Elsevier

Neuroscience

Volume 162, Issue 2, 18 August 2009, Pages 486-500
Neuroscience

Sensory System
Research Paper
Over-representation of species-specific vocalizations in the awake mouse inferior colliculus

https://doi.org/10.1016/j.neuroscience.2009.04.056Get rights and content

Abstract

Social vocalizations are particularly important stimuli in an animal's auditory environment. Because of their importance, vocalizations should be strongly represented in auditory pathways. Mice commonly emit ultrasonic vocalizations with spectral content between 45 and 100 kHz. However, there is limited representation of these ultra-high frequencies (particularly those greater than 60 kHz) throughout the ascending auditory system. Here, we show that neurons in the inferior colliculus (IC) of mice respond strongly to conspecific vocalizations even though the energy in the vocalizations is above the neurons' frequency tuning curves. This results in an over-representation of species-specific vocalizations in the IC. In addition, neurons in mouse IC show selectivity among different vocalizations. Many vocalization-responsive neurons do not respond to the individual ultrasonic frequencies contained within the vocalizations, but they do respond to combinations of ultrasonic tones if the difference between the tones is within the excitatory frequency tuning curve. The combinations of tones that elicit responses are the quadratic and/or cubic intermodulation distortion components that are generated by the cochlea. Thus, the intermodulation distortions in the cochlea may provide a previously overlooked mechanism for auditory processing of complex stimuli such as vocalizations. The implication of these findings is that nonlinear interactions of frequencies, possibly caused by distortions in the system, may be used to enhance the sensitivity to behaviorally important stimuli.

Section snippets

Surgical procedures

Female CBA/CaJ mice were used in this study. This strain exhibits normal hearing sensitivity well into its second year of life (Willott 1986, Willott 1991, Willott 2005). The care and experimental manipulations of the animals were carried out in accordance with guidelines of the National Institutes of Health and have been approved by the Washington State University Institutional Animal Care and Use Committee. Number of animals used and their suffering was minimized.

To enable extracellular

Results

We recorded well-isolated single unit responses to vocalizations in 102 neurons. These neurons had a range of characteristic frequencies between 6 and 68 kHz with the majority of CFs below 30 kHz (Fig. 1). Seventy-nine neurons responded to at least one of the vocalizations at one or more intensities. Because the focus of this study was on how IC neurons detect and discriminate vocalizations rather than other general properties of IC neurons, only those neurons that responded to at least one

Discussion

There are three main findings of this study. First, some neurons in mouse IC responded to high frequency vocalizations even though their frequency tuning curves were lower than the frequency range of the vocalizations. Second, neural selectivity among conspecific vocalizations occurs in IC. Third, neurons in IC responded to difference tones created by combinations of ultra-high frequencies.

Acknowledgments

This work was supported in part by the National Science Foundation under grants IOS-0620560 to C.V.P. and CRCNS IIS-0827722 to P.D.R.

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