends across the PR5 and SP5i
recipient zones of VPM. Thus, barreloids, as defined by CO staining,
correspond to only the rostral segment of the rod traversing the dorsal
VPM. We referred to this rostral segment as the core of barreloids in
Results. Cells within the core project only to S1, and the vast
majority seem to innervate a single barrel column. The SP5i recipient
segment contains the tail of barreloids, and the residing cells project
massively to S2 and less densely to the dysgranular zone of S1.
However, the distribution of axonal branches in S1 does not suggest any
specific topographic relationship with single barrel columns.
Therefore, cells with branching axons can hardly account for the barrel
specificity of the projections arising from the tail of barreloids.
More likely candidates are the cells that project to a single barrel
column and to the surrounding dysgranular zone. Tracer injections
suggest such cells to be located in the transition zone between dorsal VPM and VPMvl. For the moment, this zone remains ill-defined in regards
to both the topographic distribution of trigeminal inputs and the
dendroarchitecture of the relay cells. If one assumes dendritic field
sizes of 250-300 µm for VPM neurons (Harris, 1987; Chiaia et al.,
1991b), many cells straddling the VPM/VPMvl border would be in a
position to receive convergent inputs from both PR5 and SP5i afferents.
Indeed, ultrastructural and electrophysiological studies provided
evidence for the convergence of PR5 and SP5i axons onto single VPM
neurons (Chiaia et al., 1991a; Wang and Ohara, 1993; Freidberg et al.,
1999), but the location of the cells contacted by both inputs remained
undetermined. Intracellular recording of PR5- and SP5i-evoked synaptic
responses and cell labeling will be required to settle this issue.
We know of no study that investigated, at a single-cell level, the
diversity of thalamocortical projections arising from the rat VPM. Bulk
anterograde-labeling studies suggest a rather homogeneous population of
fibers that innervate single barrel columns (Chmielowska et al., 1989;
Lu and Lin, 1993; Agmon et al., 1995), and the reconstructions of
Jensen and Killackey (1987) provided several examples of such fibers
that were labeled after horseradish peroxidase injections in the white
matter beneath the barrel cortex. Interestingly, that study also
disclosed other types of fibers, some resembling that illustrated in
Figure 8D. Although additional experiments will be
required to match fiber types with the location of their cells of
origin within the barreloids, it is already clear that barrel columns
receive input from more than one type of VPM fiber and that the
thalamic neurons from the core and tail of barreloids innervate
different zones of the somatosensory areas. Our anatomical data suggest
that, whether a cell projects to a single barrel column, to a barrel
column and the surrounding dysgranular zone, or again to the
dysgranular zone and S2, relates to its location in the barreloids.
Accordingly, cells on which PR5 and SP5i afferents converge might be
the ones that innervate the granular and dysgranular zones of the
barrel field.
The requirement for parallel pathways
To what extent SP5i projections contribute to the multi-whisker
responses of cells in the barrel cortex is difficult to assess from
previous physiological studies. It is well established that, in
undrugged or lightly anesthetized rats, the receptive field of VPM
cells is composed of multiple whiskers (Simons and Carvell, 1989;
Armstrong-James and Callahan, 1991; Nicolelis and Chapin, 1994;
Freidberg et al., 1999). A dominant whisker is always found; its
deflection induces a robust short latency response, whereas the
deflection of the other whiskers composing the field produces responses
of lower magnitude at longer latency. The latter responses are
abolished by SP5i lesion, which reduces the receptive field to one or
two whiskers (Rhoades et al., 1987; Freidberg et al., 1999). Thus,
under light anesthesia, one would expect cortical cells to exhibit
similar response profiles after stimulation of the dominant and
nondominant whiskers. Indeed they do (Armstrong-James et al., 1991).
However, the SP5i-mediated multi-whisker responses of VPM neurons was
found to bear no contribution to the evoked discharges of cells in
cortical barrels, the responses to the nondominant vibrissae being
mediated by intracortical rather than thalamocortical connections
(Armstrong-James and Callahan, 1991). One must then conclude that the
late-arriving multi-whisker thalamic input is in some way suppressed by
an intracortical inhibitory mechanism. This seems plausible,
considering that thalamocortical axons make a number of synaptic
contacts with GABAergic neurons within the barrels (White, 1985;
Keller, 1995). This explanation, however, leaves unresolved the
contribution of SP5i afferents to the sensory processes taking place in
the barrel cortex.
Insofar as PR5 and SP5i cells receive input from the same primary
afferents, the requirement for parallel vibrissal pathways likely
relates not to the processing of different sensory submodalities but to
complexities arising from the operation of a mobile sensory organ. Rats
commonly explore their environment and palpate objects by repetitive
forward and backward sweeping movements of the mystacial vibrissae.
