J Neurophysiol
87: 2520 –2530, 2002; 10.1152/jn.00343.2001.
Intracellularly Labeled Fusiform Cells in Dorsal Cochlear Nucleus of
the Gerbil. II. Comparison of Physiology and Anatomy
KENNETH E. HANCOCK1 AND HERBERT F. VOIGT1,2
1
Department of Biomedical Engineering and Hearing Research Center and 2Department of Otolaryngology,
Boston University, Boston, Massachusetts 02215-2407
Received 27 April 2001; accepted in final form 20 December 2001
The cochlear nuclei are the sole target of the auditory nerve
(AN) and as such represents an obligatory processing stage in
the ascending auditory pathway. The laminated dorsal cochlear
nucleus (DCN) contains a variety of morphological cell types
exhibiting diverse physiological responses. The outputs of the
DCN arise from fusiform cells and giant cells, which project
via the dorsal acoustic stria to the contralateral inferior colliculus (Adams and Warr 1976). Fusiform cells are readily identified by large cell bodies and bipolar dendritic fields (Brawer
et al. 1974; Lorente de Nó 1981). In the superficial layer,
spinous apical dendrites interact through a network of granule
cells and cartwheel cells (Berrebi and Mugnaini 1991; Golding
and Oertel 1997; Mugnaini et al. 1980) with somatosensory
(Itoh et al. 1987; Weinberg and Rustioni 1987; Wright and
Ryugo 1996), vestibular (Burian and Gstoettner 1988; Kevetter
and Perachio 1989), and descending auditory inputs (Benson
and Brown 1990; Weedman and Ryugo 1996). The distal
portion of the basal dendrite is excited by the descending
branch of the auditory nerve (Smith and Rhode 1985), while
the soma and proximal dendrites are likely inhibited by vertical
cells (Saint-Marie et al. 1991; Voigt and Young 1980, 1990)
and possibly by stellate cells of the posteroventral cochlear
nucleus (PVCN) (Oertel et al. 1990; Zhang and Oertel 1994).
There are several theories regarding fusiform cell function.
For example, strong sideband inhibition may serve to enhance
the representation of spectral peaks (Rhode and Greenberg
1994) or to extend dynamic range in the presence of noise
(Palmer and Evans 1982). DCN neurons better code the envelopes of amplitude-modulated stimuli than do auditory nerve
fibers (Backoff et al. 1999; Kim et al. 1990), leading to the
postulation of a “second axis” that codes for envelope frequency (Kim et al. 1990) or periodicity pitch (Langner and
Schreiner 1996). Finally, recent evidence has led to the theory
that the DCN extracts spectral cues relevant for sound localization. The head-related transfer function (HRTF) of the cat
contains a prominent notch whose center frequency varies
between 8 and 30 kHz according to the elevation of the sound
source (Musicant et al. 1990; Rice et al. 1992). This frequency
range has an enlarged representation in the cat DCN as compared with the cochlea (Spirou et al. 1993). Type IV units, an
important subset of DCN projection neurons, show sensitivity
to both the width and center frequency of notches in broadband
stimuli (Nelken and Young 1994; Spirou and Young 1991), as
do type III units in gerbils (Parsons et al. 2001).
The present report describes the physiology and anatomy of
17 intracellularly recorded and labeled fusiform cells from the
DCN of anesthetized gerbils. The fusiform cells in gerbils and
cats differ in their physiological response properties in the
decerebrate preparation. In particular, the incidence of type IV
units in the gerbil is less than one-third that reported in the cat
(Davis et al. 1996; Shofner and Young 1985). Antidromic
stimulation studies in the cat indicate that at least a portion of
the type IV unit population corresponds to fusiform cells
(Young 1980). Direct intracellular recording and labeling studies, however, suggest that gerbil fusiform cells are not type IV
Address for reprint requests: H. F. Voigt, Dept. of Biomedical Engineering,
Boston University, 44 Cummington St., Boston, MA 02215-2407 (E-mail:
[email protected]).
The costs of publication of this article were defrayed in part by the payment
of page charges. The article must therefore be hereby marked ‘‘advertisement’’
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
INTRODUCTION
2520
0022-3077/02 $5.00 Copyright © 2002 The American Physiological Society
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Hancock, Kenneth E. and Herbert F. Voigt. Intracellularly labeled
fusiform cells in dorsal cochlear nucleus of the gerbil. II. Comparison
of physiology and anatomy. J Neurophysiol 87: 2520 –2530, 2002;
10.1152/jn.00343.2001. Fusiform cells represent the major class of
dorsal cochlear nucleus (DCN) projection neuron. Although much is
understood about their physiology and anatomy, there remain unexplored issues with important functional implications. These include
interspecies differences in DCN physiology and the nature of the
cell-to-cell variations in fusiform cell physiology. To address these
issues, a quantitative examination was made of the physiology and
anatomy of 17 fusiform cells from a companion study. The results
suggest that the basal dendrites of gerbil fusiform cells may be
electrotonically more compact than those of the cat. This relative
decrease in the filtering of excitatory inputs might account for the
lower incidence of type IV units in that species. These data also
suggest that the gerbil DCN lacks the high-frequency specialization
described in the cat, because the tonotopic arrangement of the gerbil
fusiform cells quantitatively matches the place-frequency map for the
gerbil cochlea. Certain physiological properties have anatomical correlates. First, the basal dendrites of low spontaneous rate cells are
directed away from the soma only in the caudal direction, while the
high spontaneous rate cells have basal dendrites extending rostrally
and caudally. Second, input resistance was dominated by the surface
area of the apical dendrite. Third, the discharge pattern was correlated
with apical dendrite orientation. Finally, there was a spatial gradient
of sensitivity to broadband noise organized at least partially within an
isofrequency axis. Such trends indicate that neighboring fusiform cells
are endowed with different signal processing capabilities.
