Development of the head, pinnae, and acoustical cues to sound location in a precocial species, the guinea pig (Cavia porcellus)

Abstract

The morphology of the head and pinna shape the spatial and frequency dependence of sound propagation that give rise to the acoustic cues to sound source location. During early development, the physical dimensions of the head and pinna increase rapidly. Thus, the binaural (interaural time and level differences, ITD and ILD) and monaural (spectral shape) cues are also hypothesized to change rapidly. Complex interactions between the size and shape of the head and pinna limit the accuracy of simple acoustical models (e.g. spherical) and necessitate empirical measurements. Here, we measured the cues to location in the developing guinea pig, a precocial species commonly used for studies of the auditory system. We measured directional transfer functions (DTFs) and the dimensions of the head and pinna in guinea pigs from birth (P0) through adulthood. Dimensions of the head and pinna increased by 87% and 48%, respectively, reaching adult values by ∼8 weeks (P56). The monaural acoustic gain produced by the head and pinna increased with frequency and age, with maximum gains at higher frequencies (>8 kHz) reaching values of 10-21 dB for all ages. The center frequency of monaural spectral notches also decreased with age, from higher frequencies (∼17 kHz) at P0 to lower frequencies (∼12 kHz) in adults. In all animals, ILDs and ITDs were dependent on both frequency and spatial location. Over development, the maximum ILD magnitude increased from ∼15 dB at P0 to ∼30 dB in adults (at frequencies >8 kHz), while the maximum low frequency ITDs increased from ∼185 μs at P0 to ∼300 μs in adults. These results demonstrate that the changes in the acoustical cues are directly related to changes in head and pinna morphology.

Keywords: Development; Guinea pig; Head related transfer function; Interaural level difference; Interaural time difference; Sound localization.

Figure 1

Measurements of head and pinna dimensions in the developing guinea pig. A: Head diameter was measured as the widest part of the skull (between points AB; see inset) as well as from P0 through P165 in 50 animals. Measurements between the ear canals were also taken (interaural distance; A’B’). B: Effective pinna diameter was calculated by measuring pinna height (CD) and pinna width (EF; see inset for equation) in 20 animals. Data points in A and B indicate single animal measurements. The dashed line and gray area indicate the mean and associated standard deviation, respectively, for the adult animal population (>P70; data points compiled on far right). Dimensions of the head and pinna increased by factors of 2.4 and 1.56, respectively, reaching adult values by ~8 weeks (P56).

Figure 2

Monaural DTF gain varies with frequency, source direction, and magnitude across animals at different ages. A: Spatial distribution of DTF gains for six frequencies for the left ear (+90° is ipsilateral) of three animals aged P0, P14, and P56 (adult). The maximum gain for each frequency shown (frequency listed on left side of every row) is given on the upper right side of each panel (italicized grey text). The contours are plotted at −5 dB intervals from the maximum gain. The color bar indicates the gain in decibels (dB), with the warmer colors indicating the positive gain with respect to the left ear. “+” indicates the origin 0°, 0°. B: Schematic representation of the speaker positions for the gain plots in (A). C: Maximal gain (dB) in the DTFs as a function of frequency for example animals aged P0 (red), P28 (green), and P56 (blue). Maximal gain is shown for both frontal and back hemispheres. The vertical dotted lines indicate the frequency at which the peak in acoustic gain (dB) occurs for each animal. D: Maximal gain as a function of age for all animals tested. Data from both left and right ears are shown. E: Frequency of peak maximal gain as a function of age. >P70 data in both E, F are from Greene et al., 2014.

Figure 3

Spatial location of the acoustic axis for azimuth (A) and elevation (B) as a function of frequency for animals aged P0 (red), P28 (green), P42 (light blue), and P56 (blue). Vertical lines in (B) indicate frequencies at which discrete transitions occur in the location of the acoustic axes with changes in sound source elevation. C: The frequency of the discrete transitions in acoustic axes (with changes in elevation) as function of age for all animals. The black line is the fitted exponential decay function. D: Linear regression (black line) between the frequency of acoustic axis shift in elevation and the effective pinna diameter.

Figure 4

Monaural broadband spectral notches shift systematically with age and are largely produced by the pinna. A: DTF gain as a function of frequency for locations varying in elevation ranging from −45° to +90° in 7.5° increments (at 0° azimuth) for animals aged P0 (red, top panel), P28 (green, middle panel), and P56 (adult; black, bottom panel). Vertical lines indicate the frequency of the first spectral notch (first notch frequency, FNF). B: The prominent spectral notches present in (A) are largely eliminated following pinna removal.

