Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6
Ascending sensory information is conveyed from the thalamus to layers 4 and 6 of the sensory cortical areas. Interestingly, receptive field properties of cortical layer-6 neurons differ from those in layer 4. Do such differences reflect distinct inheritance patterns from the thalamus, or are they...
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Lee, C.C. Imaizumi, K. 2019-02-17T18:28:41Z 2019-02-17T18:28:41Z 2013 Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 / C.C. Lee, K. Imaizumi // Нейрофизиология. — 2013. — Т. 45, № 5. — С. 445-455. — Бібліогр.: 81 назв. — англ. 0028-2561 https://nasplib.isofts.kiev.ua/handle/123456789/148230 612.825.1+612.826 Ascending sensory information is conveyed from the thalamus to layers 4 and 6 of the sensory cortical areas. Interestingly, receptive field properties of cortical layer-6 neurons differ from those in layer 4. Do such differences reflect distinct inheritance patterns from the thalamus, or are they derived instead from local cortical circuits? To distinguish between these possibilities, we utilized in vitro slice preparations containing the thalamo-cortical pathways of the auditory and somatosensory systems. Responses from neurons in layers 4 and 6 that resided in the same column were recorded using whole-cell patch clamp. Laserscanning photostimulation via uncaging of glutamate in the thalamus and cortex was used to map the functional topography of thalamo-cortical and intracortical inputs to each layer. In addition, we assessed the functional divergence of thalamo-cortical inputs by optical imaging of flavoprotein autofluorescence. We found that the thalamo-cortical inputs to layers 4 and 6 originated from the same thalamic domain, but the intracortical projections to the same neurons differed dramatically. Our results suggest that the intracortical projections, rather than the thalamic inputs, to each layer contribute more to the differences in their receptive field properties Висхідний потік сенсорної інформації передається з таламуса до шарів 4 та 6 сенсорних кортикальних зон. Цікавим є те, що властивості рецептивних полів у нейронів кортикального шару 6 є відмінними від таких у шарі 4. Чи відображають дані відмінності специфічні природжені патерни таламічних зв’язків або вони зумовлені специфікою локальних кортикальних нейронних мереж? Щоб зробити вибір між такими можливостями, ми використали слайсові препарати in vitro, котрі вміщували таламо-кортикальні шляхи слухової та соматосенсорної систем. Застосовуючи методику петчклемп у конфігурації «ціла клітина», ми відводили відповіді нейронів шарів 4 та 6, розташованих в одній і тій самій кортикальній колонці. Для отримання карт функціональної топографії таламо-кортикальних та інтракортикальних входів, до кожного із шарів ми використовували методику лазерної скануючої стимуляції, що забезпечувала вивільнення глутамату в таламусі та корі. Окрім того, ми оцінювали функціональну дивергенцію таламо-кортикальних входів за допомогою візуалізації аутофлуоресценції флавопротеїнів. Було виявлено, що таламо-кортикальні входи до шарів 4 та 6 походили від ідентичних таламічних регіонів, тоді як інтракортикальні проекції до одних і тих самих нейронів значно відрізнялися. Наші результати примушують думати, що саме інтракортикальні проекції того або іншого шару, а не таламічні входи в більшій мірі визначають відмінності відповідних рецептивних полів у згаданих шарах. We thank B. Suter and B. Theyel for their assistance with custom analysis software, X. Wu for assistance with confocal microscopy, and P. Venkatadri and C. Burgess for technical assistance. This work was supported by the NIH/NIDCD grant R03 DC 11361, SVM USDA CORP grants LAV3300 and LAV3202, NSF-LA EPSCoR grant PFUND276, and Louisiana Board of Regents RCS grant RD-A-09. en Інститут фізіології ім. О.О. Богомольця НАН України Нейрофизиология Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 Функціональна конвергенція таламічних та інтракортикальних проекцій до кортикальних шарів 4 та 6 Article published earlier |
| institution |
Digital Library of Periodicals of National Academy of Sciences of Ukraine |
| collection |
DSpace DC |
| title |
Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 |
| spellingShingle |
Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 Lee, C.C. Imaizumi, K. |
| title_short |
Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 |
| title_full |
Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 |
| title_fullStr |
Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 |
| title_full_unstemmed |
Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 |
| title_sort |
functional convergence of thalamic and intrinsic projections to cortical layers 4 and 6 |
| author |
Lee, C.C. Imaizumi, K. |
| author_facet |
Lee, C.C. Imaizumi, K. |
| publishDate |
2013 |
| language |
English |
| container_title |
Нейрофизиология |
| publisher |
Інститут фізіології ім. О.О. Богомольця НАН України |
| format |
Article |
| title_alt |
Функціональна конвергенція таламічних та інтракортикальних проекцій до кортикальних шарів 4 та 6 |
| description |
Ascending sensory information is conveyed from the thalamus to layers 4 and 6 of the
sensory cortical areas. Interestingly, receptive field properties of cortical layer-6 neurons
differ from those in layer 4. Do such differences reflect distinct inheritance patterns from
the thalamus, or are they derived instead from local cortical circuits? To distinguish between