Thus, parallel processes are required for gating sensory signals
induced by self-initiated movements, for filtering redundant information, and for deblurring "vibrissal images" acquired during head and body displacements. Whether the SP5i network fulfills any of
these functions is currently unknown, but in view of the apparent
idleness of this system in head-restrained animals, one is inclined to
believe that the type of information conveyed to the cortex by this
subsystem relates to the processing of vibrissal information during
active whisking.
| |
FOOTNOTES |
Received May 26, 2000; revised July 18, 2000; accepted July 21, 2000.
This work was supported by Medical Research Council of Canada Grant MT
5877. T.P. was supported by a CIEC Training Grant from the
Government of Canada.
Correspondence should be addressed to Martin Deschênes, Centre de
Recherche, Université Laval-Robert Giffard, Hôpital
Robert-Giffard, 2601 de la Canardière, Québec G1J 2G3,
Canada. E-mail: martind{at}microtec.net.
| |
REFERENCES |
-
Agmon A,
Yang LT,
Jones EG,
O'Dowd DK
(1995)
Topological precision in the thalamic projection to neonatal mouse barrel cortex.
J Neurosci
15:549-561[Abstract].
-
Armstrong-James M,
Callahan CA
(1991)
Thalamocortical processing of vibrissal information in the rat. II. Spatiotemporal convergence in the thalamic ventroposterior medial nucleus (VPm) and its relevance to generation of receptive fields of S1 cortical barrel neurones.
J Comp Neurol
303:211-224[Web of Science][Medline].
-
Armstrong-James M,
Callahan CA,
Friedman MA
(1991)
Thalamocortical processing of vibrissal information in the rat. I. Intracortical origins of surround but not center-receptive fields of layer IV neurones in the rat S1 barrel field cortex.
J Comp Neurol
303:193-210[Web of Science][Medline].
-
Chiaia NL,
Rhoades RW,
Bennett-Clarke CA,
Fish S,
Killackey HP
(1991a)
Thalamic processing of vibrissal information in the rat. I. Afferent input to the ventral posterior medial and posterior nuclei.
J Comp Neurol
314:201-216[Web of Science][Medline].
-
Chiaia NL,
Rhoades RW,
Fish SE,
Killackey HP
(1991b)
Thalamic processing of vibrissal information in the rat. II. Morphological and functional properties of ventral posterior medial nucleus and posterior nucleus neurons.
J Comp Neurol
314:217-236[Web of Science][Medline].
-
Chmielowska J,
Carvell GE,
Simons DJ
(1989)
Spatial organization of thalamocortical and corticothalamic projection systems in the rat SmI barrel cortex.
J Comp Neurol
285:325-338[Web of Science][Medline].
-
Freidberg MH,
Lee SM,
Ebner FF
(1999)
Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia.
J Neurophysiol
81:2243-2252[Abstract/Free Full Text].
-
Harris RM
(1987)
Morphology of physiologically identified thalamocortical relay neurons in the rat ventrobasal thalamus.
J Comp Neurol
251:491-505.
-
Hayashi H
(1980)
Distribution of vibrissae afferent fiber collaterals in the trigeminal nuclei as revealed by intra-axonal injection of horseradish peroxidase.
Brain Res
183:442-446[Web of Science][Medline].
-
Hayashi H
(1985)
Morphology and central terminations of intra-axonally stained large myelinated primary afferent fibers from facial skin in the rat.
J Comp Neurol
237:195-215[Web of Science][Medline].
-
Henderson TA,
Jacquin MF
(1995)
What makes subcortical barrels?
In: Cereb cortex, Vol 12, The barrel cortex of rodents (Jones EG,
Diamond IT,
eds), pp 123-187. New York: Plenum.
-
Hoogland PV,
Welker E,
Van der Loos H
(1987)
Organization of the projections from barrel cortex to thalamus in mice studied with Phaseolus vulgaris-leucoagglutinin and HRP.
Exp Brain Res
68:73-87[Web of Science][Medline].
-
Jacquin MF,
Mooney RD,
Rhoades RW
(1986)
Morphology, response properties, and collateral projections of trigeminothalamic neurons in brainstem subnucleus interpolaris of rat.
Exp Brain Res
61:457-468[Web of Science][Medline].
-
Jacquin MF,
Golden JP,
Panneton WM
(1988)
Structure and function of barrel "precursor" cells in trigeminal nucleus principalis.
Dev Brain Res
43:309-314.
-
Jacquin MF,
Barcia M,
Rhoades RW
(1989)
Structure-function relationships in rat brainstem subnucleus interpolaris. IV. Projection neurons.
J Comp Neurol
282:45-62[Web of Science][Medline].