COMPARISON OF DCN FUSIFORM CELL PHYSIOLOGY AND ANATOMY
METHODS
Detailed experimental methods are provided in the companion
paper (Hancock and Voigt 2002). Methods specific to the analysis of
anatomical features are described below.
Position measurements
Cell location was quantified as suggested in Fig. 1. The bottom of
the figure shows a series of coronal sections, one of which contains a
hypothetical neuron, indicated by the dark circle. The position ⌬z
corresponds to the distance between the cell body and the rostral pole
of the nucleus, while L indicates the total length of the nucleus in the
rostral-caudal direction. Near the rostral end of the nucleus, the
number of layers typically decreased from three to two; the section
where layering disappeared altogether was selected as the rostral pole.
The section containing the soma is shown rotated at the top of Fig.
1 and illustrates measurements made within the coronal plane. The
position ⌬y is the depth along a line perpendicular to the ependymal
surface. The value H is the length of this line extended to the bottom
edge of the nucleus. The position ⌬x is the length of the arc along the
bottom edge measured from the ventrolateral side to the intersection
with the line used to measure depth. The width W is the total arc
length of the bottom edge measured from ventrolateral to dorsome-
J Neurophysiol • VOL
FIG.
1.
Summary of position measurements.
dial. The positions ⌬x, ⌬y, and ⌬z were normalized by W, H, and L,
respectively, to give the relative positions Px, Py, and Pz.
Morphological analysis
The fusiform cells were reconstructed in three dimensions working
from cameral lucida drawings using custom-designed software. The
dendritic structure was analyzed quantitatively from the reconstruction data using a set of MATLAB (Mathworks) scripts. Total dendritic
length was computed by approximating each dendrite as a sequence of
small cylinders and summing the cylinder lengths.
Measurements were made individually on each of the apical and
basal arbors. The methods follow those detailed by Blackstad et al.
(1984) and will be described briefly here. The first step was to
determine the long axis of the arbor. Blackstad et al. performed this
task manually, whereas in this study an automatic method was
adopted that consisted of computing the line between the cell body
and the center of mass of the dendritic terminals. The arbor was then
rotated about its long axis in 1° steps. At each step the span of the
arbor perpendicular to the long axis was computed. The arbor thickness was defined as the narrowest span, while the arbor width was
defined as the widest span. The degree of planarity was quantified by
computing the width to thickness ratio. The arbor height was measured as the extent of the arbor along its long axis.
RESULTS
Geometry of the dendritic arbors
The fusiform cell dendritic arbors were quantified by a series
of measurements inspired by the work of Blackstad et al.
(1984) in the cat and described fully in METHODS. The results
serve as a basis for comparison of the gerbil to the cat and as
a basis for a subsequent quantitative examination of the relationship between physiology and anatomy. It is important to
note that Blackstad et al. limited their consideration to the
central third of the DCN and thus avoided effects due to the
significant curvature of the nucleus at its edges. It was not
possible to do likewise in our case due to the sample size
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units (Ding et al. 1999). This difference across species in the
response properties of an important projection neuron motivates one aim of this study: to make a detailed quantitative
comparison of gerbil fusiform cell anatomy to that of the cat.
Golgi studies in the cat provide a suitable database of anatomical measurements for comparison (Blackstad et al. 1984),
including the dimensions of each dendritic arbor. The anatomical analysis of this study suggests, in part, that gerbil fusiform
cells may be electrotonically more compact than those of the
cat, and that this difference may account for some of the
observed differences in acoustic response properties.
Another issue is that fusiform cells exhibit a variety of
response properties. In the decerebrate preparation, they have
type III unit and type IV unit response maps (Ding et al. 1999;
Young 1980). In anesthetized preparations, fusiform cells exhibit pauser/buildup, chopper, or onset discharge patterns, depending on stimulus conditions (Hancock and Voigt 2002;
Rhode et al. 1983; Rhode and Smith 1986; Smith and Rhode
1985). The existence of such variations must be related to the
complexity of the neural circuits with which fusiform cells
interact. But are the cell-to-cell differences merely the result of
random “wiring” differences, or do they reflect underlying
principles of organization? This question motivates a second
aim: to make a quantitative comparison of fusiform cell physiology and morphology in cats and gerbils. Certain physiological characteristics were indeed found to have specific anatomical correlates. Spontaneous rate (SR) was related to the
disposition of the basal dendrites, input resistance was correlated with apical dendrite total length, and the discharge pattern
at best frequency (BF) was correlated with fusiform cell orientation. It appears that neighboring fusiform cells may have
different physiological properties and hence different signal
processing capabilities by virtue of cell-to-cell variations in
morphology.