these possibilities, we utilized in vitro slice preparations containing the thalamo-cortical
pathways of the auditory and somatosensory systems. Responses from neurons in layers 4
and 6 that resided in the same column were recorded using whole-cell patch clamp. Laserscanning photostimulation via uncaging of glutamate in the thalamus and cortex was used to
map the functional topography of thalamo-cortical and intracortical inputs to each layer. In
addition, we assessed the functional divergence of thalamo-cortical inputs by optical imaging
of flavoprotein autofluorescence. We found that the thalamo-cortical inputs to layers 4 and
6 originated from the same thalamic domain, but the intracortical projections to the same
neurons differed dramatically. Our results suggest that the intracortical projections, rather
than the thalamic inputs, to each layer contribute more to the differences in their receptive
field properties
Висхідний потік сенсорної інформації передається з таламуса до шарів 4 та 6 сенсорних кортикальних зон. Цікавим є
те, що властивості рецептивних полів у нейронів кортикального шару 6 є відмінними від таких у шарі 4. Чи відображають дані відмінності специфічні природжені патерни таламічних зв’язків або вони зумовлені специфікою локальних
кортикальних нейронних мереж? Щоб зробити вибір між такими можливостями, ми використали слайсові препарати in vitro, котрі вміщували таламо-кортикальні шляхи слухової
та соматосенсорної систем. Застосовуючи методику петчклемп у конфігурації «ціла клітина», ми відводили відповіді нейронів шарів 4 та 6, розташованих в одній і тій самій
кортикальній колонці. Для отримання карт функціональної
топографії таламо-кортикальних та інтракортикальних входів, до кожного із шарів ми використовували методику лазерної скануючої стимуляції, що забезпечувала вивільнення глутамату в таламусі та корі. Окрім того, ми оцінювали
функціональну дивергенцію таламо-кортикальних входів за
допомогою візуалізації аутофлуоресценції флавопротеїнів.
Було виявлено, що таламо-кортикальні входи до шарів 4 та
6 походили від ідентичних таламічних регіонів, тоді як інтракортикальні проекції до одних і тих самих нейронів значно відрізнялися. Наші результати примушують думати, що
саме інтракортикальні проекції того або іншого шару, а не
таламічні входи в більшій мірі визначають відмінності відповідних рецептивних полів у згаданих шарах.
|
| issn |
0028-2561 |
| url |
https://nasplib.isofts.kiev.ua/handle/123456789/148230 |
| citation_txt |
Functional Convergence of Thalamic and Intrinsic Projections to Cortical Layers 4 and 6 / C.C. Lee, K. Imaizumi // Нейрофизиология. — 2013. — Т. 45, № 5. — С. 445-455. — Бібліогр.: 81 назв. — англ. |
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AT leecc functionalconvergenceofthalamicandintrinsicprojectionstocorticallayers4and6 AT imaizumik functionalconvergenceofthalamicandintrinsicprojectionstocorticallayers4and6 AT leecc funkcíonalʹnakonvergencíâtalamíčnihtaíntrakortikalʹnihproekcíidokortikalʹnihšarív4ta6 AT imaizumik funkcíonalʹnakonvergencíâtalamíčnihtaíntrakortikalʹnihproekcíidokortikalʹnihšarív4ta6 |
| first_indexed |
2025-11-25T18:53:12Z |
| last_indexed |
2025-11-25T18:53:12Z |
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| fulltext |
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5 445
UDC 612.825.1+612.826
C. C. LEE1 and K. IMAIZUMI1
FUNCTIONAL CONVERGENCE OF THALAMIC AND INTRINSIC PROJECTIONS
TO CORTICAL LAYERS 4 AND 6
Received June 06, 2013.
Ascending sensory information is conveyed from the thalamus to layers 4 and 6 of the
sensory cortical areas. Interestingly, receptive field properties of cortical layer-6 neurons
differ from those in layer 4. Do such differences reflect distinct inheritance patterns from
the thalamus, or are they derived instead from local cortical circuits? To distinguish between
these possibilities, we utilized in vitro slice preparations containing the thalamo-cortical
pathways of the auditory and somatosensory systems. Responses from neurons in layers 4
and 6 that resided in the same column were recorded using whole-cell patch clamp. Laser-
scanning photostimulation via uncaging of glutamate in the thalamus and cortex was used to
map the functional topography of thalamo-cortical and intracortical inputs to each layer. In
addition, we assessed the functional divergence of thalamo-cortical inputs by optical imaging
of flavoprotein autofluorescence. We found that the thalamo-cortical inputs to layers 4 and
6 originated from the same thalamic domain, but the intracortical projections to the same
neurons differed dramatically. Our results suggest that the intracortical projections, rather
than the thalamic inputs, to each layer contribute more to the differences in their receptive
field properties.
Keywords: thalamus, cortex, auditory, somatosensory, intracortical circuits,
photostimulation
INTRODUCTION
In the sensory forebrain, thalamo-cortical axons
branch and synapse in layers 4 and 6 of their target
cortical areas [1-4]. These branched projections enable
ascending sensory information to be conveyed directly
and in parallel to each cortical layer. Supporting such
parallel streams, the short-term synaptic plasticity
of thalamo-cortical inputs to both layers 4 and 6 are
similar, exhibiting depressing postsynaptic responses
to repetitive electrical stimulation [5-9] similar
to those observed at other synapses in the sensory
forebrain [10-12].
