The present report describes the physiology and anatomy of 17 intracellularly recorded and …

• Abstract
• Introduction
• Methods
• Results
• Discussion
• Miscellaneous
• References
• Table 1
• Table 2
• Figures

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 asa basis for comparison of the gerbil to the cat and as a basisfor a subsequent quantitative examination of the relationshipbetween physiology and anatomy. It is important to note that Blackstadet al. limited their consideration to the central third of theDCN and thus avoided effects due to the significant curvatureof the nucleus at its edges. It was not possible to do likewisein our case due to the sample size limitations inherent to anin vivo intracellular survey of thiskind.

The anatomical properties of the apical arbors are summarized in Table 1. Estimates were made of the total dendritic lengthsby summing the lengths of the individual segments comprising eachthree-dimensional (3-D) reconstruction. The mean apical lengthwas 3,359 µm, which is very close to the mean value of 3,212 µmreported by Blackstad et al. (1984) in the cat. The width andthickness measurements were obtained by rotating the arbor aboutits long axis to find the widest and narrowest projections, respectively.Both measures are smaller in the gerbil than in the cat, althoughthe ratio, which reflects the degree of arbor planarity, is approximatelythe same in both cases (2.56 in the gerbil, roughly 3 in the cat).The mean height of the apical arbor, measured parallel to thelong axis, was 157 µm in the gerbil as compared with 267 µm inthe cat.

Table 2 lists the anatomical properties of the basal dendrites in this study. The mean total length was 1,925 µm, as comparedwith 2,728 µm in the cat. The mean arbor width is smaller in thegerbil (314 µm) than in the cat (392 µm), but the thickness islarger (112 vs. 72 µm). The result is that the width to thicknessratio in the gerbil (3.07) is about half that in the cat (5.70).The mean basal arbor is 250 µm in height as compared with 389 µm in the cat. 

Tonotopy

A qualitative illustration of the tonotopic organization is presented in Fig. 2A, in which the 17 fusiform cells of this studyhave been mapped onto a single DCN. Only the basal dendrites havebeen drawn because that is presumably where fusiform cells receiveacoustic input (Smith and Rhode 1985). The dendrites are colorcoded according to BF, as shown. Figure 2A qualitatively suggeststhat the gerbil DCN has a substantial volume devoted to relativelow BFs. The orderly arrangement of cells by BF is also apparent,with the lowest BFs in the rostral-most and ventrolateral-mostaspect of the nucleus.

Figure 2A shows that BF increases in both the dorsomedial and caudal directions. This observation is quantified in Fig. 2Bwhere 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. Thestraight line fits to these data indicate that BF is indeed highlycorrelated with these twodimensions.

The tonotopic axis is described by the equation log(BF) = 1.45Px + 1.01Pz (r = 0.81, P < 0.001), obtained by performing multiplelinear regression on log BF using both the relative X- and Z-positions.A tonotopic position was determined for each neuron by projectingits location onto this axis and computing the distance from theorigin (Px = Pz = 0). The resulting positions are plotted in Fig.3 as a function of BF. For comparison, the place-frequency mapfor the gerbil cochlea is also plotted, where position indicatesthe relative distance from the base of the cochlea. In general,Fig. 3 shows that the spatial distribution of BFs in the DCN closelyfollows the distribution of characteristic frequencies (CFs) alongthe cochlea. For comparison, the place-frequency map computedfor 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 therostral end of the nucleus, the apical dendrites tend to be positionedon the rostral side of the soma while the basal dendrites extendin the caudal direction. Near the center of the DCN, the orientationis roughly vertical (dorsal to ventral). Toward the caudal pole,fusiform cells have caudally directed apical dendrites and rostrallydirected 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 ofthin shells, with the molecular layer wrapped around the fusiformcell layer, which in turn is wrapped around the deep layer. Thusfrom any position within the fusiform cell layer, the apical dendritesradiate outward to fill the molecular layer while the basal dendritesconverge inward to occupy the deep layer. A similar finding wasreported by Rhode et al. (1983), who further describe the cellsin the rostral end having more numerous apical dendrites thatmore frequently emerge directly from the soma. Neither this studynor the previous one finds any obvious physiological sequellaeto this trend, which possibly is simply a consequence of the overallcurvature of thenucleus.