Figure 5

Frequency- and spatial-dependence of ILD at different ages. Spatial distributions of ILD are shown for seven frequencies in animals aged P0, P28, and P56 (adult). Each column shows data from a representative animal at each age, and each row shows data from a different frequency (2, 4, 8, 12, 14, 16, and 20 kHz). The maximum ILD for each frequency shown is depicted on the upper right side of each panel (italicized grey text). The color bar indicates the ILD magnitude in decibels (dB), with positive ILD (warmer colors) indicating higher sound level (dB) at the left ear vs. the right ear.

Figure 6

Development of ILD along the horizontal plane. A: ILD as function of azimuth and frequency (kHz) for animals aged P0 (left panel), P28 (middle panel), and P56/adult (right panel). Measurements are shown for 25 locations in azimuth (+90° to −90°) in 7.5° increments at 0° elevation. The color bar indicates the ILD magnitude in decibels (dB), with positive ILD (warmer colors) indicating higher sound level (dB) at the left ear vs. the right ear. B: ILD (dB) at 75° azimuth as a function of frequency for animals at all ages tested. Vertical lines indicate the peak in ILD spectra. Ages with the corresponding color remain consistent throughout the figure. C: Peak ILD at 75° azimuth as a function of age. >P70 data from Greene et al., 2014. D, E: ILD at 75° azimuth for the P0 and P28 animal shown in (A) with pinna intact (solid line) and following pinna removal (dotted line). Dotted grey line: predicted ILD using the spherical head model (Duda and Martens, 1998). F: Peak ILD with pinna intact and following pinna removal. G: Sum of differences comparison of the spherical head model to the empirically-measured ILDs (normalized to “pinna intact” condition).

Figure 7

Frequency- and spatial-dependence of ITD at different ages. A: ITD (µs) vs frequency (Hz) for sound sources in the frontal plane for example animals aged P0 (left panel, red), P28 (middle panel, green) and P56/adult (right panel, blue). Each line corresponds to measurements taken from 25 locations in azimuth (+90° to −90°) in 7.5° increments. Gray bands indicate the low frequency range (500–800 Hz) and high frequency range (3–3.5 kHz) of ITDs used to compute low and high frequency ITDs, respectively. B: Fitted ITD as a function of source azimuth along the horizontal plane (0° elevation) for animals of varying ages, from P0 through adulthood (see legend). The asterisk (*) indicates the P56 animal shown in A (right panel). C, D: Maximum ITD as a function of age (n=11); colors correspond to the legend in (B). The dotted line indicates the linear regression of maximum ITD on head diameter for low frequency ITDs (C) and high frequency ITDs (D). The solid black line in (C) indicates the ITD prediction from the spherical head model of low frequency ITDs proposed by Kuhn (1977). The solid black line in (D) indicates the ITD prediction from the spherical head model of high frequency ITDs proposed by Woodworth (1938). E: Low frequency ITD (left panel) and high frequency ITD (right panel) as a function of azimuth for five animals. Solid lines indicate “pinna intact” condition, dotted lines indicate “no pinna” condition, and grey lines indicate the Kuhn (left panel) or Woodworth (right panel) ITD predictions. F: Pinna effect on the magnitude of low and high frequency ITDs. The effect is expressed in terms of percentage ([ITD_pinna/ITD_nopinna − 1]*100) averaged over all subjects from (E). Each grey data point is a different azimuthal position from 30° to 150° on either side (the small ITDs between ±29° were excluded). Error bars indicate standard deviation.

Figure 8

Estimated development of the resonance frequency, concha/ear canal length (A), and acoustic gain (B). The gain and resonance frequency were estimated from the nondirectional common components of the DTFs in 20 animals. A: Black solid line indicates the three-parameter exponential decay function relating the concha/canal resonance frequency to age (days). Red dotted line indicates the concha/canal length (in millimeters) estimated from the fitted resonance frequency function and assuming that the canal/concha can be modeled as a simple cylinder (see text). Red circles: empirical measurements of concha/canal length in 4 animals (2 canals per animal). B: The gray solid line indicates the three-parameter rise-to-max exponential function relating concha/canal resonance gain to age.

Figure 9

Variability in pinna orientation. Examples of three different guinea pig pinna morphological features: symmetric upright (A), symmetric floppy (B), and asymmetric (C). D–F: Spatial distribution of left and right ear DTF gains at 12 kHz for example animals with symmetric upright (D), symmetric floppy (E), and asymmetric (F) pinna. Contour line is plotted at -5 dB from the maximum DTF gain. G–I: ILD at +75° (red line) and −75° (blue line) azimuth as a function of frequency (at 0° elevation) for symmetric upright (G), symmetric floppy (H), and asymmetric (I) pinna. Examples shown are the same animals depicted in (D–F). J–L: Broadband ITD (µs) vs azimuth for example animals with symmetric upright (J), symmetric floppy (K), and asymmetric (L) pinna.