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First published online June 13, 2008
Journal of Experimental Biology 211, 2105-2115 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016204
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The morphology and mechanical sensitivity of lateral line receptors in zebrafish larvae (Danio rerio)

William J. Van Trump* and Matthew J. McHenry

Department of Ecology and Evolutionary Biology, 5205 McGaugh Hall, University of California at Irvine, Irvine, CA 92697-2525, USA


Figure 1
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  		Fig. 1. Morphology of the lateral line system of zebrafish larvae. (A) Lateral and (B) dorsal views illustrate the distribution of neuromasts along the body, grouped by region (Harris et al., 2003Go). The supraorbital region (blue) includes the preoptic (PO) and supraorbital (SO) neuromasts. The infraorbital region (gold) includes the mandibular (M), infraorbital (IO) and opercular (OP) neuromasts. The caudal–cranial region (purple) includes the otic (O), occipital (OC), dorsal (D) and middle (MI) neuromasts. Finally, the posterior (P) neuromasts are located in the trunk region (green). (C) The morphology of an individual neuromast illustrates its major anatomical features. Four hair cells have been highlighted to clarify the major features of each cell. Scale bar, 10 µm.

 

Figure 2
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  		Fig. 2. The method of 3D micromorphometrics. (A) In this set-up the larva is positioned beneath the water-immersion objective of a compound microscope. The microscope is free to translate in three dimensions to interrogate microscopic features within the specimen. (i–iv) The position of these features is measured with the aid of a custom-designed computer program that first (i) captures digital photographs of the microscope field of view. Each photograph captures morphology at a particular optical plane with the z-position determined by the microscope focus. (ii) The user selects landmarks from this image. Once the user has entered the position of the microscope objective in global coordinates, (iv) the 3D positions of landmarks are calculated (see Materials and methods for details). (B) These coordinates are described with respect to the central axis of the body (dashed line), which is defined by points at the rostrum and tail tip. (C) The seven landmarks from a neuromast were used to calculate the cupular height (hc), kinocilia height (hk), base diameter (db) and diameter at the kinocilia height (dk).

 

Figure 3
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  		Fig. 3. Mathematical modeling of the mechanics of superficial neuromasts. (A) The cupula of the neuromast is modeled as two beams joined end-to-end. The distal beam (light grey) is rigidly fixed to the proximal beam (dark grey), which is anchored to the body with a pinned joint and torsion spring with a stiffness equal to that of the hair bundles. This cupula is excited by a boundary layer of flow acting over the surface of the body, which is modeled as a flat plate. This model predicts the frequency response (B,C) of the sensitivity of cupular deflections to flow. (B) The amplitude of sensitivity (Eqn 7) was used to find the peak amplitude and cut-off frequency of the frequency response (see Materials and methods for details). (C) The phase of cupular sensitivity is defined with respect to the local flow velocity.

 

Figure 4
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  		Fig. 4. The frequency distribution of morphological measurements. The total number of measurements for each region of the (A) cranial and (B) trunk regions of the body. The color-coded regions of the lateral line system correspond to the neuromast locations illustrated in Fig. 1.

 

Figure 5
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  		Fig. 5. Morphological measurements and predicted frequency responses for different regions of the body. The distribution of data is shown for each locus with box and whisker plots. In each box, the center line represents the median value, the upper and lower bounds of the box represent the interquartile range, and the whiskers represent the total range. Outliers defined as exceeding 1.5 times the interquartile range are denoted by a plus sign. Data are shown for (A) cupula height (hc), (B) kinocilia height (hk), (C) cupula diameter at kinocilia tips (dk), (D) cupula diameter at its base (db), (E) peak amplitude and (F) cut-off frequency of the predicted frequency responses. Sample sizes and other statistics from these data are provided in Table 1.

 

Figure 6
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  		Fig. 6. The frequency responses modeled from morphological measurements. The predicted amplitude (upper panels) and phase (lower panels) of sensitivity are shown by transparent gray lines for all recorded neuromasts. Therefore dark regions of the drawn lines demonstrate a high degree of overlap in the frequency responses of neuromasts. (B) All neuromasts for a representative individual (11 d.p.f.) are highlighted (red lines) to demonstrate the degree of variation that may be exhibited within a larva. (C) Neuromasts at a particular locus (P8) are highlighted (red lines) for all individuals sampled.

 

Figure 7
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  		Fig. 7. The effects of morphological parameters on peak amplitude and cut-off frequency. In each plot, blue dots indicate predictions of peak amplitude (upper panels) and phase (lower panels) made from each neuromast measured. The green line shows the model predictions where only the independent variable is permitted to vary. The coefficient of determination (r2) was calculated from a comparison of these relationships to indicate the degree of variation that is caused by the independent variable. The independent variables examined were (A) cupula height (hc), (B) kinocilia height (hk), (C) cupula diameter at kinocilia tips (dk), (D) cupula diameter at its base (db) and (E) the number of kinocilia.

 

Figure 8
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  		Fig. 8. Differences in cupular morphology and frequency response for larvae of different ages. In each box, the center line represents the median value, the upper and lower bounds of the box represent the interquartile range, and the whiskers indicate the total range. Outliers defined as exceeding 1.5 times the interquartile range are denoted by a plus sign. Measurements for (A) cupula height (hc), (B) kinocilia height (hk), (C) cupula diameter at kinocilia tips (dk), (D) cupula diameter at its base (db), (E) peak sensitivity and (F) cut-off frequency are presented for multiple individuals. These data are shown for larvae at 3 d.p.f. both (i) prior to (N=5) and (ii) after hatching (N=5), and at (iii) 4 d.p.f. (N=3) and (iv) 5–20 d.p.f. (N=13) using the mean values among neuromasts for individual larvae. The letters (a, b or c) indicate statistical groups as determined by one-way ANOVA with a post-hoc comparison using Tukey's least significant difference procedure such that two ages must not share any statistical groups to be considered statistically different.

 

Figure 9
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  		Fig. 9. The proposed effect of variation in cupular height on the dynamic range of the lateral line system. (A) A region of the body encompassing three neuromasts is focused on (box) for a comparison of responses for a lateral line with cupulae of (Bii,Cii) variable height and (Bi,Ci) uniform height. (Bi,Bii) An oscillatory stimulus (blue arrow) causes greater deflection in neuromasts with taller cupulae. (Cii) The tallest and most sensitive neuromast (blue line) is anticipated to produce a transducer potential that saturates at a relatively low flow velocity. The gray lines indicate sensitivity that is dominated by the mechanics of the cupula. In contrast to the tallest cupula, the shortest cupula (green line) is less sensitive, but encodes flow at higher velocity. Therefore, the dynamic range of the entire system (gray region) is large compared with that of a lateral line system composed of neuromasts with uniform morphology (Ci). (Bi,Ci) Neuromasts having similar cupular height will deflect to the same degree and produce similar transducer potentials. As a consequence, the dynamic range for the system will be relatively narrow.

 

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