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The Journal of Neuroscience, January 1, 2003, 23(1):308-316
Functional Subregions in Primary Auditory Cortex Defined by
Thalamocortical Terminal Arbors: An Electrophysiological and
Anterograde Labeling Study
David S.
Velenovsky1,
Justin S.
Cetas1,
Robin O.
Price1,
Donal G.
Sinex2, and
Nathaniel T.
McMullen1
1 Department of Cell Biology and Anatomy, University of
Arizona College of Medicine, Tucson, Arizona 85724, and
2 Department of Speech and Hearing Science, Arizona State
University, Tempe, Arizona 85287
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ABSTRACT |
Several functional maps have been described in primary auditory
cortex, including those related to frequency, tuning, latency, binaurality, and intensity. Many of these maps are arranged in a
discontinuous or patchy manner. Similarly, thalamocortical projections arising from the ventral division of the medial geniculate body to the
primary auditory cortex are also patchy. We used anterograde labeling
and electrophysiological methods to examine the relationship between
thalamocortical patches and auditory cortical maps. Biotinylated dextran-amine was deposited into physiologically characterized sites
in the ventral division of the medial geniculate body of New Zealand
white rabbits. Approximately 7 d later, the animal was
again anesthetized and the ipsilateral auditory cortex was mapped with
tungsten microelectrodes. Multi-unit physiological data were obtained
for the following characteristics: best frequency (BF), binaurality,
response type, latency, sharpness of tuning, and threshold.
Immunocytochemical methods were used to reveal the injection site in
the ventral division of the medial geniculate body as well as the
anterogradely labeled thalamocortical afferents in the auditory cortex.
In 86% of the cases (12 of 14), entry into a thalamocortical patch was
associated with a marked change in physiological responses. A
consistent BF and binaural class were usually observed within a patch.
The patches appear to innervate distinct functional regions coding
frequency and binaurality. A model is presented showing how patchy
thalamocortical projections participate in the formation of tonotopic
and binaural maps in primary auditory cortex.
Key words:
medial geniculate body; audition; neocortex; frequency map; thalamus; patches
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Introduction |
The topographic representation of
peripheral sensory receptors in mammalian sensory systems results in a
systematic representation or functional map in sensory cortex (Marshall
et al., 1941 ; Hubel and Wiesel, 1962; Merzenich et al., 1973; Hubel and
Wiesel, 1977). The first tonotopic auditory neocortical map was
demonstrated by Woolsey and Walzl (1942) in the form of a cochleotopic
organization in the primary auditory cortex (AI) of the cat.
Other functional maps in AI include binaural interaction bands (Imig
and Adrian, 1977; Middlebrooks et al., 1980), threshold/intensity
(Tunturi, 1950; Schreiner et al., 1992), and sharpness of tuning
(Schreiner and Mendelson, 1990). Interestingly, these maps are patchy
or discontinuous in their distribution relative to the frequency map
(Merzenich et al., 1973; Brugge and Imig, 1978; Middlebrooks et al.,
1980; Reale and Imig, 1980; Redies et al., 1989; Schreiner, 1991, 1992;
Schreiner et al., 1992, 2000; Mendelson et al., 1993, 1997; Fitzpatrick
et al., 1998).
Ascending auditory signals reach AI via projections from the ventral
division of the medial geniculate body (MGV) (Mesulam and
Pandya, 1973; Sousa-Pinto, 1973; Jones and Burton, 1976; Winer et al.,
1977; Imig and Morel, 1983; Middlebrooks and Zook, 1983; LeDoux et al.,
1985). Anterograde studies of MGV projections have revealed the
existence of a discontinuous or patchy projection of afferent axons
from the MGV to layers III/IV of auditory cortex (McMullen and de
Venecia, 1993; Romanski and LeDoux, 1993; de Venecia and McMullen,
1994; Cetas et al., 1999). Patchy thalamocortical (TC) afferents
to the cortex have been described in a variety of species, including
the rat, rabbit, ferret, cat, and macaque (Winer et al., 1977;
Angelucci et al., 1993; Romanski and LeDoux, 1993; Hashikawa et al.,
1995; Huang and Winer, 2000). Some insight into the nature of TC
patches has come from studies involving the calcium-binding protein
parvalbumin (PV) (Hendry et al., 1989; Morino-Wannier et al., 1992;
McMullen et al., 1994; de Venecia et al., 1995, 1998; Jones et al.,
1995; Molinari et al., 1995). TC patches coexist with PV-positive
patches in AI (de Venecia et al., 1998). In addition, the MGV is
intensely PV-positive in many species (Hashikawa et al., 1991; Vater
and Braun, 1994; de Venecia et al., 1995; Molinari et al., 1995;
Cruikshank et al., 2001), and PV-positive relay neurons in the MGV
project to AI (de Venecia et al., 1998). Thus, at least some of the TC
patches arising from the MGV may represent a chemically coded pathway to AI. Evidence that specific TC circuits contribute to patchy functional maps in AI was presented by Middlebrooks and Zook (1983), who demonstrated that excitatory/inhibitory (EE/EI) foci in AI receive input from segregated populations of neurons in the auditory thalamus. Surprisingly, the physiological responses of neurons within
TC patches and their relationship to various acoustic maps existing in
AI have not been addressed in any species. In the present study, this
question was examined by mapping the auditory cortex in animals that
received injections of anterograde tracer into the ventral division of
the medial geniculate body. Portions of this work have been published
previously in abstract form (Velenovsky et al., 2000, 2001).
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Materials and Methods |
Animals. The animals were housed, cared for, and used
strictly in accordance with United States Department of Agriculture regulations and the Guide for the Care and Use of Laboratory
Animals (National Institutes of Health publication 85-23). The
research protocol was approved by the Institutional Animal Care and Use Committee of the University of Arizona College of Medicine. Experiments were performed on normal young adult New Zealand white (NZW)
rabbits (1-3 kg) obtained from local suppliers. The experiments were
performed in two parts. In part I, an anterograde tracer was injected
into the ventral division of the MGB and the animal was allowed to recover. In part II, the ipsilateral auditory cortex was
electrophysiologically mapped with microelectrodes 6-8 d later. All
labeling and mapping procedures were performed in an IAC model 401A
sound booth (Industrial Acoustics Company, Bronx, NY).