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 intoa low SR group (rate <2.5 spikes/s, 8/17 cells) and a high SRgroup (rate >7.5 spikes/s, 9/17 cells). The creation of two SRcategories may, in fact, represent an artificial division of acontinuously distributed property, but is useful here as a convenientmeans of visualizing a related anatomical trend. Specifically,there is a correlation between spontaneous rate group and thedisposition of the basal dendrites, as depicted in Fig. 5. Thebasal dendrites of the low SR cells (top row) are primarily directedcaudally away from the soma. The high SR cells (bottom row) tendalso to have branches oriented in the rostral direction, givingthe 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 thesoma. The trend is specifically captured by the rostral-caudalcomponent, Z_C, as shown in Fig. 5. Note that the value of Z_C ispositive for positions caudal to the soma. For every low SR cell(Z_C  63.2 µm), the basal arbor centroid is caudal to that ofevery high SR cell (Z_C  48.8 µm). No correlation was found betweenthe absolute position of the basal arbor centroid and spontaneousactivity.

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 arrangementof the basal dendrites, because as described above, the orientationof the fusiform cell long axis changes as a function of position(Fig. 4).

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 dendriticlength. The best line fit to the apical length was computed afterremoving the two points indicated by triangles in Fig. 6A. Thecorrelation with apical length is negative, so that larger lengthscorrespond to smaller resistances. This is consistent with a passivemodel in which membrane conductance is proportional to surfacearea, insofar as dendritic surface area is proportional to totallength. Input resistance was not correlated with the sum of theapical and basal lengths (r = 0.06). The presence of spines,however, greatly increases the surface area per unit length ofthe apical dendrite and so a simple sum of total lengths probablyunderstates the contribution of the apical dendrite to the overallpassive membrane conductance. We did not consider the effectsof surface area more directly because of difficulties estimatingit that arose from inconsistencies in the quality of spine labeling.

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, thetransient slope, m_T, most closely follows the classification schemeof Gdowski (1995). It is particularly sensitive to the changein interspike interval over the initial 5-10 ms of response andsince nearly all of the cells in this study had decreasing intervalsover this range, regardless of their subsequent behavior, thetransient slope was not necessarily an effective means of characterizingrate trends over the entire stimulus duration. To better capturethese rate trends, the slope measurements m₁ and m₂ were computedby performing a two-line fit to the interspike interval data afteromitting the firstbin.

Figure 7 shows that for the 10 fusiform cells with BFs less than 2 kHz, the slope m₁ is correlated with the orientation ofthe apical dendrites. The angle _apical corresponds to the rotationrequired to find the narrowest dendritic profile after makingthe long axis of the arbor vertical. A value of zero correspondsto an arbor oriented perpendicular to the coronal plane. The apicaldendrites in Fig. 7 are drawn looking down on their tops, suchthat their long axes project out of the page. The values of m₁have been divided into three groups: high, medium, and low, indicatedin Fig. 7 by circles, triangles, and squares, respectively. Thedata indicate that the fusiform cells with apical arbors orientedmost nearly perpendicular to the coronal plane have the most positivem₁ values (circles), while those oriented closest to parallelto the coronal plane have the most negative m₁ values (squares).

Correlation of cell properties with location

An effort was made to identify fusiform cell characteristics that vary systematically with location. To do this, a wide varietyof physiological response metrics (see companion paper) were systematicallycorrelated 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 decreasedin the X-direction (ventrolateral to dorsomedial), meaning thatthe responses to noise became progressively weaker in this direction(Fig. 8A). A gradient in wideband inhibitory strength is sufficientto account for this observation, as detailed in the DISCUSSION.The second trend was that input resistance also tended to decreasein the X-direction (Fig. 8B). This is consistent with the factthat total apical dendritic length increases in the same direction(Fig. 8C), since the inverse relationship between these two propertieshas already been described.

Aside from tonotopy, the only statistically significant spatial trends were found in the X-direction. Since neither trendwas accompanied by a significant dependence on Z-position, itwas not possible to compute an axis trajectory for quantitativecomparison with the tonotopic axis computed above. It can, however,be said that while best frequency is strongly correlated withboth X- and Z-position, input resistance and relative noise responseare strongly correlated only with X-position. So, although theseresults cannot resolve the issue of an orthogonal axis per se,there is at least a qualitative suggestion that the spatial gradientsof these two properties are not parallel with the frequencyaxis.