Interestingly, despite the direct nature of the
thalamo-cortical inputs to these layers, receptive
field properties in layer 6 are distinct from those in
layer 4 [13-18]. For example, spectral and temporal
modulation preferences differ between layers in the
auditory cortex,, with layer-6 units responding to
1 Department of Comparative Biomedical Sciences, LSU School of Veterinary
Medicine, Baton Rouge, Louisiana, USA
Correspondence should be addressed to: C. C. Lee
(e-mail: cclee@lsu.edu)
broader spectral and lower temporal modulations
compared to those in layer 4 [14]. Tuning preferences
likewise vary among layers in the visual [13, 16] and
somatosensory [15, 17] cortices. This arrangement
poses a dilemma, and it, therefore, remains an open
question whether such differences in receptive field
properties among layers reflect distinct inheritance
patterns from the thalamus, or these differences are
derived instead from local cortical circuits or another
mechanism.
Indeed, all layers of the cortex receive convergent
inputs from a wide constellation of intrinsic cortical
sources, which comprise over half of the total number
of convergent inputs from combined thalamic and
cortical sources [19-21]. Intrinsic synapses outnumber
those arising from thalamic sources. In the visual
cortex, for example, thalamic synapses comprise
only about 5% of the total innervation on layer-4
thalamorecipient neurons [22, 23]. Thus, the intricate
and prolific connections from local cortical circuits
are potentially poised to refine and modulate the
information arriving through the ascending thalamo-
cortical streams [12, 24-26].
Therefore, to explore the relative contributions of
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5446
C. C. LEE and K. IMAIZUMI
thalamic and intracortical projections to layers 4 and
6, we utilized in vitro slice preparations containing the
intact thalamo-cortical pathways of the auditory and
somatosensory systems. Responses from neurons in
layers 4 and 6 that resided in the same column were
recorded using whole-cell patch clamp. Laser-scanning
photostimulation via uncaging of glutamate in the
thalamus and cortex was used to map the functional
topography of thalamo-cortical and intracortical
inputs. In addition, optical imaging of flavoprotein
autofluorescence in the cortex in response to thalamic
stimulation was used to assess the spatial and temporal
pattern of activity in layers 4 and 6 following thalamic
stimulation.
METHODS
Slice Preparation. Thalamo-cortical slices were
prepared from BALB/c mice (age p11-p18). Animals
were first deeply anesthetized by isofluorane, as
assessed by cessation of withdrawal reflexes to strong
toe-pinches. Following decapitation, the brains were
quickly dissected and submerged in cool oxygenated
artificial cerebrospinal fluid (ACSF; composition in
mM: NaCl, 125, NaHCO3, 25, KCl, 3, NaH2PO4, 1.25,
MgCl2, 1, CaCl2, 2, and glucose, 25). Brains were then
blocked to preserve the thalamo-cortical projections to
either the primary auditory cortex (A1) [27] or primary
somatosensory cortex (S1) [28]. The blocked brains
were affixed to a stage with instant glue adhesive;
then, 500-µm-thick sections were collected in cold
oxygenated ACSF using a vibratome (World Precision
Instruments, USA). Collected slices were transferred
to a holding chamber for 1 h at 32°C in ACSF and then
moved to a recording chamber perfused with ACSF
at 32°C on a modified microscope stage (Siskiyou,
Grants Pass, USA).
Recording, Photostimulation, and Optical
Imaging. Neurons were visualized under DIC optics
on an Olympus BX-51 upright microscope equipped
with a U-DPMC intermediate magnification changer
with 0.25× and 4× intermediate lenses (Olympus
America, USA), rear-mounted with a Hitachi KP-
M1AN camera (Hitachi, USA) and front-mounted
with a Retiga-EX camera (QImaging, Canada). Whole-
cell voltage clamp recordings were made using the
Multiclamp 700B amplifier and pCLAMP software
(Molecular Devices, USA) or Ephus software (Janelia
Farms, USA). Recordings were performed in the
voltage clamp mode using a potassium intracellular
solution (in mM: K-gluconate, 135, NaCl, 7, HEPES,
10, Na2ATP, 1–2, GTP, 0.3, MgCl2, 2; pH 7.3 and
290 mOsm). Cytoarchitectural and anatomical markers
determined laminar positions of the neurons, as we
have previously demonstrated [9, 24, 25]. The lower
border of layer 4 was apparent by the transition
from small densely packed neurons to larger, more
sparsely packed neurons in layer 5 [29, 30]. In the
somatosensory slices, layer 4 was readily identifiable
by the canonical barrel and septal regions [9, 28].
Similarly, the borders of layer 6 were determined by
the white matter and transition to the large, sparsely
packed neurons in layer 5 [9, 24, 25]. Depolarizing
current injections were used to determine spiking
characteristics of the recorded neurons. Regular-
spiking (RS) neurons were classified as firing at slow
adapting frequencies (<30 sec–1) with small and slow
afterhyperpolarizations (AHPs; 5–10 mV), while
fast-spiking (FS) neurons were classified according
to higher maximal firing rates (>30 sec–1) and large
and fast AHPs (10–15 mV). The acquired data were
recorded and digitized using a Digidata 1440A
acquisition board (Molecular Devices) or a National
Instruments BNC 2090 terminal block (National
Instruments, USA) and then stored in a computer for
subsequent analysis.
