Research paperLaboratory rats (Rattus norvegicus) do not use binaural phase differences to localize sound
Introduction
The ability of mammals to localize sound varies among species not only in acuity, but also in the use of the two binaural locus cues: the difference in the time of arrival of a sound at the two ears and the difference in the frequency-intensity spectra reaching the two ears. Although it appears that most mammals use both binaural cues, some, such as horses and cattle, use only the binaural time-difference cue, whereas others, such as house mice and big brown bats, appear to use only the binaural spectral-difference cue. A few mammals, such as some subterranean rodents, have lost the ability to localize brief sounds altogether and thus do not use either binaural cue (for a review, see Heffner and Heffner, 2003).
The ability of an animal to use the two the binaural cues can be investigated by training it to localize the source of single, brief tone pips (e.g., Masterton et al., 1975), a procedure first used with humans (Mills, 1972, Stevens and Newman, 1936). Specifically, the ability to localize pure tones too low in frequency to generate binaural intensity differences (because they bend around the head with little attenuation) indicates the ability to use the binaural phase cue, which is a binaural time cue (e.g., Zhang and Hartmann, 2006). The ability to localize pure tones too high in frequency to provide a binaural phase cue (because successive cycles arrive too quickly for the nervous system to match the arrival of the same cycle at the two ears) indicates the ability to use the intensity-difference cue, a special case of the binaural frequency-intensity spectral cue. Among species that use the binaural phase cue, the upper-frequency limit for its use spans more than three octaves, from the 500-Hz upper limit of cattle to the 6.3-kHz upper limit of the Jamaican fruit bat (Heffner and Heffner, 2003). Thus, a comparative study of the upper limit of the use of the binaural phase cue could lead to an understanding of the reasons for this variation, and perhaps of the reasons why some species forego the use of the cue altogether.
In comparing the use of the binaural locus cues by different species, we noted that there was disagreement regarding the highest frequencies at which laboratory rats can use the binaural phase cue. Specifically, Masterton and his colleagues (1975) placed the upper limit for rats between 4 and 8 kHz whereas Kelly and Kavanagh (1986) placed it between 2 and 4 kHz. Because our comparative analysis required a more precise estimate of the upper limit for binaural phase, we decided to test laboratory rats ourselves to determine which estimate was correct. What we found, however, was that we were unable to replicate either upper limit; instead, it appears that laboratory rats are unable to use the binaural phase-difference cue at all. As described in Section 4, this finding is not incompatible with the results of anatomical and physiological studies of sound localization in the rat.
Section snippets
Methods
Four rats were trained to localize the source of brief pure tones at a fixed angle of 30° left and right of midline (60° total separation) using a conditioned-suppression avoidance procedure. The ability to localize pure tones below the frequency at which the phase cue becomes ambiguous indicates the use the binaural phase-difference cue whereas the ability to localize pure tones above the frequency of phase ambiguity indicates the ability to use the binaural intensity-difference cue.
Results
We found that although the rats easily localized high-frequency tones, indicating that they could use the binaural intensity-difference cue, they could not localize low-frequency tones, indicating that they could not use the binaural phase cue. Because the inability to localize low-frequency tones differed from the results of the two previous studies (Masterton et al., 1975, Kelly and Kavanagh, 1986), and because the performances of some of the animals on low-frequency stimuli were ambiguous,
Discussion
The original purpose of this study was to determine the highest frequency at which rats could use the binaural phase cue to localize sound. Instead, the results of our tests indicated that the rats could not localize low-frequency tones and therefore were incapable of using phase cues to localize sound. Although there was some residual ability to localize 1-kHz tones (Fig. 1, Fig. 3), control tests indicated that this was due to the transient interaural intensity difference that exists between
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Present address: The College of Mount Saint Vincent, 6301 Riverdale Ave., Riverdale, NY 10471, USA.