This work represents part of the doctoral dissertation of
K. E. Hancock.
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K. E. HANCOCK AND H. F. VOIGT
Tonotopy
A qualitative illustration of the tonotopic organization is
presented in Fig. 2A, in which the 17 fusiform cells of this
study have been mapped onto a single DCN. Only the basal
dendrites have been drawn because that is presumably where
fusiform cells receive acoustic input (Smith and Rhode 1985).
The dendrites are color coded according to BF, as shown.
Figure 2A qualitatively suggests that the gerbil DCN has a
substantial volume devoted to relative low BFs. The orderly
arrangement of cells by BF is also apparent, with the lowest
BFs in the rostral-most and ventrolateral-most aspect of the
nucleus.
TABLE
1. Properties of apical dendritic arbors
Cell
TL, ␮m
Width, ␮m
Thickness, ␮m
Ratio
Height, ␮m
95026
95055
95082
95135
97002
97005a
97008b
97022a
97054a
97054b
97055a
97072a
97073
98001
98012a
98014
98024a
Mean
Cat mean
2,539
3,465
2,138
3,290
3,097
3,541
2,410
4,294
4,068
3,228
2,554
6,435
3,348
2,843
2,327
3,238
4,289
3,359
3,212
195
344
235
297
283
369
219
323
346
341
146
373
226
214
218
243
294
274
354
118
99
97
121
180
61
93
104
93
100
104
173
121
167
87
93
203
118
138
1.66
3.47
2.42
2.45
1.57
6.05
2.35
3.10
3.74
3.43
1.41
2.15
1.86
1.28
2.51
2.61
1.45
2.56
⬃3
117
119
185
168
144
206
102
147
179
216
233
137
157
123
151
135
154
157
267
TL, total length.
J Neurophysiol • VOL
TABLE
2. Properties of basal dendritic arbors
Cell
TL, ␮m
Width, ␮m
Thickness, ␮m
Ratio
Height, ␮m
95026
95055
95082
95135
97002
97005a
97008b
97022a
97054a
97054b
97055a
97072a
97073
98001
98012a
98014
98024a
Mean
Cat mean
636
3,359
1,776
5,600
1,788
1,191
1,658
1,490
1,704
941
1,391
1,047
1,236
3,196
3,443
1,371
897
1,925
2,728
178
301
325
515
297
240
314
389
191
248
318
264
235
538
529
242
218
314
392
34
137
85
274
119
143
75
106
58
119
86
79
80
180
150
89
95
112
72
5.28
2.20
3.81
1.88
2.50
1.68
4.19
3.67
3.31
2.09
3.71
3.34
2.94
2.99
3.52
2.72
2.30
3.07
5.70
187
563
368
318
282
157
227
182
210
118
80
288
316
356
173
220
205
250
389
TL, total length.
Figure 2A shows that BF increases in both the dorsomedial
and caudal directions. This observation is quantified in Fig. 2B
where the BF is plotted as a function of the relative X-positions
(ventrolateral-to-dorsomedial location) and the relative Z-positions (rostral-to-caudal location) of the fusiform cell somata.
The straight line fits to these data indicate that BF is indeed
highly correlated with these two dimensions.
The tonotopic axis is described by the equation log(BF) ⫽
1.45Px ⫹ 1.01Pz (r ⫽ 0.81, P ⬍ 0.001), obtained by performing multiple linear regression on log BF using both the relative
X- and Z-positions. A tonotopic position was determined for
each neuron by projecting its location onto this axis and computing the distance from the origin (Px ⫽ Pz ⫽ 0). The
resulting positions are plotted in Fig. 3 as a function of BF. For
comparison, the place-frequency map for the gerbil cochlea is
also plotted, where position indicates the relative distance from
the base of the cochlea. In general, Fig. 3 shows that the spatial
distribution of BFs in the DCN closely follows the distribution
of characteristic frequencies (CFs) along the cochlea. For comparison, the place-frequency map computed for the cat DCN by
Spirou et al. (1993) is also plotted.
Fusiform cell orientation varies with location
Figure 4 summarizes a systematic shift in the orientation of
the long axis as a function of rostral-caudal position. In the
rostral end of the nucleus, the apical dendrites tend to be
positioned on the rostral side of the soma while the basal
dendrites extend in the caudal direction. Near the center of the
DCN, the orientation is roughly vertical (dorsal to ventral).
Toward the caudal pole, fusiform cells have caudally directed
apical dendrites and rostrally directed basal dendrites.
It would appear that this trend is a consequence of the shape
of the DCN itself. The DCN can be visualized as a series of
thin shells, with the molecular layer wrapped around the fusiform cell layer, which in turn is wrapped around the deep layer.
