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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

Multi-unit responses in the inferior colliculus to tones and vocalizations.(A) Each panel shows FRAs for each of the 64 recording sites across a single electrode penetration in the IC. Two different penetrations are shown with the most rostral location in the IC at the top and the most caudal location at the bottom. The white vertical line denotes the separation between the ICC and EIC. The borders between the ICC and the DIC were not easily distinguishable in most of the electrode penetrations we performed. (B) FRAs estimated from multi-unit activity at three different recording sites across a single penetration along the dorsal-ventral axis in the IC. Each location is indicated by the corresponding white rectangles in Fig 4A (top panel). (C) Histograms showing the distribution of CFs across the sites we recorded from the IC for each of 5 animals. (D) PSTHs of the responses to the vocalization stimuli for the two electrode penetrations for which the FRAs were shown in (A). For each recording site, the x-axis (time) covers the range from 0 to 130 msec and the y-axis (SDs above spontaneous) covers the range from 0 to 16. (E) SNR for each recording site as a function of its Fmax. For each site, SNR values were averaged across the 9 different vocalizations tested. Colors correspond to those in C.
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pone.0133251.g004: Multi-unit responses in the inferior colliculus to tones and vocalizations.(A) Each panel shows FRAs for each of the 64 recording sites across a single electrode penetration in the IC. Two different penetrations are shown with the most rostral location in the IC at the top and the most caudal location at the bottom. The white vertical line denotes the separation between the ICC and EIC. The borders between the ICC and the DIC were not easily distinguishable in most of the electrode penetrations we performed. (B) FRAs estimated from multi-unit activity at three different recording sites across a single penetration along the dorsal-ventral axis in the IC. Each location is indicated by the corresponding white rectangles in Fig 4A (top panel). (C) Histograms showing the distribution of CFs across the sites we recorded from the IC for each of 5 animals. (D) PSTHs of the responses to the vocalization stimuli for the two electrode penetrations for which the FRAs were shown in (A). For each recording site, the x-axis (time) covers the range from 0 to 130 msec and the y-axis (SDs above spontaneous) covers the range from 0 to 16. (E) SNR for each recording site as a function of its Fmax. For each site, SNR values were averaged across the 9 different vocalizations tested. Colors correspond to those in C.

Mentions: Finally, we investigated the representation of high ultrasonic frequencies in the inferior colliculus of the midbrain. Like in the DCN, we performed multiple electrode penetrations in an attempt to sample the entire IC. The width of the probe (see Methods for further details) was sufficient to record responses from the different subnuclei, namely, the dorsal (DIC) and external (EIC) cortices, and the central nucleus (ICC). We distinguished the different subnuclei based on differences in the response properties between neighboring sites. For instance, the white vertical lines in Fig 4A separate the ICC from EIC, with the latter identified by its multi-modal FRAs (the border between the DIC and ICC was not clearly distinguishable in the penetrations shown in Fig 4A). We focused our analysis only on the ICC, which serves as the midbrain relay for the primary ascending auditory pathway. Unlike the AN and DCN, the most common CFs in the ICC were above 40 kHz. Fig 4C shows the distribution of CFs across all recording sites in the ICC for each of the five animals in our sample population. The CF distributions were not significantly different across animals (ANOVA, p > 0.7).


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)

Multi-unit responses in the inferior colliculus to tones and vocalizations.(A) Each panel shows FRAs for each of the 64 recording sites across a single electrode penetration in the IC. Two different penetrations are shown with the most rostral location in the IC at the top and the most caudal location at the bottom. The white vertical line denotes the separation between the ICC and EIC. The borders between the ICC and the DIC were not easily distinguishable in most of the electrode penetrations we performed. (B) FRAs estimated from multi-unit activity at three different recording sites across a single penetration along the dorsal-ventral axis in the IC. Each location is indicated by the corresponding white rectangles in Fig 4A (top panel). (C) Histograms showing the distribution of CFs across the sites we recorded from the IC for each of 5 animals. (D) PSTHs of the responses to the vocalization stimuli for the two electrode penetrations for which the FRAs were shown in (A). For each recording site, the x-axis (time) covers the range from 0 to 130 msec and the y-axis (SDs above spontaneous) covers the range from 0 to 16. (E) SNR for each recording site as a function of its Fmax. For each site, SNR values were averaged across the 9 different vocalizations tested. Colors correspond to those in C.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0133251.g004: Multi-unit responses in the inferior colliculus to tones and vocalizations.(A) Each panel shows FRAs for each of the 64 recording sites across a single electrode penetration in the IC. Two different penetrations are shown with the most rostral location in the IC at the top and the most caudal location at the bottom. The white vertical line denotes the separation between the ICC and EIC. The borders between the ICC and the DIC were not easily distinguishable in most of the electrode penetrations we performed. (B) FRAs estimated from multi-unit activity at three different recording sites across a single penetration along the dorsal-ventral axis in the IC. Each location is indicated by the corresponding white rectangles in Fig 4A (top panel). (C) Histograms showing the distribution of CFs across the sites we recorded from the IC for each of 5 animals. (D) PSTHs of the responses to the vocalization stimuli for the two electrode penetrations for which the FRAs were shown in (A). For each recording site, the x-axis (time) covers the range from 0 to 130 msec and the y-axis (SDs above spontaneous) covers the range from 0 to 16. (E) SNR for each recording site as a function of its Fmax. For each site, SNR values were averaged across the 9 different vocalizations tested. Colors correspond to those in C.
Mentions: Finally, we investigated the representation of high ultrasonic frequencies in the inferior colliculus of the midbrain. Like in the DCN, we performed multiple electrode penetrations in an attempt to sample the entire IC. The width of the probe (see Methods for further details) was sufficient to record responses from the different subnuclei, namely, the dorsal (DIC) and external (EIC) cortices, and the central nucleus (ICC). We distinguished the different subnuclei based on differences in the response properties between neighboring sites. For instance, the white vertical lines in Fig 4A separate the ICC from EIC, with the latter identified by its multi-modal FRAs (the border between the DIC and ICC was not clearly distinguishable in the penetrations shown in Fig 4A). We focused our analysis only on the ICC, which serves as the midbrain relay for the primary ascending auditory pathway. Unlike the AN and DCN, the most common CFs in the ICC were above 40 kHz. Fig 4C shows the distribution of CFs across all recording sites in the ICC for each of the five animals in our sample population. The CF distributions were not significantly different across animals (ANOVA, p > 0.7).

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