Laser-scanning photostimulation (LSPS) with caged
glutamate was used to map the thalamic and cortical
regions eliciting EPSCs in the recorded layer-4 or
-6 neurons of interest [9, 25, 31]. After patching, a
recirculating ACSF bath containing nitroindolinyl(NI)-
caged glutamate (0.37 mM; Sigma-RBI, USA) was
switched in place of the regular ACSF bath. Direct
responses to photostimulation were determined by
using a solution containing caged glutamate in a
low-Ca2+ (0.2 mM) / high-Mg2+ (6 mM) ACSF solution
with TTX (1 μM), and synaptic responses were
estimated by subtraction. Photolysis of the caged
glutamate was done focally with a pulsed UV laser
(DPSS Lasers, Inc., USA). Custom software (Ephus)
written in MATLAB (MathWorks Inc., USA) was
used to control the galvanometer mirror positioning
of the laser beam for photostimulation and to analyze
the data [32]. We used a 16×16 stimulation array
with 80 µm spacing between adjacent rows and
columns. Previous controls demonstrated that laser
uncaging of glutamate elicits action potentials (APs)
within 40-50 µm with respect to the soma [25, 33].
The mean EPSCs elicited from three map repetitions
were averaged, and the interpolated plots were
superimposed on photomicrographs corresponding to
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5 447
FUNCTIONAL CONVERGENCE OF THALAMIC AND INTRINSIC PROJECTIONS
the stimulation sites. Thalamic and laminar boundaries
were determined from cytoarchitectural landmarks in
the DIC images [9, 33]. The ventrobasal (VB) nucleus
was discerned as a dark crescent-shaped structure
with fibers traversing it laterally [9, 28]. The medial
geniculate body (MGB) was visualized as an almond-
shaped structure that was lighter in brightness than the
laminated structure of the lateral geniculate nucleus
(LGN) rostrally and the darker appearance of the
ventrobasal complex medially [9, 27, 33]. The thalamic
region projecting to a given recorded layer-6 neuron
was measured from the thalamic photostimulation
sites that elicited EPSCs and normalized to the region
eliciting EPSCs of the recorded layer-4 neuron in the
same column. The averaged mean EPSCs were totaled
from each stimulation site in both the thalamus and
cortex for a given neuron to determine the normalized
contribution (%) from each thalamic and intracortical
source. Statistical comparisons of distributions
of numerical data were performed using StatPlus
(AnalystSoft, USA).
Metabolic activity in response to thalamic
stimulation was measured with the front-mounted
Retiga-EX camera (QImaging) by capturing green
light (~510–540 nm) generated by mitochondrial
f lavoproteins in the presence of blue l ight
(~450–490 nm) [34]. Optical images were captured
over 12-sec runs using Streampix 5.13 (Norpix
Inc., Canada) following electrical stimulation in the
thalamic regions projecting to the cortical areas being
imaged. Electrical stimulation was performed using
a concentric bipolar electrode (WPI, USA) to deliver
a repetitive stimulation train of 100 sec–1 lasting
for 500 msec and controlled by a Master-9 pulse
generator (A.M.P.I., Israel) at stimulation intensities
of 50-200 µA adjusted using an A365R stimulus
isolator (World Precision Instruments, USA). The
image exposure time ranged from 80 to 150 msec.
Images were taken at a 4× magnification and processed
using custom software written to run on Matlab
[34, 35]. Spatial and temporal signal profiles were
analyzed using ImageJ (NIH, USA). Defined regions
of interest (ROIs) were used to measure changes in
the pixel intensity within or across cortical layers.
For temporal analyses, ROIs in the center of maximal
activation in layers 4 or 6 in the same column were
chosen, and the change in intensity across image
stacks (time) was plotted for each layer.
In vitro tract-tracing. Following physiological
recordings, selected slices were transferred for
post-fixation to a 4% paraformaldehyde solution
(Electron Microscopy Sciences, USA) in 10 mM
phosphate-buffered saline (pH 7.3). DiI crystals
(Life Technologies, USA) were carefully placed with
a needle into the thalamic nuclei (VB or MGB) of
thalamocortical slices under a dissecting microscope
(AmScope, USA). Slices were covered with aluminum
foil and incubated in the dark at room temperature for
2-3 months. Following adequate lipophilic diffusion of
DiI into thalamo-cortical fibers, slices were mounted
between two pieces of coverglass with Vectashield
hard set mounting medium (Vector Labs, USA).
DiI-labeled fibers were then visualized using a Leica
TCS SP2 confocal laser-scanning microscope (Leica
Microsystems, USA) housed in the microscopy center
at the LSU School of Veterinary Medicine. Acquired
images were analyzed using ImageJ (NIH).
RESULTS
In order to assess the connectivity of the
thalamocortical slice preparations, DiI crystals were
placed into the respective thalamic nuclei in the
auditory and somatosensory slices (Figs. 1, 2). In the
auditory preparations (Fig. 1), thalamo-cortical fibers
F i g. 1. Thalamo-cortical projections in an auditory slice preparation.
