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An Overrepresentation of High Frequencies in the Mouse Inferior Colliculus Supports the Processing of Ultrasonic Vocalizations.

Garcia-Lazaro JA, Shepard KN, Miranda JA, Liu RC, Lesica NA - PLoS ONE (2015)

Bottom Line: Auditory brainstem response measurements suggested stronger responses in the midbrain relative to the periphery for frequencies higher than 32 kHz.This result was confirmed by single- and multi-unit recordings showing that high ultrasonic frequency tones and vocalizations elicited responses from only a small fraction of cells in the periphery, while a much larger fraction of cells responded in the inferior colliculus.These results suggest that the processing of communication calls in mice is supported by a specialization of the auditory system for high frequencies that emerges at central stations of the auditory pathway.

View Article: PubMed Central - PubMed

Affiliation: Ear Institute, University College London, 332 Grays Inn Road, London, WC1X 8EE, United Kingdom.

ABSTRACT
Mice are of paramount importance in biomedical research and their vocalizations are a subject of interest for researchers across a wide range of health-related disciplines due to their increasingly important value as a phenotyping tool in models of neural, speech and language disorders. However, the mechanisms underlying the auditory processing of vocalizations in mice are not well understood. The mouse audiogram shows a peak in sensitivity at frequencies between 15-25 kHz, but weaker sensitivity for the higher ultrasonic frequencies at which they typically vocalize. To investigate the auditory processing of vocalizations in mice, we measured evoked potential, single-unit, and multi-unit responses to tones and vocalizations at three different stages along the auditory pathway: the auditory nerve and the cochlear nucleus in the periphery, and the inferior colliculus in the midbrain. Auditory brainstem response measurements suggested stronger responses in the midbrain relative to the periphery for frequencies higher than 32 kHz. This result was confirmed by single- and multi-unit recordings showing that high ultrasonic frequency tones and vocalizations elicited responses from only a small fraction of cells in the periphery, while a much larger fraction of cells responded in the inferior colliculus. These results suggest that the processing of communication calls in mice is supported by a specialization of the auditory system for high frequencies that emerges at central stations of the auditory pathway.

No MeSH data available.


Related in: MedlinePlus

Auditory nerve responses to tones and vocalizations.(A) FRA of a representative auditory nerve fiber. FRAs were constructed from the responses elicited by tones of varying frequency (x-axis) and intensity (y-axis). (B) FRA of one AN fiber that was responsive to high frequency tones. The white arrow marks the location of a spectral notch created by the pinna. (C) Histogram of the distribution of CFs across the population of AN fibers. (D) Sound pressure waveforms (top panel) and spectrograms (lower panel) for the nine different CBA/Ca mouse vocalizations we tested. Note that all the vocalizations span a frequency range from 60–90 kHz. (E) PSTH of the response of the same fiber to a single mouse vocalization with a duration of 60 ms and averaged over 256 repeats. The spectrogram and sound pressure waveforms are shown at the top and bottom panels respectively. (F) Responsiveness to vocalizations. Each point indicates the SNR for one fiber as a function of the highest frequency for which its responses to tones were significantly greater than its spontaneous activity (Fmax). SNR values were averaged across the 9 different calls we tested.
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pone.0133251.g002: Auditory nerve responses to tones and vocalizations.(A) FRA of a representative auditory nerve fiber. FRAs were constructed from the responses elicited by tones of varying frequency (x-axis) and intensity (y-axis). (B) FRA of one AN fiber that was responsive to high frequency tones. The white arrow marks the location of a spectral notch created by the pinna. (C) Histogram of the distribution of CFs across the population of AN fibers. (D) Sound pressure waveforms (top panel) and spectrograms (lower panel) for the nine different CBA/Ca mouse vocalizations we tested. Note that all the vocalizations span a frequency range from 60–90 kHz. (E) PSTH of the response of the same fiber to a single mouse vocalization with a duration of 60 ms and averaged over 256 repeats. The spectrogram and sound pressure waveforms are shown at the top and bottom panels respectively. (F) Responsiveness to vocalizations. Each point indicates the SNR for one fiber as a function of the highest frequency for which its responses to tones were significantly greater than its spontaneous activity (Fmax). SNR values were averaged across the 9 different calls we tested.