Part I: anterograde labeling of TC pathway. Animals were
anesthetized with ketamine (44 mg/kg, i.m.) and xylazine (10 mg/kg, i.m.) and then placed in a Kopf stereotaxic device (David Kopf Instruments, Tujunga, CA). Surgery was performed under sterile conditions. Injection sites were referenced to bregma (lambda and
bregma in the same horizontal plane) using stereotaxic coordinates (McMullen and de Venecia, 1993). The final coordinate ranges were as
follows: anteroposterior, 6.5-7.2 mm; lateral, 5.3-5.6 mm; dorsoventral, 12.25-13.65 (referenced from skull surface). After small
holes were drilled through the skull, tungsten electrodes (2-4 M ;
World Precision Instruments, Sarasota, FL) were advanced stereotaxically into the auditory thalamus using a Kopf
micromanipulator fitted with a motorized stage (model MC-3B-11;
National Aperture Inc., Salem, NH). Custom-fabricated
transducers coupled to custom-molded earpieces were used to deliver
acoustic stimuli. Tucker-Davis Technologies (Gainesville,
FL) system II hardware controlled by a Gateway (Poway,
CA) personal computer using custom software were used to
generate auditory stimuli and analyze multi-unit responses as the
electrode was advanced in 100 µm steps. Multi-unit responses were
amplified and filtered using a Grass P511 preamplifier (Grass
Instruments, West Warwick, RI). After noise bursts (one per second;
100-200 msec duration) revealed an acoustically responsive area, tone bursts (one per second; 100-200 msec duration) were used to
characterize best frequency (BF), latency, and response profile of the
site. When short-latency-onset responses and sharp tuning curves in
response to tone bursts were seen, the coordinates were noted and the
electrode was slowly removed. A borosilicate glass electrode (outside
tip diameter, 10-13 µm) filled with 10% biotinylated dextran-amine
(BDA, molecular weight of 10,000; Molecular Probes, Eugene, OR)
in 0.1 M PBS was returned to the MGB
recording site. This was accomplished by placing the injection
microelectrode at the bregma reference site under high magnification.
The identical stereotaxic coordinates of the tungsten electrode were
used to locate the injection electrode at the original recording site. The BDA was deposited using positive current pulses (0.9 Hz, 3 µA for
20 min) with a Transkinetics CS-3 current generator. After the
electrode was removed, the incision was sutured, and chloromycetin (30 mg/kg, s.c.) was administered. The animal was returned to its
cage after it recovered from anesthesia and was monitored daily for
signs of infection or discomfort.
Part II: mapping of TC patches. After 6-8 d, the animal was
returned to the recording room and to the Kopf stereotaxic device for
cortical mapping. The animal was anesthetized using urethane (1.25 mg/kg, i.v.) and ketamine (13 mg/kg, i.m., every 50 min). Oval holes of
~4 × 6 mm were drilled through the skull just dorsal to AI.
Tangential penetrations were made through the auditory cortex (McMullen
and Glaser, 1982) with tungsten microelectrodes (2-4 M; World
Precision Instruments). Multi-unit response properties were determined
at 300 µm intervals. This recording interval was large enough to
maximize cortical mapping but remained fine enough to permit
functional/anatomical correlations. Broadband noise bursts were used to
determine the overall responsiveness of an area to auditory stimuli.
When a responsive area was located, the characteristic frequency,
threshold, and binaurality were determined using tone bursts (100 msec
duration). Binaurality was determined by presenting noise bursts at a
level 20-40 dB above threshold. For binaural presentation, diotic
stimuli were used. Responsiveness was judged by listening to multi-unit
activity through a monitor speaker and viewing real-time spike rasters. Responses were classified as EE if diotic stimuli elicited the most
robust response and EI if stimulating the contralateral ear elicited a
more robust response. No preference for contralateral or binaural
stimulation was classified as excitatory/occlusion (EO) (Imig
and Adrian, 1977; Middlebrooks and Zook, 1983). Afterward, spike
rasters, poststimulus time histograms (PSTHs) and tuning curves
were obtained (Cetas et al., 2002a). The binaurality determined for
noise bursts was used to set the mode of stimulus presentation (contra
or binaural) when the automated tuning curve program was run. The BF
from the tuning curve program was then evaluated for binaurality, using
levels and procedure as for noise above (Cetas et al., 2001).
Electrolytic lesions (10 µA for 10 sec) were placed at the end
of each penetration and at the location of the initial acoustic
response to assist in electrode track reconstructions. At completion of
the mapping experiments, the animal was perfused with 4%
paraformaldehyde in PBS and the brain was removed. The brain was
dissected into cortical and thalamic blocks and postfixed overnight in
4% paraformaldehyde at 4°C. The blocks were cryoprotected in
ascending sucrose solutions (to 30%) before sectioning.
Tissue processing. For the localization of injection sites,
coronal thalamic sections were cut using a sledge-type microtome (75 µm thick) and incubated for 15 min in 1%
H2O2 to suppress endogenous
peroxidase activity. BDA was localized by avidin-biotin-horseradish peroxidase histochemistry (Vector Elite ABC Kit; Vector Laboratories, Burlingame, CA) using nickel-cobalt intensification of the
diaminobenzidine (DAB) reaction product (Adams, 1981). Sections were
mounted on gelatinized slides and counterstained with 1% aqueous
methylene blue to confirm the location and extent of the MGV
injections. The electrophysiologically mapped cortices were gently
flattened between glass slides and fixed in 4% paraformaldehyde.