A) Placement of DiI crystals in the medial geniculate body (MGB).
Labeled fibers traverse toward the thalamic reticular nucleus (TRN)
continuing onward towards the primary auditory cortex (A1). B)
Thalamo-cortical fiber terminations in the A1. C) Labeled axonal
fibers and retrogradely labeled cells in layer 6. D) Labeled fibers
extending to layer 4.
Р и с. 1. Таламо-кортикальні проекції в слайс-препараті слухової
кори.
L
C
L
C
MGB
TRN
BIC
A1
Hip
Hip
A1
TRN
1
2/3
4
5
6
2/3
4
5
5
6
4
500 mµ
100 mµ 6
A
C
B
D
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5448
C. C. LEE and K. IMAIZUMI
F i g. 2. DiI tracing of projections in the somatosensory thalamo-
cortical slice. A) DiI crystal placement in the ventroposterior
nucleus (VP) and fibers traversing to the primary somatosensory
cortex (S1). B) Fiber terminations in the primary somatosensory
cortex. C) Axonal fibers and retrogradely labeled cells in layer 6. D)
Labeled fibers extending to layer 4.
Р и с. 2. Виявлення проекцій у слайсі таламуса і соматосенсорної
кори.
F i g. 3. Areal and laminar activation pattern of flavoprotein autofluorescence (FA) in the auditory cortex (zone A1) following electrical
stimulation of the MGB. A) FA image of the A1 at the time of maximal autofluorescence following thalamic stimulation. B) Laminar FA
profile in the A1 at the time of maximal autofluorescence. C) Areal profile of FA responses across layers 4 and 6. D) Time course of a cortical
FA response in layers 4 and 6 of the A1.
Р и с. 3. Зонний і ламінарний патерни аутофлуоресценції флавопротеїнів (FA) в слуховій корі (зона А1) після електричної стимуляції
медіального колінчастого тіла.
originated from the medial geniculate body (MGB)
and traversed rostrally towards the thalamic reticular
nucleus (TRN) (Fig. 1A). There they ramified profusely
before continuing laterally towards the cerebral
cortex (Fig. 1B). As these fibers approached the
primary auditory cortex (A1), they rerouted caudally
before entering the deep cortical layers (Fig. 1B, C).
Upon entering the deep layers, the fibers branched
in layer 6 before continuing towards the upper
cortical layers (Fig. 1D). This pattern was similar,
but somewhat more continuous, to that described
earlier [27]. In the somatosensory slice preparations
(Fig. 2), thalamo-cortical fibers traversed laterally
from the ventrobasal complex to the TRN before
curving dorsally towards the primary somatosensory
cortex (S1) (Fig. 2A, B), where they formed a distinct
band in layers 4 and 6 of the S1 (Fig. 2C, D). In
both auditory and somatosensory slices, retrogradely
labeled cell somata were observed in layer 6
(Fig 1C, 2C), indicative of the robust feedback
projections from the cortex to the thalamus [36-38].
To further characterize the thalamo-cortical
projections in these slice preparations, we utilized
optical imaging of flavoprotein autofluorescence (FA)
A 500 mµ
D
L
D
L100 mµ
B
C D
VP
TRN
S1
S1 1
2/3
4
5
6
5
6
2/3
4
5
6
20 10.5 1.5
100
0
25
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75
mm
C
2 4 6%
250 mµ
L
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A
1
2/3
4
5
6
wm
0
0 25
0.25
0.5
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1
1.25
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50 10075 %
B
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4
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6
layer
0 2 4 6 8
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–50 sec
D
stim
Hip
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NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5 449
FUNCTIONAL CONVERGENCE OF THALAMIC AND INTRINSIC PROJECTIONS
in the cortex following electrical stimulation of the
thalamus (Figs. 3, 4). We found robust FA activation
in the primary auditory and somatosensory cortices,
which peaked approximately 1 sec following thalamic
stimulation and was observed in both layers 4 and 6
(Figs. 3D, 4D). At the time of maximal activation,
robust autofluorescence was especially visible in
layers 3 and 4 of the auditory cortex (n = 3), with
weaker activation in lower layers, including layer 6
(Fig. 3A, B). Despite the difference in the intensity
among layers 4 and 6 (Fig. 3B), the areal extent of
the activation was similar for both layers 4 and
6, originating at similar rostral-caudal extremes
and cresting at the same rostral-caudal location
(Fig. 3A, C). In the primary somatosensory cortex
(n = 3), autofluorescence was most prevalent in the
barrel regions of layer 4 and decreased in the upper
and lower cortical layers (Fig. 4A, B). The barrel
architecture resulted in a periodic areal pattern of
activation across the S1 in layer 4, which was not
evident in layer 6 (Fig. 4A, C).