Thus from any position within the fusiform cell layer, the
apical dendrites radiate outward to fill the molecular layer
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limitations inherent to an in vivo intracellular survey of this
kind.
The anatomical properties of the apical arbors are summarized in Table 1. Estimates were made of the total dendritic
lengths by summing the lengths of the individual segments
comprising each three-dimensional (3-D) reconstruction. The
mean apical length was 3,359 ␮m, which is very close to the
mean value of 3,212 ␮m reported by Blackstad et al. (1984) in
the cat. The width and thickness measurements were obtained
by rotating the arbor about its long axis to find the widest and
narrowest projections, respectively. Both measures are smaller
in the gerbil than in the cat, although the ratio, which reflects
the degree of arbor planarity, is approximately the same in both
cases (2.56 in the gerbil, roughly 3 in the cat). The mean height
of the apical arbor, measured parallel to the long axis, was 157
␮m in the gerbil as compared with 267 ␮m in the cat.
Table 2 lists the anatomical properties of the basal dendrites
in this study. The mean total length was 1,925 ␮m, as compared with 2,728 ␮m in the cat. The mean arbor width is
smaller in the gerbil (314 ␮m) than in the cat (392 ␮m), but the
thickness is larger (112 vs. 72 ␮m). The result is that the width
to thickness ratio in the gerbil (3.07) is about half that in the cat
(5.70). The mean basal arbor is 250 ␮m in height as compared
with 389 ␮m in the cat.
COMPARISON OF DCN FUSIFORM CELL PHYSIOLOGY AND ANATOMY
2523
while the basal dendrites converge inward to occupy the deep
layer. A similar finding was reported by Rhode et al. (1983),
who further describe the cells in the rostral end having more
numerous apical dendrites that more frequently emerge directly
from the soma. Neither this study nor the previous one finds
any obvious physiological sequellae to this trend, which possibly is simply a consequence of the overall curvature of the
nucleus.
FIG. 3. Comparison of frequency-place maps for the gerbil cochlea and
DCN. Place-frequency data for fusiform cells obtained by projecting soma
locations onto frequency axis computed in the text. Place-frequency map for
the gerbil cochlea from Müller (1996). Place-frequency map for the cat DCN
from Spirou et al. (1993).
J Neurophysiol • VOL
Spontaneous rate depends on basal dendrite orientation
The spontaneous discharge rates of the fusiform cells in this
sample range from 0 to 54 spikes/s. These can be separated into
a low SR group (rate ⬍2.5 spikes/s, 8/17 cells) and a high SR
group (rate ⬎7.5 spikes/s, 9/17 cells). The creation of two SR
categories may, in fact, represent an artificial division of a
continuously distributed property, but is useful here as a convenient means of visualizing a related anatomical trend. Specifically, there is a correlation between spontaneous rate group
FIG. 4. Fusiform cell orientation changes with rostral-caudal position.
DCN is represented by a series of coronal slices. Arrows point from soma
locations to renderings of fusiform cells in a sagittal view. Thick gray lines
indicate the long axis of each cell. D, dorsal; C, caudal.
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FIG. 2. Tonotopic organization of the gerbil dorsal cochlear nucleus (DCN). A: the basal dendrites of the 17 fusiform cells from
this study mapped onto a single DCN. A patch has been removed from the surface of the DCN to show the interior. Dendrites are
color-coded according to best frequency (BF) as shown. D, dorsal; R, rostral; L, lateral. B: scatterplots showing BF vs. relative
X-position (top) and relative Z-position (bottom). Regression line for X-position given by log(BF) ⫽ 2.38x ⫺ 0.72, r ⫽ 0.62, P ⬍
0.01. Regression line for Z-position given by log(BF) ⫽ 1.30x ⫺ 0.26, r ⫽ 0.74, P ⬍ 0.001.
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K. E. HANCOCK AND H. F. VOIGT
Input resistance is a function of total apical dendritic length
Figure 6 shows that fusiform cell input resistance is correlated with apical dendritic length, but not with basal dendritic
length. The best line fit to the apical length was computed after
removing the two points indicated by triangles in Fig. 6A. The
correlation with apical length is negative, so that larger lengths
correspond to smaller resistances. This is consistent with a
passive model in which membrane conductance is proportional
to surface area, insofar as dendritic surface area is proportional
to total length. Input resistance was not correlated with the sum
of the apical and basal lengths (r ⫽ ⫺0.06). The presence of
spines, however, greatly increases the surface area per unit
length of the apical dendrite and so a simple sum of total
lengths probably understates the contribution of the apical
FIG. 6. Relationship between input resistance and arbor length. A: input
resistance is highly correlated with apical dendrite length. Regression line: y ⫽
⫺10.5x ⫹ 48.2, r ⫽ ⫺0.79, P ⬍ 0.001. Triangles indicate data points omitted
as outliers. B: input resistance is uncorrelated with basal dendrite length.
Regression line: y ⫽ 0.6x ⫹ 16.8, r ⫽ 0.08, ns.
dendrite to the overall passive membrane conductance. We did
not consider the effects of surface area more directly because
of difficulties estimating it that arose from inconsistencies in
the quality of spine labeling.