Tangential frozen sections through the cortex were cut on a sledge-type
microtome at a thickness of 50 µm. A sensitive immunoperoxidase
method was used to visualize BDA-labeled axons in the cortex
ipsilateral to MGV injections (McMullen and de Venecia, 1993; de
Venecia and McMullen, 1994). Briefly, sections were incubated for 48 hr
at 4°C in goat anti-biotin antibody (Vector Laboratories) diluted 1:10,000 in PBS containing 3% normal rabbit serum (NRS),
followed by biotinylated rabbit anti-goat IgG (Vector Laboratories)
diluted 1:200 in 3% NRS-PBS for 2 hr at room temperature. The labeled axons were visualized with a standard DAB histochemistry reaction with
heavy metal intensification (Adams, 1981). Because PV has been shown to
be an excellent marker for AI in a variety of species (Wallace et al.,
1991; McMullen et al., 1994; Hashikawa et al., 1995; Kosaki et al.,
1997; de Venecia et al., 1998; Budinger et al., 2000; Cruikshank et
al., 2001), alternative cortical sections were processed for this
calcium-binding protein. The monoclonal antibody against PV used in
these experiments was Swiss Antibodies #235 (Swant, Bellinzona,
Switzerland). All immunohistochemical procedures were performed
on free-floating sections using a rocker table for gentle agitation.
Dilutions and rinses were done with 0.1 M PBS, pH
7.4. Sections were first submerged in 1%
H2O2 for 15 min to suppress
endogenous peroxidase activity and then placed into 3% normal horse
serum (NHS; Vector Laboratories) with 1% Triton X-100 for 60 min to
block nonspecific labeling and to increase antibody penetration. The
sections were incubated in primary mouse monoclonal antibody to PV
(1:5000-1:15,000 dilution with 3% NHS) for 72 hr at 4°C, followed
by biotinylated horse anti-mouse IgG (1:200 dilution with 3% NHS) for
2 hr, and avidin-biotin-horseradish peroxidase complex
(Vector Laboratories Standard ABC kit) for 90 min at room temperature.
PV immunoreactivity was visualized using the cobalt-nickel DAB
intensification method of Adams (1981). No specific staining was
observed in control experiments in which sections were incubated in
primary antibody preadsorbed with HPLC-purified rat parvalbumin (Swiss
antibodies). All sections were then mounted onto gelatinized slides and
coverslipped with Permount. TC patches, electrode tracks, and
electrolytic lesions were reconstructed from serial sections with the
aid of a computer microscope (MicroBrightField Inc., Colchester, VT) or
an Aus Jena Macro-Projector (AusJena, Jena, Germany). Tissue
shrinkage was determined by measuring the distances between lesions
after tissue processing and comparing those values with those measured
in situ. A shrinkage measurement of 30% was determined and
applied to reconstruct the cortical electrode penetrations.
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Results |
All successful injections into the MGV resulted in labeled TC
patches. AI was mapped in 12 animals, with a total of 35 tangential electrode penetrations. In seven animals, at least one TC patch was
traversed by a mapping penetration. In six of the seven animals, the BF
of the MGV injection site was determined. In three of the six animals,
BF and binaurality of the injection site were represented in at least
one TC patch. Reconstructions of frequency and binaural maps obtained
from tangential electrode penetrations in three animals are shown in
Figure 1. In all cases in which AI was
mapped, a high-to-low dorsoventral frequency progression was seen. In 16 penetrations, an additional tonotopic field was located dorsal and
often anterior to the primary field, with a low-to-high frequency progression that mirrored the progression in the primary field. This
secondary field is shown for animals CM-4 and CM-13 in Figure 1
(denoted by asterisks) and CM-15 in Figure 3. The
distribution of binaural categories relative to the tonotopic maps is
also shown in Figure 1. In general, neurons formed clusters of binaural categories that extended across isofrequency contours. EE and EO
categories predominated and formed regions 0.5-2.0 mm wide. EI regions
were seen less frequently.
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Figure 1.
Reconstruction of frequency and binaural maps from
three animals (CM-4, CM-6, and CM-13). Gray shaded areas
represent regions of no response (NR) to acoustic
stimuli. The numbers represent BF in kilohertz at each
recording site. Binaural classes (EE, Red; EO,
yellow; EI, blue) are also
indicated. Note the clusters of similar binaural classes in each
penetration. The reverse (low-high) tonotopic progression in the
dorsal region of CM-4 and CM-13 (asterisks) represents a
second auditory field. Inset, Side view of the rabbit
brain showing the location of the AI and the orientation of
isofrequency contours. A, Anterior; D,
dorsal; P, posterior; V, ventral.
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A total of 14 BDA-labeled TC patches were mapped in seven animals.
Typically, multiple TC arbors in AI resulted from a single BDA
injection in the MGV (Fig. 2). In many
cases, the TC patches in the tangential plane appeared oriented along
the presumptive isofrequency contours in AI (shown in Fig. 1) of the
rabbit (see Figs. 2, 3, 5, 7, 9). In all
but one case, labeled patches arising from MGV tracer injections
coincided with tonotopically organized areas in auditory cortex, whose
functional characteristics (short latency, low threshold, dorsoventral
high-to-low frequency organization) were consistent with AI of this
species (McMullen and Glaser, 1982). In 86% (12 of 14 in seven
animals) of the penetrations through labeled TC patches, entry and exit
into anterograde-labeled terminal fields were characterized by abrupt
changes in physiological responses (e.g., binaurality, latency, and
frequency) to acoustic stimuli. In general (10 of 14 penetrations), TC
patches defined cortical regions of uniform multi-unit response
profiles (e.g., BF or binaurality). The patches were not associated
with any one group of unvarying response properties (i.e., consistent
frequency or binaurality was not always represented in every
patch).
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Figure 2.
Thalamic BDA injection and anterograde-labeled TC
fields. Left, Methylene blue counterstained coronal
section through the right MGV showing large BDA injection ventral
division (V) of the MGV. The injection is
elongated parallel to the MGV cellular laminas, which exhibit a
dorsomedial to ventrolateral orientation. Dorsal
(D) and internal
(I) MGV subdivisions are also visible.
Scale bar, 500 µm. Right, Tangential view of four TC
patches labeled by the BDA injection shown to the left.
Scale bar, 1.0 mm. Inset, Side view of the rabbit brain.
The boxed region shows the location of labeled TC
patches in AI. Scale bar, 5.0 mm.
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Figure 3.
Reconstruction of two mapping penetrations
superimposed on TC terminal field axons arising from the BDA injection
shown in Figure 2. Graphs depict BF as a function of electrode depth
throughout tangential penetrations 4 and 5. Dotted lines
indicate the BF reversal at the border between the dorsal field
(D) and AI. The shaded area
in each graph represents the portion of the penetration that passed
through a TC terminal field. Note the consistent BF within the patches
and the change in frequency as each electrode enters or exits the TC
terminal fields. A, Anterior; V, ventral;
P, posterior. Scale bar, 1.0 mm.