We further sought to compare the functional
convergence of inputs to pairs of neurons in
layers 4 and 6 in the auditory and somatosensory
systems using whole-cell patch clamp recordings
of cortical neurons in response to laser-scanning
photostimulation (LSPS) via uncaging of glutamate
(Figs. 5, 6) [9, 24, 25, 33]. In each slice preparation,
we recorded from regular-spiking (RS) neurons in
layers 4 and 6 (A1, n = 6 pairs; S1, n = 10 pairs)
residing along a presumptive cortical column, as
determined by cytoarchitectural and anatomical
boundaries. We then mapped the topography of LSPS-
evoked EPSCs in the thalamic and cortical areas
projecting to the recorded neuron. In both the auditory
(Fig. 5) and somatosensory (Fig. 6) slices, we found
that the areal extent and location of the thalamus
that elicited EPSCs in layer-4 (Figs. 5A, 6A) and
layer-6 (Figs. 5B, 6B) neurons were similar to each
other (Figs. 5E, 6E) (layer 6 to 4 ratio: A1, 99 ± 43%;
S1, 108 ± 31%; combined, 103 ± 35%). The mean
evoked currents to layer 6 were, however, weaker than
F i g. 4. Areal and laminar activation pattern of flavoprotein autofluorescence (FA) in the somatosensory cortex (area S1) following
electrical stimulation of the VPm. A) FA image of the S1 at the time of maximal autofluorescence following thalamic stimulation. B)
Autofluorescence responses across layers at the time of maximal FA response. C) Areal profile of FA responses across layers 4 and 6 in the
S1. D) Time course of the cortical FA response in layers 4 and 6 of the S1.
Р и с. 4. Зонний і ламінарний патерни аутофлуоресценції флавопротеїнів у соматосенсорній корі (зона S1) після електричної
стимуляції заднього вентрально-медіального ядра таламуса (VPm).
2 4 6%
250 mµ
D
L
A
1
2/3
4
5
6
wm
0
0 25
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0.75
1
1.25
mm
50 10075 %
1
2/3
4
5
6
layer
B
20 10.5 1.5
mm
100
% %
0
25
50
75
C
0 2 4 6 8 10
sec
0
50
100
–50
D
stim
l.4
l.6
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5450
C. C. LEE and K. IMAIZUMI
F i g. 5. Auditory thalamo-cortical and
intracortical inputs to layers 4 and 6 of the
A1. A-D) Average LSPS plots of mean
EPSCs recorded in a layer-4 neuron (A,C)
or a layer-6 neuron (B,D) in response to
photostimulation of the medial geniculate
body (MGB; A-B) or auditory cortex (A1;
C-D). Filled regions in C and D illustrate
direct response areas of the recorded neurons.
E) Mean thalamic area and mean total evoked
current in layer 6 normalized to that of
layer-4 neurons recorded in the same column.
F) Mean percentage of total current elicited
from the MGB and layers 2-6 in either the
layer-4 neuron (blue) or layer-6 neuron (red).
Р и с. 5. Слухові таламо-кортикальні та
внутрішньокортикальні входи до шарів 4
і 6 зони А1.
F i g. 6. Somatosensory thalamo-cortical and
intracortical inputs to layers 4 and 6 of the S1.
A-D) Photostimulation of the ventral posterior
medial nucleus (VPm; A-B) or primary
somatosensory barrel cortex (area SI; C-D).
Plots illustrate averaged mean EPSCs . Filled
regions in C and D illustrate direct response
areas of the recorded neurons (E) Mean area
evoking EPSCs in the thalamus and the mean
total evoked current from the VPm in layer
6 normalized to that of layer 4. F) Mean
percentage of total current elicited from the
VPm and layers 2-6 in either the layer-4
neuron (blue) or the layer-6 neuron (red).
Р и с. 6. Соматосенсорні таламокорти-
кальні та внутрішньокортикальні входи до
шарів 4 і 6 зони S1.
–20
–15
–10
–5
0
–10
–8
–6
–4
–2
0
MGB
LGN
Hip
MGB
LGN
Hip
1
23
4
5
6
1
3
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2
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250 mµ pA
250 mµ
L
C
L
CpA
pA
pA
–15
–10
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0
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EPSC Area0
20
40
60
100
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% %
80
MGB L2 L3 L4 L5 L60
10
20
30
40
50
Origin
A B
E F
C D
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–10
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POm
A
VPm
POm
B
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5
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–25
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–15
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01 2
3
4
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6
1 2
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6
pA
pA pA
pA
250 mµ
250 mµ
D
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VPm L2 L3 L4 L5 L6
0
10
20
30
40
50
Origin
l.4 l.6
EPSC Area0
20
40
60
100
120
% %
80
VPl
VPm
VPl
C
E F
D
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5 451
FUNCTIONAL CONVERGENCE OF THALAMIC AND INTRINSIC PROJECTIONS
those to layer 4 (Figs. 5E, 6E) (layer 6 to 4 ratio: A1,
86 ± 24%; S1, 89 ± 19%; combined, 88 ± 21%).
The similar functional topography of the thalamic
inputs contrasted with different input patterns from
intracortical laminar sources to layers 4 and 6. In
general, layer-4 neurons received the bulk of total
evoked current from layer 3 (A1, 29.2 ± 4.6%;
S1, 25.0 ± 6.5%, combined, 26.5 ± 5.9%) and layer 4
(A1, 33.3 ± 2.9%; S1, 42.4 ± 11.5%; combined, 39.0 ±
± 10.0%) (Figs. 5C, F; 6C, F; Table 1). In comparison,
layer 6 received the bulk of evoked current from layer
5 (A1, 29.2 ± 7.3%, S1, 31.8 ± 3.1%; combined, 30.8 ±
± 4.8%) and layer 6 (A1, 44.5 ± 2.1%; S1, 46.9 ±
± 7.2%; combined, 46.0 ± 5.8%) (Figs. 5D, F; 6D,
F; Table 1). The proportion of evoked currents from
these laminar sources to neurons in layers 4 and 6
was statistically different (t-test, p<0.01; Table 1).