FIG. 5. Spontaneous activity and basal
dendrite arrangement. Neurons are from the
0- to 2-kHz region and are drawn in a parasagittal view. Apical dendrites are shown in
gray; basal dendrites in black. Basal dendrites of low spontaneous rate (SR) cells (top
row) are oriented primarily in the caudal
direction. Those of the high SR cells (bottom
row) have both rostrally and caudally directed branches. This difference is quantified
using the parameter ZC, which is the rostralcaudal component of the basal arbor’s centroid, measured with respect to the soma.
The low SR units have larger ZC values (centroids located more caudally) than the high
SR units.
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and the disposition of the basal dendrites, as depicted in Fig. 5.
The basal dendrites of the low SR cells (top row) are primarily
directed caudally away from the soma. The high SR cells
(bottom row) tend also to have branches oriented in the rostral
direction, giving the distribution of the basal dendrites a more
symmetrical appearance.
These observations were put on a more quantitative basis by
computing the centroid of each basal arbor with respect to the
soma. The trend is specifically captured by the rostral-caudal
component, ZC, as shown in Fig. 5. Note that the value of ZC
is positive for positions caudal to the soma. For every low SR
cell (ZC ⱖ 63.2 ␮m), the basal arbor centroid is caudal to that
of every high SR cell (ZC ⱕ 48.8 ␮m). No correlation was
found between the absolute position of the basal arbor centroid
and spontaneous activity.
The nine cells shown in Fig. 5 come from the same general
region of the DCN, reflected by the similarity of their best
frequencies. This is an important consideration when examining the arrangement of the basal dendrites, because as described above, the orientation of the fusiform cell long axis
changes as a function of position (Fig. 4).
COMPARISON OF DCN FUSIFORM CELL PHYSIOLOGY AND ANATOMY
Regularity histogram shape depends on orientation
of apical arbor
Regularity histogram shapes were quantified using three
slope measurements as described in the companion paper.
Briefly, the transient slope, mT, most closely follows the classification scheme of Gdowski (1995). It is particularly sensitive
to the change in interspike interval over the initial 5–10 ms of
response and since nearly all of the cells in this study had
decreasing intervals over this range, regardless of their subsequent behavior, the transient slope was not necessarily an
effective means of characterizing rate trends over the entire
stimulus duration. To better capture these rate trends, the slope
measurements m1 and m2 were computed by performing a
two-line fit to the interspike interval data after omitting the
first bin.
2525
Figure 7 shows that for the 10 fusiform cells with BFs less
than 2 kHz, the slope m1 is correlated with the orientation of
the apical dendrites. The angle ␸apical corresponds to the rotation required to find the narrowest dendritic profile after making the long axis of the arbor vertical. A value of zero corresponds to an arbor oriented perpendicular to the coronal plane.
The apical dendrites in Fig. 7 are drawn looking down on their
tops, such that their long axes project out of the page. The
values of m1 have been divided into three groups: high, medium, and low, indicated in Fig. 7 by circles, triangles, and
squares, respectively. The data indicate that the fusiform cells
with apical arbors oriented most nearly perpendicular to the
coronal plane have the most positive m1 values (circles), while
those oriented closest to parallel to the coronal plane have the
most negative m1 values (squares).
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FIG. 7. Relationship between regularity histogram shape and orientation of apical arbor.
Top: slope m1 from the regularity histogram
plotted vs. the orientation of the apical arbor.
The orientation ␸apical is the rotation about the
long axis giving the narrowest arbor profile. See
text for a detailed description of how these
values are measured. Regression line: y ⫽
⫺1.1x ⫹ 21.8, r ⫽ ⫺0.82, P ⬍ 0.01. Data
points indicated by circles, triangles, and
squares represent high, middle, and low m1 values, respectively. Bottom: each group corresponds to the data points above and shows the
fusiform cell apical arbors after superimposing
the somata. The view is looking down on top of
apical arbors, so that the long axes project out of
the page. R, rostral; M, medial.
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K. E. HANCOCK AND H. F. VOIGT
Correlation of cell properties with location
DISCUSSION
A detailed quantitative examination of fusiform cell physiology and anatomy was made in this study. The following
findings will be discussed. 1) The basal dendrite in the gerbil is
shorter than in the cat. 2) The gerbil DCN appears to lack the
high-frequency specialization of the cat DCN. 3) High spontaneous firing rates are correlated with basal dendrites having
both rostrally and caudally directed branches, while low spontaneous rates are correlated with basal dendrites having only
caudally directed branches. 4) The inhibition reflected in the
slope of the regularity histogram is related to the orientation of
the apical arbor. 5) Noise response strength appears to be
systemically organized within an isofrequency sheet.
Consideration of the basal arbor total length
FIG. 8. Physiological properties correlated with position. Relative noise
index (A) and input resistance (B) are negatively correlated with position in the
X-direction. Regression line for noise index: y ⫽ ⫺1.16 ⫻ 10⫺3x ⫹1.30, r ⫽
⫺0.53, P ⬍ 0.05. Regression line for input resistance: y ⫽ ⫺50.0 ⫻ 10⫺3x ⫹
50.7, r ⫽ ⫺0.67, P ⬍ 0.01. C: total apical dendritic length increases with
X-position. Regression line: y ⫽ 3.01 ⫻ 10⫺3x ⫹ 1.17, r ⫽ 0.56, P ⬍ 0.025.