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An example of anterograde labeled patches in AI resulting from a large
BDA injection into the MGV of animal CM-15 is illustrated in Figure 2
(left). In this case, the BDA injection labeled an elongated
slab-like region whose orientation paralleled the cellular laminas in
the rabbit MGV (Cetas et al., 2001, 2002b). The TC projections labeled
by this injection consisted of four distinct patches shown in Figure 2
(right). A comparison with Figure 1 indicates that the
overall orientation of the patches parallels the isofrequency contours
of this species (Fig. 2). This relationship was observed in several
experiments (see below); it suggests a point-to-strip organization of
TC projections in this species. A reconstruction of the mapping
experiment for animal CM-15 is shown in Figure 3. A high-to-low
frequency progression was seen during mapping experiments, as revealed
by the graphs for penetrations 4 and 5 shown in Figure 3. A dorsal
tonotopic field was also seen in this experiment, characterized by a
steep low-to-high frequency progression that mirrored the frequency
organization of AI (Fig. 3). In experiment CM-15, frequency was
consistent throughout mapped portions of each of the TC patches.
Binaurality, in the form of EE, was also consistent in each of the
penetrations through the TC patches (Fig. 3).
Figure 4 illustrates a coronal section of
the MGV from animal CM-27, which received a small BDA injection located
at the lateral edge of the anterior MGV. A computer microscope
reconstruction of the small TC terminal fields labeled by this
injection, along with a reconstruction of one tangential electrode
penetration, is shown in Figure 5.
Typical for small patches labeled by injections of this size, BF (15 kHz) and binaurality (EE) remained consistent within the TC patch,
whereas threshold and PSTH response type varied (Fig. 5). Note also the
posterodorsal to anteroventral orientation of the two small patches
shown in the reconstruction of penetration 3, an orientation that
parallels the isofrequency contours of the rabbit AI (Fig. 1).
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Figure 4.
Methylene blue counterstained coronal
section through the right MGB in experiment CM-27, showing a small BDA
injection (arrow) in the far lateral MGV (V).
D, Dorsal subdivision of the MGB; I,
internal division of the MGB; LGN, lateral geniculate
nucleus. Scale bar, 500 µm.
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Figure 5.
Small TC patches are associated with regions of
consistent BF. Reconstruction of electrode penetration through TC
axonal fields from experiment CM-27. The graph depicts BFs as a
function of electrode depth throughout penetration 3. The shaded
area represents the portion of the penetration that passed
through the TC patch. Note the consistent BF (15 kHz) and binaural
responses (EE) within the patch and the change in frequency as the
electrode exits the patch. A, Anterior;
D, dorsal; P, posterior;
V, ventral. Scale bar, 1.0 mm.
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Figure 6 is a photomicrograph of a larger
BDA injection in the high-frequency area of the MGV for experiment
CM-13. Similar to CM-15, shown in Figure 2, the BDA injection site has
a dorsomedial-ventrolateral orientation similar to that of cellular
laminas and frequency slabs that have been described in the MGV (Cetas
et al., 2001). A computer microscope reconstruction of TC terminal
fields along with reconstructions of two tangential electrode
penetrations in auditory cortex from experiment CM-13 are shown in
Figure 7. Because of the large BDA
injection in the MGV, the TC terminal fields were larger here relative
to those from experiment CM-27 (Fig. 5). Similar to those of
experiments CM-15 and CM-27 (Figs. 3, 5), the TC terminal fields were
oriented in an anteroventral-to-posterodorsal direction. In each
penetration, both BF and binaurality remained constant within the TC
axonal field. In penetration 1, a change in binaurality occurred on
entering and exiting the TC field. A consistent BF (16 kHz) and
binaurality (EO) were observed within the patch. A consistent BF (23 kHz) and binaural response (EO) were also seen in the small patch
mapped in penetration 3 (Fig. 7, right). Although frequency
remained consistent in both TC fields, the BFs were not the same (16 and 23 kHz). It is interesting to note that 23 kHz is ~0.7 octaves
above 16 kHz, a frequency step size that has been described in the
rabbit MGB (Cetas et al., 2001).
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Figure 6.
Methylene blue counterstained coronal section
through the right MGB in experiment CM-13 showing BDA injection
(arrow) in the high-frequency region of MGV.
D, Dorsal subdivision of the MGB; I,
internal division of the MGB. Scale bar, 500 µm.
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Figure 7.
TC patches are associated with areas of consistent
binaurality. Reconstruction of two electrode penetrations through
elongated TC bands from experiment CM-13. The graphs depict binaurality
(EE, EO, EI) as a function of depth throughout the penetrations. The
graph on the leftrepresents binaurality throughout
penetration 1; the graph on the rightrepresents the same
for penetration 3. The shaded arearepresents the portion
of penetrations 1 and 3 that passed through TC fields. Note the
consistent binaurality within the patches and the change in binaurality
at patch borders. BF was constant within each mapped patch.
A, Anterior; D, dorsal; P,
posterior; V, ventral. Scale bar, 1.0 mm.
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The BDA injection in the MGV for experiment CM-29 is shown in Figure
8. Unlike the MGV injections in
experiments CM-15 (Fig. 3) and CM-13 (Fig. 6), the injection focus
extends vertically across the MGV laminas. Such an injection would be
expected to cross multiple frequency slabs in this species (Cetas et
al., 2002b).
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Figure 8.
Methylene blue counterstained coronal section
through the right MGB showing a large BDA injection
(arrow) in the lateral MGV (V).
D, Dorsal subdivision of the MGB; I,
internal division of the MGB. Scale bar, 500 µm.
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A computer reconstruction of the large terminal TC field labeled by the
BDA injection shown in Figure 8 (CM-29) is shown in Figure
9. Note the
anteroventral-to-posterodorsal orientation of the TC field, similar to
that of CM-15 (Fig. 3) and CM-27 (Fig. 5). Multi-unit responses to
acoustic stimulation were more robust within the terminal
field than those outside the TC arbors (Fig. 9). The multi-unit
response type (onset/sustained) is also consistent throughout the
labeled terminal field. A stepwise frequency progression was observed
within the TC patch. Binaurality was also consistent throughout the
patch, with the majority being classified as EO.
