Elsevier

Hearing Research

Volume 265, Issues 1–2, 14 June 2010, Pages 54-62
Hearing Research

Research paper
Laboratory rats (Rattus norvegicus) do not use binaural phase differences to localize sound

https://doi.org/10.1016/j.heares.2010.02.011Get rights and content

Abstract

The ability of Norway rats to use binaural time- and intensity-difference cues to localize sound was investigated by determining their ability to localize pure tones from 500 Hz to 32 kHz. In addition, their ability to use the binaural time cues present in the envelope of a signal was determined by presenting them with a 1-kHz tone that was amplitude modulated at either 250 or 500 Hz. Although the animals were easily able to localize tones above 2 kHz, indicating that they could use the binaural intensity-difference cue, they were virtually unable to localize the lower-frequency stimuli, indicating that they could not use the binaural phase (time) cue. Although some animals showed a residual ability to localize low-frequency tones, control tests indicated that they were using the transient interaural intensity difference in the onset of a sound that exists after it reaches the near ear but before it reaches the far ear. Thus, in contrast to earlier studies, we conclude that the Norway rat is unable to use the ongoing time cues available in low-frequency tones to localize sound, raising the possibility that the rat may not use interaural time 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

References (37)

  • Heffner, R.S., Heffner, H.E., 1987. Localization of noise, use of binaural cues, and a description of the superior...
  • H.E. Heffner et al.

    Effect of bilateral auditory cortex lesions on sound localization in Japanese macaques

    J. Neurophysiol.

    (1990)
  • H.E. Heffner et al.

    Conditioned avoidance

  • H.E. Heffner et al.

    Audition

  • H. Heffner et al.

    Contribution of auditory cortex to hearing in the monkey Macaca mulatta

  • R.S. Heffner et al.

    Sound localization in the new-world frugivorous bat, Artibeus jamaicensis: acuity, use of binaural cues, and relationship to vision

    J. Acoust. Soc. Am.

    (2001)
  • Heffner, R.S., Koay, G., Heffner, H.E., 2010. Use of binaural cues for sound localization in two non-echolocating bats:...
  • P. Heil et al.

    First-spike timing of auditory-nerve fibers and comparison with auditory cortex

    J. Neurophysiol.

    (1997)
  • Cited by (29)

    • High frequency sensitivity to interaural onset time differences in the bat inferior colliculus

      2021, Hearing Research
      Citation Excerpt :

      The current evidence does not suggest that transient ITDs are the dominant cue in azimuthal sound localization in bats, but rather that they serve as a weak binaural cue that could contribute to overall azimuthal localization performance, particularly in ambiguous environments as has been demonstrated in human psychoacoustical studies (Buell et al; 1991; Buell et al., 2008). In Norway rats, shortening the duration of a low frequency (1 kHz) tone improved rather than hindered rats’ ability to localize a sound source, suggesting enhanced sensitivity to the transient onset cue over the ongoing phase cue (Wesolek et al., 2010). Behavioral sensitivity to onset ITDs has also been demonstrated in Wister rats capable of lateralizing sharp onset rectangular windows of pulse-resonance sounds during a two-alternative forced choice sound lateralization task (Li et al., 2019).

    • Neuronal sensitivity to the interaural time difference of the sound envelope in the mouse inferior colliculus

      2020, Hearing Research
      Citation Excerpt :

      There are small animals like the Jamaican fruit bat and common vampire bat, similar in size to mice, that can use the envelope ITD as a sound localization cue (Heffner et al., 2001, 2015), although other species of bats could not localize an AM tone with a low-frequency carrier (Heffner et al., 2010a, 2010b). In laboratory rats, sound localization performance may be enhanced by amplitude modulation (Wesolek et al., 2010). Furthermore, a recent study showed that the rats could detect the ITD in the envelope (Li et al., 2019).

    • Spatial hearing ability of the pigmented Guinea pig (Cavia porcellus): Minimum audible angle and spatial release from masking in azimuth

      2018, Hearing Research
      Citation Excerpt :

      These results thus suggest that guinea pig MAA is between 3.75° and 7.5°. Laboratory rats, another common model used in the study of the auditory system, do not appear to discriminate between two sound sources within a hemifield, and show few deficits in sound localization ability following lesion of auditory cortex (Heffner and Heffner, 1985; Heffner et al., 1994a; Kavanagh and Kelly, 1986; Kelly, 1980; Kelly and Kavanagh, 1986; Wesolek et al., 2010). We investigated the guinea pig's ability to discriminate sound sources within a hemifield using a similar SSwap task as described above, using a broadband noise CS, but with the animal cage rotated 45° to the right (Fig. 5A).

    • Spectral and temporal auditory processing in the superior colliculus of aged rats

      2017, Neurobiology of Aging
      Citation Excerpt :

      Whereas, only a small percentage (adult rats: 7%; aged rats: 2%) of them responded to CFs ≤4 kHz. According to Wesolek et al. (2010), rats have rather a greater ability to localize tones above 2 kHz, indicating therefore that they are more likely prone to use the binaural level-difference to localize high-frequency tones present in the envelope of a signal. Undoubtedly, this could explain in part why only a few auditory neurons were sensitive to CF tones ≤4 kHz.

    View all citing articles on Scopus
    1

    Present address: The College of Mount Saint Vincent, 6301 Riverdale Ave., Riverdale, NY 10471, USA.

    View full text