Triangle indicates an outlier removed from the regression analysis.
The basal dendrites in the gerbil have about 70% the total
length that they do in the cat and thus may be electrotonically
more compact. The equivalent cylinder model for a dendritic
arbor has a characteristic electrotonic length, which is proportional to the ratio of the physical length of the cylinder to the
square root of its diameter (Rall 1977). Consider a hypothetical
cat fusiform cell that has three primary basal dendrites giving
rise to identical branching structures. One possibility is that the
“gerbil” fusiform cell retains all three branches, but each
branch is shortened by a third. The equivalent cylinder for such
a cell would be physically shorter than its counterpart in the
cat, but have the same diameter and hence a shorter electrotonic length. A gerbil fusiform cell could also be produced by
removing one of the three hypothetical branches, giving the
observed one-third reduction in total length. The equivalent
cylinder would have the same physical length as the cat fusiform cell, but its diameter would be smaller, resulting in a
longer electrotonic length.
Which case best represents the actual situation? Blackstad et
al. did not report branch order statistics for the cat, so it is not
possible to make a comparison in this regard. But, as shown in
Table 2, the height of the basal arbor is about one-third smaller
in the gerbil than in the cat. This would seem to reject the
second scenario above, since the pruning of one branch would
not affect the size of the remaining branches and hence the
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An effort was made to identify fusiform cell characteristics
that vary systematically with location. To do this, a wide
variety of physiological response metrics (see companion paper) were systematically correlated with the normalized X-, Y-,
and Z-position measurements (see METHODS).
Two statistically significant trends were identified, roughly
orthogonal to the tonotopic axis. The relative noise index
decreased in the X-direction (ventrolateral to dorsomedial),
meaning that the responses to noise became progressively
weaker in this direction (Fig. 8A). A gradient in wideband
inhibitory strength is sufficient to account for this observation,
as detailed in the DISCUSSION. The second trend was that input
resistance also tended to decrease in the X-direction (Fig. 8B).
This is consistent with the fact that total apical dendritic length
increases in the same direction (Fig. 8C), since the inverse
relationship between these two properties has already been
described.
Aside from tonotopy, the only statistically significant spatial
trends were found in the X-direction. Since neither trend was
accompanied by a significant dependence on Z-position, it was
not possible to compute an axis trajectory for quantitative
comparison with the tonotopic axis computed above. It can,
however, be said that while best frequency is strongly correlated with both X- and Z-position, input resistance and relative
noise response are strongly correlated only with X-position. So,
although these results cannot resolve the issue of an orthogonal
axis per se, there is at least a qualitative suggestion that the
spatial gradients of these two properties are not parallel with
the frequency axis.
COMPARISON OF DCN FUSIFORM CELL PHYSIOLOGY AND ANATOMY
Tonotopic organization of the gerbil DCN
The qualitative picture of tonotopy presented in Fig. 2 agrees
well with the description of frequency organization in gerbil
DCN obtained using measurements of 2-deoxyglucose uptake
(Ryan et al. 1982). On a more quantitative basis, the fusiform
cell BFs were plotted in Fig. 3 as a function of the cell position
along the tonotopic axis. The data plotted in this manner
correspond well with the cochlea place-frequency map determined by Müller (1996) in the Mongolian gerbil (Fig. 3). Such
quantitative correspondence between frequency representation
in the cochlea and tonotopic organization in central auditory
structures is frequently observed (Müller 1990).
A notable exception is the cat DCN, whose representation of
the 8- to 30-kHz range is disproportionately larger than the
representation of the same frequency range in the cochlea
(Spirou et al. 1993). The head-related transfer function (HRTF)
in the cat contains spectral notches that may serve as cues for
determining sound source elevation (Rice et al. 1992). These
notches fall in the 8- to 30-kHz range, suggesting that the
enhanced representation of these frequencies in the cat DCN is
a functional specialization related to coding those particular
spectral features (Spirou et al. 1993).
The place-frequency analysis shown in Fig. 3 is limited to
J Neurophysiol • VOL
the extent that it is a one-dimensional description of the tonotopy; it does not consider variations in cell density or the
possibility of a two-dimensional frequency gradient. The comparison with the cat data of Spirou et al. (1993) is appropriate
insofar as the cat data are also based on a one-dimensional
frequency axis. That study, however, was based on BF estimates made at finely spaced locations from a large number of
electrode tracks. Furthermore, Spirou et al. (1993) accounted
for variations in fusiform cell density when drawing conclusions about BF representation in the DCN.
The present data therefore should be regarded as preliminary
but appear to underscore the fact that the tonotopy of the gerbil
DCN (and cochlea) is largely devoted to a lower frequency
range. Frequencies below 10 kHz occupy about 60% of the
length of both structures, and no specialized frequency representation in the gerbil DCN is apparent. It is currently unknown whether or not the gerbil HRTF contains spectral elevation cues similar to those identified in the cat HRTF.