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Figure 9.
Reconstruction of an electrode
penetration through a large TC terminal field from experiment CM-29.
Rasters to the left of the penetration indicate
multi-unit response patterns at discrete recording points. Note that
the type and strength of multi-unit responses change at the patch
borders and remain consistent within the patch. The graph on the
right depicts response latency throughout the
penetration. The shaded area represents the portion of
the penetration through the TC patch. Frequency progression was
stepwise in this patch; binaurality was consistent (EO). Note the
consistent short-latency responses within the patch. Outside the patch,
regions of longer latency or no response (NR)
predominate. A, Anterior; D, dorsal;
P, posterior; V, ventral. Scale bar, 1.0 mm.
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Discussion |
Auditory fields and TC patches
Although physiological (Colwell and Merzenich, 1975; Middlebrooks
et al., 1980) and anatomical (Middlebrooks and Zook, 1983; Angelucci et
al., 1993; McMullen and de Venecia, 1993; de Venecia and McMullen,
1994; Hashikawa et al., 1995; Cetas et al., 1999) evidence for the
existence of multiple parallel pathways linking the auditory thalamus
and AI has existed for years, there have been few attempts to correlate
auditory physiological maps with TC circuits (Middlebrooks and Zook,
1983). In the present study, focal tracer injections in the MGV
frequently resulted in a band of TC axons composed of multiple patches
(McMullen and de Venecia, 1993). A consistent finding in the present
study was that TC patches defined a cortical module with a particular
BF. Electrophysiological mapping of several patches making up a band
revealed a common BF within the band (experiment CM-15). In most cases,
the TC axonal fields were aligned parallel to isofrequency contours in
AI, an arrangement predicted by Tunturi (1950) more than 50 years ago. These results are consistent with anterograde and retrograde studies of
auditory thalamic pathways that have shown that restricted areas of the
MGV diverge to widespread areas along an isofrequency contour (Colwell
and Merzenich, 1975; Merzenich et al., 1982; McMullen and de Venecia,
1993; Cetas et al., 1999). We conclude that functionally defined
isofrequency contours in AI derive from the patchy divergent
projections of auditory thalamic neurons.
Binaural interaction bands form an additional functional map in AI
(Imig and Adrian, 1977; Middlebrooks et al., 1980). Neuronal groups
projecting to either EE or EI bands are spatially segregated from one
another within the MGV (Middlebrooks and Zook, 1983), suggesting the
existence of several classes of MGV neurons with unique projections to
AI. In the present study, clusters of binaural regions were found
within AI composed of EE, EO, or EI response types, which crossed
isofrequency contours. The distribution of binaural classes in the
rabbit AI is similar to what has been described in AI of several other
species, such as the cat (Imig and Adrian, 1977; Middlebrooks et al.,
1980; Schreiner, 1991, 1995) and rat (Kelly and Sally, 1988), but has
not been reported before in this species. TC patches were also
associated with the clustered distribution of binaural classes in AI.
In many cases, the patch boundaries defined the borders of binaural
transitions (Fig. 7, EI-EO, EO-EE). Our results suggest
that TC patches represent the anatomical substrate for frequency and
binaural maps in AI. Several other discontinuous maps in the AI overlay
the tonotopic and binaural maps and include sharpness of tuning
(Schreiner, 1991; Recanzone et al., 1999), intensity tuning (Schreiner
et al., 1992; Recanzone et al., 1999), latency (Recanzone et al., 1999), and temporal response properties (Schreiner, 1991; Schulze et
al., 1997). How these maps relate to TC patches requires additional study.
In experiment CM-29, at least three distinct BFs were represented
within a large TC field. In contrast, binaurality (as well as latency
and response profile) remained consistent. We believe this finding is
related to the number of frequency laminas encompassed by the MGV
injection (Cetas et al., 2001). The frequency steps within the TC
axonal field (0.7 octave) were identical to those observed in mapping
penetrations across cell laminas in the MGV (Cetas et al., 2001). The
constancy of binaural responses within the large patches is consistent
with the distribution of binaural classes in the auditory thalamus. In
the MGV of the rabbit (Cetas et al., 2001) and cat (Rodrigues-Dagaeff
et al., 1989), binaural response classes are mapped independently of frequency.
Auditory cortical maps in the rabbit: comparison with
other species
In our experiments, all TC patches but one were found in areas
with a frequency organization that was typical of what has been
reported in AI of the rabbit: a dorsoventral high-to-low frequency
progression (McMullen and Glaser, 1982). This was expected, because our
injections were made in the MGV, the source of the main lemniscal
pathway to AI (Winer et al., 1977; Niimi and Matsuoka, 1979;
Imig and Morel, 1983; McMullen and de Venecia, 1993). In AI of the
rabbit, the tonotopic map and its representative isofrequency contours
appear rotated 90° compared with that in cats and monkeys (Merzenich
et al., 1973; Imig et al., 1977; Reale and Imig, 1980; Schreiner, 1991;
Recanzone et al., 1999). This rotation is consistent with the relative
orientation of cellular laminas in the MGV (Morest, 1965; Imig and
Morel, 1984; Cetas et al., 2001). A tonotopic map with isofrequency
contours similar to that of rabbits has been reported in an Australian
marsupial (Aitkin et al., 1986) and in ferrets (Angelucci et al.,
1993). In most mammalian species, the primary auditory field is
surrounded by one or more tonotopically organized areas (Tunturi, 1950;
Merzenich and Brugge, 1973; Imig et al., 1977; Reale and Imig, 1980;
Redies et al., 1989; Hackett et al., 1998). In the rabbit, a secondary
field with a tonotopic organization that mirrors AI lies dorsal to AI.
Based on its frequency organization and its position relative to AI,
this field appears to be the homolog to the anterior auditory
field of the cat (Reale and Imig, 1980) and the dorsal caudal
field of the guinea pig (Redies et al., 1989; Wallace et al.,
2000).