Mentions: We began by recording responses from the auditory nerve. We used established physiological criteria to differentiate AN fibers from CN neurons (see Methods and S1 Fig). We isolated 94 fibers recorded from 23 animals. Fig 2A and 2B show FRAs for two representative fibers (the spectral notches created by the pinna are evident in Fig 2B). Across our sample population, the most commonly occurring CFs were between 20 and 30 kHz (Fig 2C). This is consistent with the distribution of CFs observed in a previous study of the mouse AN [13]. We also recorded the responses of AN fibers to conspecific vocalizations with frequencies between 60 and 90 kHz (the sound pressure waveforms and spectrograms are shown in Fig 2D). To determine whether a vocalization evoked a significant response, we compared the distribution of driven spike counts to the distribution of spontaneous spike counts (Wilcoxon rank-sum test, p < 0.05). Fibers were regarded as responsive if statistically significant responses were evoked by at least 3 of the 9 different vocalizations we tested. Only a small number of fibers (7 out of 94 ≈ 7%; 95% CI via bootstrap resampling = [3% 12%]) responded to the vocalizations (the response of an example AN fiber is shown in Fig 2E). We quantified the responsiveness of each fiber to the vocalizations using a measurement of the signal-to-noise ratio (SNR) of the response, defined as the ratio of the variance of the PSTH to the average variance of the deviation from the PSTH on each trial. To determine the extent to which each fiber’s responsiveness to vocalizations correlated with its sensitivity to high ultrasonic frequencies, we determined the highest frequency for which its responses to tones were significantly greater than its spontaneous activity (Fmax). For the population of fibers we studied, only the small fraction with the highest Fmax responded strongly to the vocalizations (Fig 2F).


An Overrepresentation of High Frequencies in the Mouse Inferior Colliculus Supports the Processing of Ultrasonic Vocalizations.

Garcia-Lazaro JA, Shepard KN, Miranda JA, Liu RC, Lesica NA - PLoS ONE (2015)

Auditory nerve responses to tones and vocalizations.(A) FRA of a representative auditory nerve fiber. FRAs were constructed from the responses elicited by tones of varying frequency (x-axis) and intensity (y-axis). (B) FRA of one AN fiber that was responsive to high frequency tones. The white arrow marks the location of a spectral notch created by the pinna. (C) Histogram of the distribution of CFs across the population of AN fibers. (D) Sound pressure waveforms (top panel) and spectrograms (lower panel) for the nine different CBA/Ca mouse vocalizations we tested. Note that all the vocalizations span a frequency range from 60–90 kHz. (E) PSTH of the response of the same fiber to a single mouse vocalization with a duration of 60 ms and averaged over 256 repeats. The spectrogram and sound pressure waveforms are shown at the top and bottom panels respectively. (F) Responsiveness to vocalizations. Each point indicates the SNR for one fiber as a function of the highest frequency for which its responses to tones were significantly greater than its spontaneous activity (Fmax). SNR values were averaged across the 9 different calls we tested.
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Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4526676&req=5