Measurements of the HRTF in gerbil and a more detailed
examination of frequency representation in the DCN are essential to a comparative evaluation of DCN function in the two
species.
Spontaneous rate
The results indicate that the disposition of the basal dendrites
is correlated with spontaneous rate for the fusiform cells with
best frequencies less than 2 kHz. The basal dendrites of low SR
cells are directed away from the soma only in the caudal
direction, while the high SR cells have basal dendrite branches
extending both rostrally and caudally. The basal arbors of the
low SR units, relative to those of the high SR units, have more
caudally located centroids. It is important to note that this
observation is based on relative comparisons of basal arbor
structure among cells having similar orientations. No absolute
metric was found to allow for a global quantification of the
relationship between SR and basal dendrite position. It was
thus necessary to limit consideration to this BF range because
of the general shift in long axis orientation with rostral-caudal
position (and hence BF) and because there were not sufficient
numbers in any other frequency band for cell-to-cell comparisons to be made.
It is not immediately clear how the orientation of the basal
dendrites may influence spontaneous activity. Liberman (1993)
suggested that auditory nerve inputs to the cat DCN may be
segregated based on spontaneous rate, with the high SR fibers
terminating deeper in the nucleus than the low SR fibers. This
appears to be inconsistent with our results, since the rostrally
directed basal dendrites of the high SR fusiform cells tend to be
more shallow in depth than the caudally directed branches
common to both SR groups.
Another possibility is that the rostrally directed branches
access some other set of inputs that modulate spontaneous
activity. It also may be that the orientation characteristic of the
high SR cells has electrotonic consequences that emphasize
excitatory inputs over inhibitory inputs. Regardless of the
mechanism, the results suggest that the distribution of fusiform
cell spontaneous activities is not entirely due to happenstance.
It is difficult to say what functional consequences may arise
from having a subset of the fusiform cell population preferentially receive low SR input. It has been suggested that low SR
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arbor height should remain about the same. This leaves the first
scenario as the most viable and suggests that the effect of
dendritic shortening in the gerbil is to make the basal arbor
electrotonically more compact than in the cat.
Assuming that inputs from the auditory nerve are distributed
toward the distal ends of the basal dendrites (Smith and Rhode
1985), a possible effect of this electrotonic shortening would
be to decrease the attenuation of excitatory synaptic potentials.
To the extent that inhibitory inputs are received at more proximal locations (Berrebi and Mugnaini 1991; Saint-Marie et al.
1991), they are relatively unaffected by the overall length of
the dendrite. Hence, an electrotonically more compact basal
dendrite might preferentially enhance excitatory drive relative
to inhibition. Indeed, previous results suggest that the proportion of DCN units having type IV unit properties is smaller in
the gerbil than in the cat (11% vs. 32– 45%) and the proportion
of type III units is larger (62% vs. 23%) (Davis et al. 1996).
Ding et al. (1999) reported on 13 labeled fusiform cells from
the decerebrate gerbil, none of which had classic type IV unit
response properties. Interestingly, the type IV unit incidence in
rabbit (23%) and chinchilla (25%) appears to follow the same
size-related trend (Davis et al. 1996; Hui and Disterhoft 1980;
Kaltenbach and Saunders 1987).
This species-related difference in unit incidence was considered by Davis and Voigt (1996) using a point neuron model.
Their hypothesis was that a weakened contingent of type II unit
inhibition onto DCN projection neurons was responsible for
the lack of type IV units found in the gerbil relative to the cat.
They showed that a 40 –50% reduction in the number of type
II unit inputs was sufficient to turn a model type IV unit into a
type IV-T or type III unit. A hypothesis based on the present
finding in regard to basal dendrite length, in contrast, suggests
that the balance is shifted toward excitation by an enhancement
of the excitatory inputs, rather than by a reduction of the
inhibitory inputs. These issues might effectively be explored
using a compartmental model of a fusiform cell.
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K. E. HANCOCK AND H. F. VOIGT
auditory nerve fibers are recruited to improve intensity discrimination at high sound levels or are useful for signal in noise
problems (Viemeister 1983). Extending such interpretations to
the DCN is problematic, because they are based on the fact that
low SR AN fibers typically have high acoustic thresholds
(Liberman 1978), a trend not generally characteristic of DCN
units. It has been shown that low SR AN fibers better synchronize to AM tones (Joris and Yin 1992), but there remains
disagreement over the general suitability of DCN projection
neurons for encoding such stimuli (Joris and Smith 1998).
Shape of regularity histogram
Organization of sensitivity to broadband noise
The notion that the DCN contains a functional axis orthogonal to the frequency axis is suggested by anatomical features.
First, there is the network of parallel fibers oriented perpendicular to the underlying auditory nerve fibers. If systematic
variations in activity within the parallel fiber network contribute to the variations in fusiform cell physiology, then fusiform
cell properties might vary in a spatially dependent manner.