Integrity of tracer-injected MGV
An important concern when performing combined anterograde labeling
and mapping experiments is the possibility that the tracer used to
label anatomical structures may damage or destroy cells at the
injection site. In addition, uptake, transport, and distribution of the
tracer could modify the transmission of information to axonal targets,
thus altering the response profile of cortical sites coextensive with
the labeled axons. The evidence that BDA injections into the MGV and
its transport to AI did not result in alterations in the functional
properties of AI include the following: (1) The cortical frequency maps
obtained in our studies were very similar to those determined in
previous mapping studies of NZW rabbits (McMullen and Glaser, 1982).
(2) More importantly, experimental animals served as their own
controls; adjacent cortical penetrations in which one electrode passed
through a TC patch while the other did not were comparable in frequency
progression, latency, sharpness of tuning, and response strength. (3)
In some cases, the multi-unit responses within a TC patch were more
exuberant than those outside the patch. One would expect the opposite
effect if the BDA had eliminated excitatory input to cortical neurons. (4) In several cases, the BF of the injection site was represented within the area of a mapped TC patch. If neurons at the MGV injection site had been damaged or destroyed, we would not expect to see the BF
of that area represented within a TC patch. In fact, we might
expect to see areas of no response or frequency gaps during cortical
mapping, but this was not the case. We conclude that the cortical
response properties were not significantly affected by the thalamic
injections of BDA.
A model of MGB-AI connections
One of the problems in understanding auditory TC relationships is
the difficulty of reconciling continuously distributed functional maps
(e.g., frequency) with those exhibiting a discontinuous (e.g., binaural) organization. A model incorporating both of these
features of TC circuitry based on anatomical and physiological data
(Cetas et al., 1999, 2001, 2002a,b) is shown in Figure
10. In this model, TC axons originating
from binaural-specific relay neurons located in frequency slabs in the
MGV terminate in patches along a frequency strip in AI. Adjacent MGB
neurons within the same frequency slab but coding for a different
binaural class project to separate fields within the same frequency
strip. This model explains how continuous and discontinuous maps in AI
derive from patchy TC circuits.
View larger version (34K):
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Figure 10.
Inset, Diagram of TC projection
from the ventral nucleus of the MGB to AI. D, Dorsal
division; I, internal division; SC,
superior colliculus. Main diagram, Schematic of
the MGV showing ovoidea (OV) and laminated
(LV) regions (Cetas et al., 2001, 2002a, 2002b).
TC axons originating from binaural-specific relay neurons (red,
blue) located in frequency slabs terminate in patches along a
frequency strip in AI. Adjacent MGB neurons within the same frequency
slab but coding for a different binaural class project to separate
fields with the same frequency strip. This model explains how
continuous and discontinuous maps in AI derive from patchy TC
circuits.
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FOOTNOTES |
Received Aug. 27, 2002; revised Oct. 16, 2002; accepted Oct. 17, 2002.
This work was supported by National Institutes of Health (NIH)/National
Institute of Neurological and Communicative Disorders and Stroke Grants
DC05108 (D.S.V.) and DC02410 (N.T.M.) and a Deafness Research
Foundation Award (D.S.V.). J.S.C. was the recipient of a Predoctoral
Fellowship from NIH Training Grant NS07434. R.O.P. was supported by the
Undergraduate Biology Research Program at the University of Arizona and
the Howard Hughes Medical Institute. We thank Dr. Naomi Rance for
useful comments on a previous version of this manuscript, Jeb Zirato
for his help with the photomicroscopy, and Vanessa Lopez for assistance
with generation of computer reconstructions of thalamocortical patches.
Correspondence should be addressed to Dr. D. S. Velenovsky,
Department of Cell Biology and Anatomy, University of Arizona College
of Medicine, P.O. Box 245044, 1501 North Campbell Avenue, Tucson, AZ
85724. E-mail: dsv{at}u.arizona.edu.
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References |
-
Adams JC
(1981)
Heavy metal intensification of DAB-based HRP reaction product.
J Histochem Cytochem
29:775[Web of Science][Medline].
-
Aitkin LM,
Irvine DR,
Nelson JE,
Merzenich MM,
Clarey JC
(1986)
Frequency representation in the auditory midbrain and forebrain of a marsupial, the northern native cat (Dasyurus hallucatus).
Brain Behav Evol
29:17-28[Web of Science][Medline].
-
Angelucci A,
Clasca F,
Sur M
(1993)
Multiple cortical auditory fields in the ferret defined by their architectonics and thalamocortical connections.
Soc Neurosci Abstr
19:1427.
-
Brugge JF,
Imig TJ
(1978)
Some relationships of binaural response patterns of single neurons to cortical columns and interhemispheric connections of auditory area AI of cat cerebral cortex.
In: Evoked electrical activity in the auditory nervous system (Naunton RF,
Fernandez C,
eds), pp 487-503. New York: Academic.
-
Budinger E,
Heil P,
Scheich H
(2000)
Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivision and corticocortical connections.
Eur J Neurosci
12:2425-2451[Web of Science][Medline].
-
Cetas JS,
de Venecia RK,
McMullen NT
(1999)
Thalamocortical afferents of Lorente de No: medial geniculate axons that project to primary auditory cortex have collateral branches to layer I.
Brain Res
830:203-208[Web of Science][Medline].
-
Cetas JS,
Price RO,
Velenovsky DS,
Sinex DG,
McMullen NT
(2001)
Frequency organization and cellular lamination in the medial geniculate body of the rabbit.
Hear Res
155:113-123[Web of Science][Medline].
-
Cetas JS,
Price RO,
Velenovsky DS,
Crowe JJ,
Sinex DG,
McMullen NT
(2002a)
Cell types and response properties of neurons in the ventral division of the medial geniculate body of the rabbit.
J Comp Neurol
445:78-96[Medline].
-
Cetas JS, Price RO, Velenovsky DS, Crowe JJ, Sinex DG, McMullen
NT (2002b) Dendritic orientation and laminar architecture in
the rabbit auditory thalamus. J Comp Neurol, in press.
-
Colwell SA,
Merzenich MM
(1975)
Organization of thalamocortical and corticothalamic projections to and from physiologically defined loci within primary auditory cortex in the cat.
Anat Rec
181:336.
-
Cruikshank SJ,
Killackey HP,
Metherate R
(2001)
Parvalbumin and calbindin are differentially distributed within primary and secondary subregions of the mouse auditory forebrain.