-
Jensen KF,
Killackey HP
(1987)
Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents.
J Neurosci
7:3529-3543[Abstract].
-
Keller A
(1995)
Synaptic organization of the barrel cortex.
In: Cereb cortex, Vol 12, The barrel cortex of rodents (Jones EG,
Diamond IT,
eds), pp 221-262. New York: Plenum.
-
Land PW,
Buffer SA,
Yaskosky DJ
(1995)
Barreloids in adult rat thalamus: three-dimensional architecture and relationship to somatosensory cortical barrels.
J Comp Neurol
355:573-588[Web of Science][Medline].
-
Lu S-M,
Lin RC-S
(1993)
Thalamic afferents of the rat barrel cortex: a light- and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer.
Somatosens Mot Res
10:1-16[Web of Science][Medline].
-
Nicolelis MAL,
Chapin JK
(1994)
Spatiotemporal structure of somatosensory responses of many neurons ensembles in the rat ventral posterior medial nucleus of the thalamus.
J Neurosci
14:3511-3542[Abstract].
-
Olfer ED,
Cross BM,
McWilliams AA
(1993)
In: Guide to the care and use of experimental animals. Bradda, Canada: Canadian Council on Animal Care.
-
Paxinos G,
Watson C
(1986)
In: The rat brain in stereotaxic coordinates, Ed 2. Sydney: Academic.
-
Phelan KD,
Falls WM
(1991)
A comparison of the distribution and morphology of thalamic, cerebellar and spinal projection neurons in rat trigeminal nucleus interpolaris.
Neuroscience
40:497-511[Web of Science][Medline].
-
Rhoades RW,
Belford GR,
Killackey HP
(1987)
Receptive-field properties of rat ventral posterior medial neurons before and after selective kainic acid lesions of the trigeminal brain stem complex.
J Neurophysiol
57:1577-1600[Abstract/Free Full Text].
-
Saporta S,
Kruger L
(1977)
The organization of thalamocortical relay neurons in the rat ventrobasal complex studied by the retrograde transport of horseradish peroxidase.
J Comp Neurol
174:187-208[Medline].
-
Shipley MT
(1974)
Response characteristics of single units in the rat's trigeminal nuclei to vibrissa displacements.
J Neurophysiol
37:73-90[Free Full Text].
-
Simons DJ,
Carvell GE
(1989)
Thalamocortical response transformation in the rat vibrissa-barrel system.
J Neurophysiol
61:311-330[Abstract/Free Full Text].
-
Veinante P,
Deschênes M
(1999)
Single- and multi-whisker channels in the ascending projections from the principal trigeminal nucleus in the rat.
J Neurosci
19:5085-5095[Abstract/Free Full Text].
-
Veinante P,
Jacquin MF,
Deschênes M
(2000)
Thalamic projections from the whisker-sensitive regions of the spinal trigeminal complex in the rat.
J Comp Neurol
420:233-243[Web of Science][Medline].
-
Wang B-R,
Ohara PT
(1993)
Convergent projections of trigeminal afferents from the principal nucleus and subnucleus interpolaris upon rat ventral posteromedial thalamic neurons.
Brain Res
629:253-259[Web of Science][Medline].
-
White EL
(1985)
Terminations of thalamic afferents.
In: Cereb cortex, Vol 5, Sensory-motor areas and aspects of cortical connectivity (Jones EG,
Peters AJ,
eds), pp 271-289. New York: Plenum.
-
Williams MN,
Zahm DS,
Jacquin MF
(1994)
Differential foci and synaptic organization of the principal and spinal trigeminal projections to the thalamus in the rat.
Eur J Neurosci
6:429-453[Web of Science][Medline].
-
Wong-Riley MTT
(1979)
Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry.
Brain Res
171:11-28[Web of Science][Medline].
-
Woolston DC,
LaLonde JR,
Gilson JM
(1982)
Comparison of response properties of cerebellar and thalamic-projecting interpolaris neurons.
J Neurophysiol
48:160-173[Free Full Text].