Another anatomical substrate for a second axis in the DCN is
a progressive decrease in the number of vertical cells in the
dorsomedial direction within the coronal plane (Lorente de Nó
1981). Since vertical cells presumably inhibit fusiform cells,
the magnitude of inhibitory response features (tone slope,
interspike interval slope, etc.) should also decrease in the
dorsomedial direction.
The results show that the relative noise index is negatively
Possible significance of physiology-morphology correlations
Figures 5–7 demonstrate that certain morphological features
are correlated with specific physiological properties. The geometries of the apical and basal arbors influence input resistance and spontaneous activity, respectively, while some aspect
of cell orientation apparently contributes to the inhibition measured in the regularity histogram. It is thus possible that fusiform cells along the isofrequency axis have graded physiological properties, and hence different signal processing
characteristics. In this way, the fusiform cell population might
be capable of performing different operations on the same set
of inputs.
J Neurophysiol • VOL
FIG. 9. Two neighboring fusiform cells from the caudal end of the DCN.
Long axes are nearly horizontal in accordance with the general rostral-caudal
shift in orientation. At the top, the cells are drawn in their correct relative
positions. At the bottom, they are drawn separately to show individual details
clearly.
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For the fusiform cells in the 0- to 2-kHz band, a correlation
was observed between the orientation of the apical dendritic
arbor, quantified by the rotation, ␸apical, about the long axis
yielding the narrowest projection of the arbor, and the shape of
the regularity histogram, as quantified by the slope, m1 (Fig. 7).
The slope values m1 and m2 are obtained by simultaneously
fitting two lines to the interspike interval plot after omitting the
first bin. For the data of this study, the value of m1 appears to
be a more useful measure of inhibition than the monotonicity
of the BF rate-level curve, because the m1 values are more
evenly distributed over a wider interval. A positive value of m1
reflects a rate trend similar to the underlying excitatory drive
from auditory nerve fibers and hence suggests relatively weak
inhibitory input. Negative values are taken as an indication of
a relatively stronger inhibitory contribution.
One interpretation of this result is that the apical dendrite
orientation determines the cross-sectional area of the arbor
perpendicular to the trajectory of the parallel fibers and hence
affects the pattern of activity in the apical arbor. For example,
those presenting a narrow face to the parallel fiber network
may be more strongly influenced by inhibitory inputs from the
cartwheel cell population. Although cartwheel cells are known
to be acoustically responsive, their activity is relatively weak
and of high threshold (Ding et al. 1999; Parham and Kim 1995)
and would not be expected to account for the relatively strong
inhibition represented by negative values of m1.
A second possibility is that since the neurons represented in
Fig. 7 come from the ventrolateral third of the nucleus, the
change in apical arbor orientation may result from curvature of
the strial axis in this region (Blackstad et al. 1984). In this case,
the variations in orientation and in slope m1 may, in fact, be
functions of position. That no such dependence was apparent in
our position data may indicate limitations in the accuracy of
mapping position across different tissue samples.
A chance example from the present study illustrates that
significant morphological differences may indeed exist between nearby cells. Figure 9 is a sagittal view of two fusiform
cells, labeled in a single electrode track, their cell bodies
separated by less than 10 ␮m. They were located in the caudal
DCN, and hence, as described earlier, their long axes have a
rostral-to-caudal orientation. The apical arbor of the blackcolored neuron is sparser than that of the gray-colored neuron.
Furthermore, the two basal arbors do not overlap completely,
but follow slightly different trajectories. The results of Fig. 9
support the notion that neighboring fusiform cells might have
markedly different morphologies.
COMPARISON OF DCN FUSIFORM CELL PHYSIOLOGY AND ANATOMY
IV unit receives input from a band of type II units (presumably
vertical cells) centered spatially on BF, then the resulting
inhibitory band would have a lower BF because the vertical
cells are more dense in that direction. Similarly, if the wideband inhibition is stronger in the dorsomedial direction, inhibition from a band spatially centered on BF will itself have a
higher BF. The idea that these two inhibitory sources might
trade for one another across the width of the DCN is consistent
with data presented by Nelken and Young (1994). Their Fig.
8B suggests that the influence of inhibition by type II units, as
measured by the maximum driven BF rate, is negatively correlated with the influence of wideband inhibition, as measured
by the minimum inhibitory notch width.
Conclusion
This report has described differences between cats and gerbils in the anatomical properties of DCN fusiform cells and in
their tonotopic arrangement. The report also described systematic distributions of functional properties within the fusiform
cell population. How such variations contribute to DCN function is yet to be understood.
We thank committee members H. S. Colburn, L. H. Carney, M. C. Liberman, and A. M. Berglund for helpful comments and suggestions. We also
thank D. Oertel for comments and P. Patterson for processing some of the
tissue.
K. E. Hancock was supported by a fellowship from The Whitaker Foundation. This work was funded by Grant DC-01099 from the National Institute on
Deafness and Other Communication Disorders.
Present address of K. E. Hancock: Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, 243 Charles St., Boston, MA 02114.
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FIG. 10. Inhibitory components of a type IV unit response map. Gray,
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