Neuroscience
105:553-569[Web of Science][Medline].
-
de Venecia RK,
McMullen NT
(1994)
Single thalamocortical axons diverge to multiple patches in neonatal auditory cortex.
Brain Res Dev Brain Res
81:135-142[Medline].
-
de Venecia RK,
Smelser CB,
Lossman SD,
McMullen NT
(1995)
Complementary expression of parvalbumin and calbindin D-28k delineates subdivisions of the rabbit medial geniculate body.
J Comp Neurol
359:595-612[Web of Science][Medline].
-
de Venecia RK,
Smelser CB,
McMullen NT
(1998)
Parvalbumin is expressed in a reciprocal circuit linking the medial geniculate body and auditory neocortex in the rabbit.
J Comp Neurol
400:349-362[Web of Science][Medline].
-
Fitzpatrick DC,
Suga N,
Olsen JF
(1998)
Distribution of response types across entire hemispheres of the mustached bat's auditory cortex.
J Comp Neurol
391:353-365[Web of Science][Medline].
-
Hackett TA,
Stepniewska I,
Kaas JH
(1998)
Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys.
J Comp Neurol
394:475-495[Web of Science][Medline].
-
Hashikawa T,
Rausell E,
Molinari M,
Jones EG
(1991)
Parvalbumin- and calbindin-containing neurons in the monkey medial geniculate complex: differential distribution and cortical layer specific projections.
Brain Res
544:335-341[Web of Science][Medline].
-
Hashikawa T,
Molinari M,
Rausell E,
Jones EG
(1995)
Patchy and laminar terminations of medial geniculate axons in monkey auditory cortex.
J Comp Neurol
362:195-208[Web of Science][Medline].
-
Hendry SH,
Jones EG,
Emson PC,
Lawson DE,
Heizmann CW,
Streit P
(1989)
Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities.
Exp Brain Res
76:467-472[Web of Science][Medline].
-
Huang CL,
Winer JA
(2000)
Auditory thalamocortical projections in the cat: laminar and areal patterns of input.
J Comp Neurol
427:302-331[Web of Science][Medline].
-
Hubel DH,
Wiesel TN
(1962)
Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.
J Physiol (Lond)
160:106-154.
-
Hubel DH,
Wiesel TN
(1977)
Ferrier lecture: functional architecture of macaque monkey visual cortex.
Proc R Soc Lond B Biol Sci
8:1-59.
-
Imig TJ,
Adrian HO
(1977)
Binaural columns in the primary field (A1) of cat auditory cortex.
Brain Res
138:241-257[Web of Science][Medline].
-
Imig TJ,
Morel A
(1983)
Organization of the thalamocortical auditory system in the cat.
Annu Rev Neurosci
6:95-120[Web of Science][Medline].
-
Imig TJ,
Morel A
(1984)
Topographic and cytoarchitectonic organization of thalamic neurons related to their targets in low-, middle-, and high-frequency representations in cat auditory cortex.
J Comp Neurol
227:511-539[Web of Science][Medline].
-
Imig TJ,
Ruggero MA,
Kitzes LM,
Javel E,
Brugge JF
(1977)
Organization of auditory cortex in the owl monkey (Aotus trivirgatus).
J Comp Neurol
171:111-128[Web of Science][Medline].
-
Jones EG,
Burton H
(1976)
Areal differences in the laminar distribution of thalamic afferents in cortical fields of the insular, parietal and temporal regions of primates.
J Comp Neurol
168:197-247[Web of Science][Medline].
-
Jones EG,
Dell'Anna ME,
Molinari M,
Rausell E,
Hashikawa T
(1995)
Subdivisions of macaque monkey auditory cortex revealed by calcium-binding protein immunoreactivity.
J Comp Neurol
362:153-170[Web of Science][Medline].
-
Kelly JB,
Sally SL
(1988)
Organization of auditory cortex in the albino rat: binaural response properties.
J Neurophysiol
59:1756-1769[Abstract/Free Full Text].
-
Kosaki H,
Hishikawa T,
He J,
Jones EG
(1997)
Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys.
J Comp Neurol
386:304-316[Web of Science][Medline].
-
LeDoux JE,
Ruggiero DA,
Reis DJ
(1985)
Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat.
J Comp Neurol
242:182-213[Web of Science][Medline].
-
Marshall WH,
Woolsey CN,
Bard P
(1941)
Observations on cortical somatic sensory mechanisms of cat and monkey.
J Neurophysiol
4:1-24[Free Full Text].
-
McMullen NT,
de Venecia RK
(1993)
Thalamocortical patches in auditory neocortex.
Brain Res
620:317-322[Web of Science][Medline].
-
McMullen NT,
Glaser EM
(1982)
Tonotopic organization of rabbit auditory cortex.
Exp Neurol
75:208-220[Web of Science][Medline].
-
McMullen NT,
Smelser CB,
de Venecia RK
(1994)
A quantitative analysis of parvalbumin neurons in rabbit auditory neocortex.
J Comp Neurol
349:493-511[Medline].
-
Mendelson JR,
Schreiner CE,
Sutter ML,
Grasse KL
(1993)
Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps.
Exp Brain Res
94:65-87[Web of Science][Medline].
-
Mendelson JR,
Schreiner CE,
Sutter ML
(1997)
Functional topography of cat primary auditory cortex: response latencies.
J Comp Physiol [A]
181:615-633[Medline].
-
Merzenich MM,
Brugge JF
(1973)
Representation of the cochlear partition of the superior temporal plane of the macaque monkey.
Brain Res
50:275-296[Web of Science][Medline].
-
Merzenich MM,
Knight PL,
Roth GL
(1973)
Cochleotopic organization of primary auditory cortex in the cat.
Brain Res
63:343-346[Web of Science][Medline].
-
Merzenich MM,
Colwell SA,
Andersen RA
(1982)
Thalamocortical and corticothalamic connections in the auditory system of the cat.
In: Cortical sensory organization III (Woolsey CN,
ed)., pp -57. Clifton, NJ: Humana.
-
Mesulam MM,
Pandya DN
(1973)
The projections of the medial geniculate complex within the sylvian fissure of the rhesus monkey.
