There are three main acoustical cues to sound location, each attributable to space-and frequency-dependent filtering of the propagating sound waves by the outer ears, head, and torso: Interaural differences in time (ITD) and level (ILD) as well as monaural spectral shape cues. While the guinea pig has been a common model for studying the anatomy, physiology, and behavior of binaural and spatial hearing, extensive measurements of their available acoustical cues are lacking. Here, these cues were determined from directional transfer functions (DTFs), the directional components of the head-related transfer functions, for eleven adult guinea pigs. In the frontal hemisphere, monaural spectral notches were present for frequencies from ~10 to 20 kHz; in general, the notch frequency increased with increasing sound source elevation and in azimuth toward the contralateral ear. The maximum ITDs calculated from low-pass filtered (2 kHz cutoff frequency) DTFs were ~250 µs, whereas the maximum ITD measured with low frequency tone pips was over 320 µs. A spherical head model underestimates ITD magnitude under normal conditions, but closely approximates values when the pinnae were removed. Interaural level differences (ILDs) strongly depended on location and frequency; maximum ILDs were < 10 dB for frequencies < 4 kHz and were as large as 40 dB for frequencies > 10 kHz. Removal of the pinna reduced the depth and sharpness of spectral notches, altered the acoustical axis, and reduced the acoustical gain, ITDs, and ILDs; however, spectral shape features and acoustical gain were not completely eliminated, suggesting a substantial contribution of the head and torso in altering the sounds present at the tympanic membrane.
A common way to assess the function of sensory neurons is to measure the number of spikes produced by individual neurons while systematically varying a given dimension of the stimulus. Such measured tuning curves can then be used to quantify the accuracy of the neural representation of the stimulus dimension under study, which can in turn be related to behavioral performance. However, tuning curves often change shape when other dimensions of the stimulus are varied, reflecting the simultaneous sensitivity of neurons to multiple stimulus features. Here we illustrate how one-dimensional information analyses are misleading in this context, and propose a framework derived from Fisher information that allows the quantification of information carried by neurons in multidimensional stimulus spaces. We use this method to probe the representation of sound localization in auditory neurons of chinchillas and guinea pigs of both sexes, and show how heterogeneous tuning properties contribute to a representation of sound source position that is robust to changes in sound level.
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.
Sensory performance is constrained by the information in the stimulus and the precision of the involved sensory system(s). Auditory spatial acuity is robust across a broad range of sound frequencies and source locations, but declines at eccentric lateral angles. The basis of such variation is not fully understood. Low-frequency auditory spatial acuity is mediated by sensitivity to interaural time difference (ITD) cues. While low-frequency spatial acuity varies across azimuth and some physiological models predict strong medial bias in the precision of ITD sensitivity, human psychophysical ITD sensitivity appears to vary only slightly with reference ITD magnitude. Correspondingly, recent analyses suggest that spatial variation in human low-frequency acuity is well-accounted for by acoustic factors alone. Here we examine the matter of high-frequency auditory acuity, which is mediated by sensitivity to interaural level difference (ILD) cues. Using two different psychophysical tasks in human subjects, we demonstrate decreasing ILD acuity with increasing ILD magnitude. We then demonstrate that the multiplicative combination of spatially variant sensory precision and physical cue information (local slope of the ILD cue) provides improved prediction of classic high-frequency spatial acuity data. Finally, we consider correlates of magnitude dependent acuity in neurons that are sensitive to ILDs.
Despite the common use of guinea pigs in investigations of the neural mechanisms of binaural and spatial hearing, their behavioral capabilities in spatial hearing tasks have surprisingly not been thoroughly investigated. To begin to fill this void, we tested the spatial hearing of adult male guinea pigs in several experiments using a paradigm based on the prepulse inhibition (PPI) of the acoustic startle response. In the first experiment, we presented continuous broadband noise from one speaker location and switched to a second speaker location (the "prepulse") along the azimuth prior to presenting a brief, ∼110 dB SPL startle-eliciting stimulus. We found that the startle response amplitude was systematically reduced for larger changes in speaker swap angle (i.e., greater PPI), indicating that using the speaker "swap" paradigm is sufficient to assess stimulus detection of spatially separated sounds. In a second set of experiments, we swapped low- and high-pass noise across the midline to estimate their ability to utilize interaural time- and level-difference cues, respectively. The results reveal that guinea pigs can utilize both binaural cues to discriminate azimuthal sound sources. A third set of experiments examined spatial release from masking using a continuous broadband noise masker and a broadband chirp signal, both presented concurrently at various speaker locations. In general, animals displayed an increase in startle amplitude (i.e., lower PPI) when the masker was presented at speaker locations near that of the chirp signal, and reduced startle amplitudes (increased PPI) indicating lower detection thresholds when the noise was presented from more distant speaker locations. In summary, these results indicate that guinea pigs can: 1) discriminate changes in source location within a hemifield as well as across the midline, 2) discriminate sources of low- and high-pass sounds, demonstrating that they can effectively utilize both low-frequency interaural time and high-frequency level difference sound localization cues, and 3) utilize spatial release from masking to discriminate sound sources. This report confirms the guinea pig as a suitable spatial hearing model and reinforces prior estimates of guinea pig hearing ability from acoustical and physiological measurements.
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