In comparison with the thalamic evoked currents,
intracortical sources provided approximately 90%
of the total evoked current, while thalamic sources
contributed less than 10% (Figs. 5F, 6F, 7; Table 1).
DISCUSSION
Ascending thalamo-cortical axons innervate layers
4 and 6 of the primary auditory and somatosensory
cortices [1-4]. Using laser-scanning photostimulation
via uncaging of glutamate to map the functional
convergence of thalamo-cortical inputs, we found that
neurons in layers 4 and 6 in a cortical column receive
functional inputs from the same thalamic region. In
our experiments, we recorded primarily from young
animals whose synaptic properties and connectivity
may be undergoing rapid changes [39-41]. Although
the relative proportion and spatial distribution of
excitatory inputs were similar for all animals in our
study, we did not directly assess convergence from
intracortical inhibitory sources [42, 43], which may
be still developing at this time point [39, 41].
Our results are consistent with previous studies
of the functional topography of the thalamo-
cortical pathways [9, 44, 45]. In their study, Bureau
et al. [44] found that the thalamic inputs from the
lemniscal and paralemniscal nuclei (VPm and POm)
to the somatosensory cortex were interdigitated,
such that POm projected primarily to layer 5a, while
VPm projections to layers 4, 5b, and 6 overlapped
for pairs in the same column. Here, we found a
similar alignment of thalamic projections to layer-4
and layer-6 neurons in the somatosensory barrel
cortex [46], which we also observed in the auditory
thalamo-cortical projections to layers 4 and 6 of A1.
This suggests that a similar topographic principle
organizes the TC projections in both systems, and
this, perhaps, extends to other modalities, such as the
visual system [8].
This pattern of functional convergence revealed
by LSPS mapping of thalamo-cortical projections is
supported by the pattern of divergence revealed by
optical imaging methods [34, 35, 47-57]. Although we
observed that electrical stimulation of the thalamus
resulted in similar temporal patterns of activation
in these layers of the auditory and somatosensory
cortices (also similar to observations in previous
studies [48, 49, 51-54]), the autofluorescence imaging
method that we employed does not enable the fine
temporal discrimination available with voltage-
Table 1. Normalized intensity, %, of mean evoked EPSCs from thalamic and intracortical sources
Таблиця 1. Нормована інтенсивність, %, усереднених ЗПСС, викликаних активацією таламічних та інракортикальних
джерел.
Thalamus Layer 2 Layer 3 Layer 4 Layer 5 Layer 6
Auditory
Layer 4 9.0 ± 5.2 2.5 ± 2.1 29.2 ± 4.6 33.3 ± 2.9 19.1 ± 5.1 6.9 ± 1.0
Layer 6 7.9 ± 6.7 1.3 ± 0.6 4.2 ± 2.5 12.7 ± 3.1 29.2 ± 7.3 44.5 ± 2.1
Somatosensory
Layer 4 9.4 ± 2.9 2.1 ± 2.1 25.0 ± 6.5 42.4 ± 11.5 13.9 ± 6.4 7.2 ± 4.2
Layer 6 8.1 ± 2.3 1.0 ± 0.8 3.0 ± 1.4 9.2 ± 2.7 31.8 ± 3.1 46.9 ± 7.2
Combined
Layer 4 9.2 ± 3.5 2.2 ± 1.9 26.5 ± 5.9 39.0 ± 10.0 15.8 ± 6.2 7.2 ± 3.2
Layer 6 8.1 ± 4.0 1.1 ± 0.7 3.4 ± 1.8 10.5 ± 3.2 30.8 ± 4.8 46.0 ± 5.8
Footnote: Means ± s. d. are shown
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5452
C. C. LEE and K. IMAIZUMI
sensitive dyes, which has revealed possible laminar
latency differences in the auditory cortex [55]. Our
experiments and other previous studies allowed one to
observe robust flavoprotein activation in layers 4 and
6 of the auditory and somatosensory cortices following
thalamic electrical and photostimulation, but typically
with a more prominent activity in layer 6 [35, 47]. Our
finding of relatively weaker activity in layer 6 matches
more closely that observed by Broicher et al. [55],
who used voltage-sensitive dyes and attributed laminar
intensity differences in the A1 to the interaction of
intracortical circuits. Our findings may result from
similar intrinsic mechanisms or methodological ones,
such as the intensity of stimulation and, perhaps, less
antidromic activation of layer-6 cortico-thalamic
neurons. Still, the spatial distribution of activity in
layers 4 and 6 observed in this and previous studies
suggest that feedforward and feedback projections are
likely topographically aligned.