Copyright © 2000 Society for Neuroscience 0270-6474/00/20197455-08$05.00/0
This article has been cited by other articles:
|
|
|
|
 
R. Masri, R. L. Quiton, J. M. Lucas, P. D. Murray, S. M. Thompson, and A. Keller
Zona Incerta: A Role in Central Pain
J Neurophysiol,
July 1, 2009;
102(1):
181 - 191.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Furuta, T. Kaneko, and M. Deschenes
Septal Neurons in Barrel Cortex Derive Their Receptive Field Input from the Lemniscal Pathway
J. Neurosci.,
April 1, 2009;
29(13):
4089 - 4095.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. C. Voigt, M. Brecht, and A. R. Houweling
Behavioral Detectability of Single-Cell Stimulation in the Ventral Posterior Medial Nucleus of the Thalamus
J. Neurosci.,
November 19, 2008;
28(47):
12362 - 12367.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. Masri, T. Bezdudnaya, J. C. Trageser, and A. Keller
Encoding of Stimulus Frequency and Sensor Motion in the Posterior Medial Thalamic Nucleus
J Neurophysiol,
August 1, 2008;
100(2):
681 - 689.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Chakrabarti, M. Zhang, and K. D. Alloway
MI Neuronal Responses to Peripheral Whisker Stimulation: Relationship to Neuronal Activity in SI Barrels and Septa
J Neurophysiol,
July 1, 2008;
100(1):
50 - 63.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Hirata and M. A. Castro-Alamancos
Cortical Transformation of Wide-Field (Multiwhisker) Sensory Responses
J Neurophysiol,
July 1, 2008;
100(1):
358 - 370.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Bokor, L. Acsady, and M. Deschenes
Vibrissal Responses of Thalamic Cells That Project to the Septal Columns of the Barrel Cortex and to the Second Somatosensory Area
J. Neurosci.,
May 14, 2008;
28(20):
5169 - 5177.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. D. Alloway
Information Processing Streams in Rodent Barrel Cortex: The Differential Functions of Barrel and Septal Circuits
Cereb Cortex,
May 1, 2008;
18(5):
979 - 989.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Urbain and M. Deschenes
A New Thalamic Pathway of Vibrissal Information Modulated by the Motor Cortex
J. Neurosci.,
November 7, 2007;
27(45):
12407 - 12412.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. J. Simons, G. E. Carvell, H. T. Kyriazi, and R. M. Bruno
Thalamocortical Conduction Times and Stimulus-Evoked Responses in the Rat Whisker-to-Barrel System
J Neurophysiol,
November 1, 2007;
98(5):
2842 - 2847.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Furuta, K. Nakamura, and M. Deschenes
Angular Tuning Bias of Vibrissa-Responsive Cells in the Paralemniscal Pathway
J. Neurosci.,
October 11, 2006;
26(41):
10548 - 10557.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. Derdikman, C. Yu, S. Haidarliu, K. Bagdasarian, A. Arieli, and E. Ahissar
Layer-Specific Touch-Dependent Facilitation and Depression in the Somatosensory Cortex during Active Whisking.
J. Neurosci.,
September 13, 2006;
26(37):
9538 - 9547.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
F. Oury, Y. Murakami, J.-S. Renaud, M. Pasqualetti, P. Charnay, S.-Y. Ren, and F. M. Rijli
Hoxa2- and Rhombomere-Dependent Development of the Mouse Facial Somatosensory Map
Science,
September 8, 2006;
313(5792):
1408 - 1413.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. E. Kwegyir-Afful and A. Keller
Response Properties of Whisker-Related Neurons in Rat Second Somatosensory Cortex
J Neurophysiol,
October 1, 2004;
92(4):
2083 - 2092.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Timofeeva, P. Lavallee, D. Arsenault, and M. Deschenes
Synthesis of Multiwhisker-Receptive Fields in Subcortical Stations of the Vibrissa System
J Neurophysiol,
April 1, 2004;
91(4):
1510 - 1515.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Fox, N. Wright, H. Wallace, and S. Glazewski
The Origin of Cortical Surround Receptive Fields Studied in the Barrel Cortex
J. Neurosci.,
September 10, 2003;
23(23):
8380 - 8391.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
B. S. Minnery, R. M. Bruno, and D. J. Simons
Response Transformation and Receptive-Field Synthesis in the Lemniscal Trigeminothalamic Circuit
J Neurophysiol,
September 1, 2003;
90(3):
1556 - 1570.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. P. Killackey and S. M. Sherman
Corticothalamic Projections from the Rat Primary Somatosensory Cortex
J. Neurosci.,
August 13, 2003;
23(19):
7381 - 7384.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Deschenes, E. Timofeeva, and P. Lavallee
The Relay of High-Frequency Sensory Signals in the Whisker-to-Barreloid Pathway
J. Neurosci.,
July 30, 2003;
23(17):
6778 - 6787.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. A. Swadlow, A. G. Gusev, and T. Bezdudnaya
Activation of a Cortical Column by a Thalamocortical Impulse
J. Neurosci.,
September 1, 2002;
22(17):
7766 - 7773.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Varga, A. Sik, P. Lavallee, and M. Deschenes
Dendroarchitecture of Relay Cells in Thalamic Barreloids: A Substrate for Cross-Whisker Modulation
J. Neurosci.,
July 15, 2002;
22(14):
6186 - 6194.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
TOP
ABSTRACT
INTRODUCTION
Compound via MeSH