Brain Res
60:315-333[Web of Science][Medline]. arsid5590278
-
Middlebrooks JC,
Zook JM
(1983)
Intrinsic organization of the cat's medial geniculate body identified by projections to binaural response-specific bands in the primary auditory cortex.
J Neurosci
3:203-224[Abstract]. arsid5590278
-
Middlebrooks JC,
Dykes RW,
Merzenich MM
(1980)
Binaural response-specific bands in primary auditory cortex (AI) of the cat: topographical organization orthogonal to isofrequency contours.
Brain Res
181:31-48[Web of Science][Medline].
-
Molinari M,
Dell'Anna ME,
Rausell E,
Leggio MG,
Hashikawa T,
Jones EG
(1995)
Auditory thalamocortical pathways defined in monkeys by calcium-binding protein immunoreactivity.
J Comp Neurol
362:171-194[Web of Science][Medline].
-
Morest DK
(1965)
The laminar structure of the medial geniculate body of the cat.
J Anat Lond
99:143-160.
-
Morino-Wannier P,
Fujita SC,
Jones EG
(1992)
GABAergic neuronal populations in monkey primary auditory cortex defined by co-localized calcium binding proteins and surface antigens.
Exp Brain Res
88:422-432[Medline].
-
Niimi K,
Matsuoka H
(1979)
Thalamocortical organization of the auditory system in the cat studied by retrograde axonal transport of horseradish peroxidase.
Adv Anat Embryol Cell Biol
57:1-56[Medline].
-
Reale RA,
Imig TJ
(1980)
Tonotopic organization in auditory cortex of the cat.
J Comp Neurol
192:265-291[Web of Science][Medline].
-
Recanzone GH,
Schreiner CE,
Sutter ML,
Beitel RE,
Merzenich MM
(1999)
Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey.
J Comp Neurol
415:460-481[Web of Science][Medline].
-
Redies H,
Sieben U,
Creutzfeldt OD
(1989)
Functional subdivisions in the auditory cortex of the guinea pig.
J Comp Neurol
282:473-488[Web of Science][Medline].
-
Rodrigues-Dagaeff C,
Simm G,
De Ribaupierre Y,
Villa A,
De Ribaupierre F,
Rouiller EM
(1989)
Functional organization of the ventral division of the medial geniculate body of the cat: evidence for a rostral-caudal gradient of response properties and cortical projections.
Hear Res
39:103-126[Web of Science][Medline].
-
Romanski LM,
LeDoux JE
(1993)
Organization of rodent auditory cortex: anterograde transport of PHA-L from MGB to temporal neocortex.
Cereb Cortex
3:499-514[Abstract/Free Full Text].
-
Schreiner CE
(1991)
Functional topographies in the primary auditory cortex of the cat.
Acta Otolaryngol Suppl (Stockh)
491:7-16.
-
Schreiner CE
(1992)
Functional organization of the auditory cortex: maps and mechanisms.
Curr Opin Neurobiol
2:516-521[Medline].
-
Schreiner CE
(1995)
Order and disorder in auditory cortical maps.
Curr Opin Neurobiol
5:489-496[Web of Science][Medline].
-
Schreiner CE,
Mendelson JR
(1990)
Functional topography of cat primary auditory cortex: distribution of integrated excitation.
J Neurophysiol
64:1442-1459[Abstract/Free Full Text].
-
Schreiner CE,
Mendelson JR,
Sutter ML
(1992)
Functional topography of cat primary auditory cortex: representation of tone intensity.
Exp Brain Res
92:105-122[Web of Science][Medline].
-
Schreiner CE,
Read HL,
Sutter ML
(2000)
Modular organization of frequency integration in primary auditory cortex.
Annu Rev Neurosci
23:501-529[Web of Science][Medline].
-
Schulze H,
Ohl FW,
Heil P,
Scheich H
(1997)
Field-specific responses in the auditory cortex of the unanaesthetized Mongolian gerbil to tones and slow frequency modulations.
J Comp Physiol [A]
181:573-589[Web of Science][Medline].
-
Sousa-Pinto A
(1973)
Cortical projections of the medial geniculate body of the cat.
Adv Anat Embryol Cell Biol
48:1-42[Medline].
-
Tunturi AR
(1950)
Physiological determination of the arrangement of the afferent connections to the middle ectosylvian auditory area in the dog.
Am J Physiol
162:489-502[Free Full Text].
-
Vater M,
Braun K
(1994)
Parvalbumin, calbindin D-28k, and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats.
J Comp Neurol
341:534-558[Web of Science][Medline].
-
Velenovsky DS,
Cetas JS,
Price RO,
McMullen NT
(2000)
Thalamocortical patches represent isofrequency regions with consistent binaural response classes: a combined anterograde labeling and mapping study.
Abstr Midwinter Res Meet Assoc Res Otolaryngol
23:794.
-
Velenovsky DS,
Cetas JS,
Price RO,
Sinex DG,
McMullen NT
(2001)
Correspondence between functional subregions and thalamocortical terminal fields in AI arising from the ventral division of the medial geniculate body.
Abstr Midwinter Res Meet Assoc Res Otolaryngol
24:171.
-
Wallace MN,
Kitzes LM,
Jones EG
(1991)
Chemoarchitectonic organization of the cat primary auditory cortex.
Exp Brain Res
86:518-526[Web of Science][Medline].
-
Wallace MN,
Rutkowski RG,
Palmer AR
(2000)
Identification and localisation of auditory areas in guinea pig cortex.
Exp Brain Res
132:445-456[Web of Science][Medline].
-
Winer JA,
Diamond IT,
Raczkowski D
(1977)
Subdivisions of the auditory cortex of the cat: the retrograde transport of horseradish peroxidase to the medial geniculate body and posterior thalamic nuclei.
J Comp Neurol
176:387-417[Web of Science][Medline].
-
Woolsey CN,
Walzl EM
(1942)
Topical projection of nerve fibers from local regions of the cochlea to cerebral cortex of the cat.
Bull Johns Hopkins Hosp
71:315-344.
Copyright © 2003 Society for Neuroscience 0270-6474/03/231308-09$05.00/0
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ABSTRACT
Introduction
Compound via MeSH