Despite the similar functional topography of the
thalamic inputs, the intracortical inputs to layers 4
and 6 differed from each other. We found that layer 4
received predominant inputs from layers 3 and 4, while
layer 6 received predominant inputs from layers 5 and
6; this is similar to the distributions observed in prior
studies [24, 45, 58-63]. In general, local connectivity
within a layer tends to predominate for each layer [60],
although area-specific differences in local circuits
do exist, such as the respective parallel layer 4- and
5a-projections to layers 2 and 3 in the barrel and septal
regions of the S1 [64, 65] and the asymmetric layer-6
projections to layer 3 in the A1 [45]. These functional
patterns of connectivity align with the morphological
distributions of local circuit axons observed in
layers 4 and 6 of the cat A1 [30, 66-71]. As such,
the laminar differences in local circuit connectivity
provide a morphological basis for the differences in
receptive field properties observed between layers 4
and 6 [13-18]. In this respect, while the same basic
features of the receptive field are inherited from
thalamic sources [72, 73], the subsequent and ongoing
recruitment of local intracortical sources likely
sculpt responsive refinements, e.g., the observed
temporal and modulation preferences in layers 4 and 6
of the A1 [14].
Finally, we found that the thalamo-cortical
projections account for approximately 10% of the total
evoked current in both layers from the thalamic and
intracortical sources. Interestingly, these values are
similar in the magnitude to anatomical estimates of the
proportion of thalamic and intracortical synapses in
layer 4 [22, 23] and the proportion of thalamic neurons
converging across layers [20, 74]. This suggests a
relative equivalence in the efficacy of the thalamic
and intracortical projections, which anatomically
contribute nearly half of the total convergent inputs to
an area [19-23, 75] and is consistent with the notion
of synchronous convergent thalamic synapses that are
weak individually [76]. This arrangement may also
be necessary for the fewer thalamic inputs to activate
the more numerous intracortical projections, which
may amplify and process the ascending signals [52,
77-80], resulting in the observed differences in laminar
receptive field properties among layers. The thalamo-
cortical recruitment of intracortical circuits, both
excitatory and inhibitory, may also account for the
differences in cortical dynamic responses to transient
and sustained activity [81]. Thus, the functional
circuitry of the sensory forebrain is comprised of
convergent thalamo-cortical pathways that lead to
computationally divergent outcomes emerging from
concurrent intracortical projections.
The Institutional Animal Care and Use Committee of the
Louisiana State University School of Veterinary Medicine
approved all experimental procedures.
The authors, Ch. C. Lee and K. Imaizumi, confirm that they
have no conflict of interest.
We thank B. Suter and B. Theyel for their assistance with
custom analysis software, X. Wu for assistance with confocal
microscopy, and P. Venkatadri and C. Burgess for technical
assistance. This work was supported by the NIH/NIDCD
grant R03 DC 11361, SVM USDA CORP grants LAV3300 and
LAV3202, NSF-LA EPSCoR grant PFUND276, and Louisiana
Board of Regents RCS grant RD-A-09.
Ч. Лі1, Л. Імаізумі1
ФУНКЦІОНАЛЬНА КОНВЕРГЕНЦІЯ ТАЛАМІЧНИХ ТА
ІНТРАКОРТИКАЛЬНИХ ПРОЕКЦІЙ ДО КОРТИКАЛЬ-
НИХ ШАРІВ 4 ТА 6
1 Луїзіанський університет ветеринарної медицини, Батон
Рут (США).
Р е з ю м е
Висхідний потік сенсорної інформації передається з таламу-
са до шарів 4 та 6 сенсорних кортикальних зон. Цікавим є
те, що властивості рецептивних полів у нейронів кортикаль-
ного шару 6 є відмінними від таких у шарі 4. Чи відобража-
ють дані відмінності специфічні природжені патерни тала-
мічних зв’язків або вони зумовлені специфікою локальних
кортикальних нейронних мереж? Щоб зробити вибір між та-
кими можливостями, ми використали слайсові препарати in
NEUROPHYSIOLOGY / НЕЙРОФИЗИОЛОГИЯ.—2013.—T. 45, № 5 453
FUNCTIONAL CONVERGENCE OF THALAMIC AND INTRINSIC PROJECTIONS
vitro, котрі вміщували таламо-кортикальні шляхи слухової
та соматосенсорної систем. Застосовуючи методику петч-
клемп у конфігурації «ціла клітина», ми відводили відпові-
ді нейронів шарів 4 та 6, розташованих в одній і тій самій
кортикальній колонці. Для отримання карт функціональної
топографії таламо-кортикальних та інтракортикальних вхо-
дів, до кожного із шарів ми використовували методику ла-
зерної скануючої стимуляції, що забезпечувала вивільнен-
ня глутамату в таламусі та корі. Окрім того, ми оцінювали
функціональну дивергенцію таламо-кортикальних входів за
допомогою візуалізації аутофлуоресценції флавопротеїнів.
Було виявлено, що таламо-кортикальні входи до шарів 4 та
6 походили від ідентичних таламічних регіонів, тоді як ін-
тракортикальні проекції до одних і тих самих нейронів зна-
чно відрізнялися. Наші результати примушують думати, що
саме інтракортикальні проекції того або іншого шару, а не
таламічні входи в більшій мірі визначають відмінності від-
повідних рецептивних полів у згаданих шарах.
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