Sound localization cues in the marmoset monkey

Abstract

The most important acoustic cues available to the brain for sound localization are produced by the interaction of sound with the animal's head and external ears. As a first step in understanding the relation between these cues and their neural representation in a vocal new-world primate, we measured head-related transfer functions (HRTFs) across frequency for a wide range of sound locations in three anesthetized marmoset monkeys. The HRTF magnitude spectrum has a broad resonance peak at 6-12 kHz that coincides with the frequency range of the major call types of this species. A prominent first spectral notch (FN) in the HRTF magnitude above this resonance was observed at most source locations. The center frequency of the FN increased monotonically from approximately 12 to 26 kHz with increases in elevation in the lateral field. In the frontal field FN frequency changed in a less orderly fashion with source position. From the HRTFs we derived interaural time (ITDs) and level differences (ILDs). ITDs and ILDs (below 12 kHz) varied as a function of azimuth between +/-250 micros and +/-20dB, respectively. A reflexive orienting behavioral paradigm was used to confirm that marmosets can orient to sound sources.

Figure 1

Signal processing steps to compute the HRTF. A. Impulse response computed using the Golay method of a speaker located at 0° AZ and 0° EL in free field. The microphone and probe tube were placed at approximately the same position in the room as if in the ear canal, but no animal was present. Reflections from the wall are evident. The Hanning window used to smooth the signals is shown. B. Impulse response for the same speaker and microphone placement, except recorded in the ear canal. The impulse response is shown after the window was applied. C. Spectra of the un-windowed impulse responses in the ear canal and free field, as the magnitude of the Fourier transforms of the signals. The dB scale is arbitrary, with 0 dB at the peak amplitude. The noise floor was measured with the probe tube filled with modeling clay. D. Magnitude of the HRTF for the signals in C unwindowed (gray line) and windowed (black line).

Figure 2

The external ear of the marmoset. A. A scale sketch of the left profile of marmoset 9N. Hair tufts have been removed to expose the pinna. B. A tracing of a horizontal section through the right ear (marmoset 77T), looking downward from above. The middle and inner ear are also shown. The approximate height of the section is indicated by the gray line in Fig. 1A. The white asterisk in the ear canal indicates the approximate position of the probe tube during the measurements. (A = anterior, M = medial.)

Figure 3

Comparison between HRTFs and DTFs. A. The individual HRTF (red), average HRTF (green), and individual DTF (blue) measured in the right ear at 0° AZ and 0° EL in marmoset 9N. A. The individual HRTF (red), average HRTF (green), and individual DTF (blue) measured in the right ear at 120° AZ and -7.5° EL.

Figure 4

Magnitudes of HRTFs from 15 speaker positions, as indicated in the figure. HRTFs are shown for both ears, the right ear as the black line (AZ is positive to the right) and the left ear as the red line.

Figure 5

Magnitudes of HRTFs from three spatial regions, in front of the animal (A), above the animal (B), and behind the animals (C). In each case a notch-free ILD region is present at frequencies below 12 kHz, a first-notch (FN) region between 12-24 kHz, and a high frequency (HF) region above 24 kHz.

Figure 6

A. B. Magnitudes of HRTFs for a range of AZs, identified in the legend, at 0° EL. Data from two animals are shown. C,D. ILDs computed from the data in A and B as the difference of the HRTFs in A and B at corresponding left and right AZs.

Figure 7

ILDs averaged across three frequency bands are shown as a function of AZ and EL plotted on a Mollweide equal area projection. The dots indicate the location of the ear canals. A. B. Results for frequencies in the ΔL region. C. Results from the FN frequency region.

Figure 8

Examples of spectral cues in four regions of space. The main plots show magnitudes of HRTFs measured at locations in the frontal field (A,B) and the lateral field (C,D) for changes in EL (A,C) and AZ (B,D). The FN region is expanded in the insets.

Figure 9

Spherical contour plots of FN frequency as a function of AZ and EL for the three animals. These are for HRTFs in the right ear (dot). The regions without reliable FNs, as defined in the text, are blank. Some regions contain high frequency FNs that saturate the color scale (red).

Figure 10

Magnitudes of HRTFs for five positions in the median plane, showing the spectral cues that accompany the mostly zero binaural cues.

Figure 11

Similarity of HRTFs across different animals. Magnitudes of HRTFs are shown for four source positions in three different animals, coded by color. Data for the left (dotted lines) and right (solid lines) ears are shown. In Fig. 11C,D the azimuth (+/- 105°) is ipsilateral to the ear.

Figure 12

ITD measurements. A. IPD versus frequency measured at different AZs in the frontal field (0° EL). ITDs are the slopes of the lines. Note the discontinuities in the FN region. B. ITD versus AZ in the frontal field (0° EL) measured in 3 monkeys (colored lines). The black curve is a theoretical prediction from the Woodworth model for a head radius of 2.5 cm. C. A contour plot of ITD at different locations relative to the ears (dots).

Figure 13

Reflexive sound localization behavior in marmosets. A, Example of the elevation change measured during a gaze shift in response to a noise stimulus (top) located at 0° AZ and 60° EL. The green box indicates the movement and the red line indicates the period over which the response was calculated. B, Behavioral gaze shifts to sources located at 0° EL and +60° (red) and -60° (blue) AZ. The noise stimulus was lowpass filtered at 8 (blue) or 30 kHz (red). The arrows indicate the movement direction between the initial and final position (dots). The inset shows ΔEL versus ΔAZ normalized by the initial distance to the target. C, Behavioral gaze shifts to sources located at 60° EL and 0° AZ. The noise stimulus was lowpass filtered at 8 (blue) or 30 kHz (red). The arrows indicate the movement direction between the initial and final position (dots). The inset shows the ΔEL normalized by the initial distance to the target versus ΔAZ. One response is not shown in the inset. The response was to the noise lowpass filtered at 30 kHz and had a ΔEL/distance to target = -1.27 and ΔAZ = 50.