pone.0133251.g002: Auditory nerve responses to tones and vocalizations.(A) FRA of a representative auditory nerve fiber. FRAs were constructed from the responses elicited by tones of varying frequency (x-axis) and intensity (y-axis). (B) FRA of one AN fiber that was responsive to high frequency tones. The white arrow marks the location of a spectral notch created by the pinna. (C) Histogram of the distribution of CFs across the population of AN fibers. (D) Sound pressure waveforms (top panel) and spectrograms (lower panel) for the nine different CBA/Ca mouse vocalizations we tested. Note that all the vocalizations span a frequency range from 60–90 kHz. (E) PSTH of the response of the same fiber to a single mouse vocalization with a duration of 60 ms and averaged over 256 repeats. The spectrogram and sound pressure waveforms are shown at the top and bottom panels respectively. (F) Responsiveness to vocalizations. Each point indicates the SNR for one fiber as a function of the highest frequency for which its responses to tones were significantly greater than its spontaneous activity (Fmax). SNR values were averaged across the 9 different calls we tested.
Mentions: We began by recording responses from the auditory nerve. We used established physiological criteria to differentiate AN fibers from CN neurons (see Methods and S1 Fig). We isolated 94 fibers recorded from 23 animals. Fig 2A and 2B show FRAs for two representative fibers (the spectral notches created by the pinna are evident in Fig 2B). Across our sample population, the most commonly occurring CFs were between 20 and 30 kHz (Fig 2C). This is consistent with the distribution of CFs observed in a previous study of the mouse AN [13]. We also recorded the responses of AN fibers to conspecific vocalizations with frequencies between 60 and 90 kHz (the sound pressure waveforms and spectrograms are shown in Fig 2D). To determine whether a vocalization evoked a significant response, we compared the distribution of driven spike counts to the distribution of spontaneous spike counts (Wilcoxon rank-sum test, p < 0.05). Fibers were regarded as responsive if statistically significant responses were evoked by at least 3 of the 9 different vocalizations we tested. Only a small number of fibers (7 out of 94 ≈ 7%; 95% CI via bootstrap resampling = [3% 12%]) responded to the vocalizations (the response of an example AN fiber is shown in Fig 2E). We quantified the responsiveness of each fiber to the vocalizations using a measurement of the signal-to-noise ratio (SNR) of the response, defined as the ratio of the variance of the PSTH to the average variance of the deviation from the PSTH on each trial. To determine the extent to which each fiber’s responsiveness to vocalizations correlated with its sensitivity to high ultrasonic frequencies, we determined the highest frequency for which its responses to tones were significantly greater than its spontaneous activity (Fmax). For the population of fibers we studied, only the small fraction with the highest Fmax responded strongly to the vocalizations (Fig 2F).

Bottom Line: Auditory brainstem response measurements suggested stronger responses in the midbrain relative to the periphery for frequencies higher than 32 kHz.This result was confirmed by single- and multi-unit recordings showing that high ultrasonic frequency tones and vocalizations elicited responses from only a small fraction of cells in the periphery, while a much larger fraction of cells responded in the inferior colliculus.These results suggest that the processing of communication calls in mice is supported by a specialization of the auditory system for high frequencies that emerges at central stations of the auditory pathway.

View Article: PubMed Central - PubMed

Affiliation: Ear Institute, University College London, 332 Grays Inn Road, London, WC1X 8EE, United Kingdom.

ABSTRACT
Mice are of paramount importance in biomedical research and their vocalizations are a subject of interest for researchers across a wide range of health-related disciplines due to their increasingly important value as a phenotyping tool in models of neural, speech and language disorders. However, the mechanisms underlying the auditory processing of vocalizations in mice are not well understood. The mouse audiogram shows a peak in sensitivity at frequencies between 15-25 kHz, but weaker sensitivity for the higher ultrasonic frequencies at which they typically vocalize. To investigate the auditory processing of vocalizations in mice, we measured evoked potential, single-unit, and multi-unit responses to tones and vocalizations at three different stages along the auditory pathway: the auditory nerve and the cochlear nucleus in the periphery, and the inferior colliculus in the midbrain. Auditory brainstem response measurements suggested stronger responses in the midbrain relative to the periphery for frequencies higher than 32 kHz. This result was confirmed by single- and multi-unit recordings showing that high ultrasonic frequency tones and vocalizations elicited responses from only a small fraction of cells in the periphery, while a much larger fraction of cells responded in the inferior colliculus. These results suggest that the processing of communication calls in mice is supported by a specialization of the auditory system for high frequencies that emerges at central stations of the auditory pathway.

No MeSH data available.


Related in: MedlinePlus