Temporal vocal features suggest different call-pattern generating mechanisms in mice and bats

BMC Neuroscience

Anna M Stein¹  Ferdinand Salomon¹  Natalja Gavrilov¹  Steffen R Hage¹ 

[1] Animal Physiology, Institute of Neurobiology, University of Tübingen, Auf der Morgenstelle 28, Tübingen, 72076, Germany

关键词: Vocal pattern generation;    Mouse model;    Mice;    Mammal;    Bat;    Acoustic communication;   

Others  :  1140086
DOI  :  10.1186/1471-2202-14-99

 received in 2013-07-30, accepted in 2013-09-03,  发布年份 2013

【 摘 要 】

Background

Mice produce ultrasonic vocalizations in various inter-individual encounters and with high call rates. However, it is so far virtually unknown how these vocal patterns are generated. On the one hand, these vocal patterns could be embedded into the normal respiratory cycle, as happens in bats and other mammals that produce similar call rates and frequencies. On the other, mice could possess distinct vocal pattern generating systems that are capable of modulating the respiratory cycle, which is what happens in non-human and human primates. In the present study, we investigated the temporal call patterns of two different mammalian species, bats and mice, in order to differentiate between these two possibilities for mouse vocalizations. Our primary focus was on comparing the mechanisms for the production of rapid, successive ultrasound calls of comparable frequency ranges in the two species.

Results

We analyzed the temporal call pattern characteristics of mice, and we compared these characteristics to those of ultrasonic echolocation calls produced by horseshoe bats. We measured the distributions of call durations, call intervals, and inter-call intervals in the two species. In the bat, and consistent with previous studies, we found that call duration was independent of corresponding call intervals, and that it was negatively correlated with the corresponding inter-call interval. This indicates that echolocation call production mechanisms in the bat are highly correlated with the respiratory cycle. In contrast, call intervals in the mouse were directly correlated with call duration. Importantly, call duration was not, or was only slightly, correlated with inter-call intervals, consistent with the idea that vocal production in the mouse is largely independent of the respiratory cycle.

Conclusions

Our findings suggest that ultrasonic vocalizations in mice are produced by call-pattern generating mechanisms that seem to be similar to those that have been found in primates. This is in contrast to the production mechanisms of ultrasonic echolocation calls in horseshoe bats. These results are particularly interesting, especially since mouse vocalizations have recently attracted increased attention as potential indicators for the degree of progression of several disease patterns in mouse models for neurodegenerative and neurodevelopmental disorders of humans.

【 授权许可】

   
2013 Hage et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Jürgens U: The neural control of vocalization in mammals: a review. J Voice 2009, 23:1-10.
• [2]Hage SR: Neuronal networks involved in the generation of vocalization. In Handbook of mammalian vocalization. Edited by Brudzynski SM. Oxford: Academic Press; 2009:329-338.
• [3]Ludlow CL: Central nervous system control of interactions between vocalization and respiration in mammals. Head Neck 2011, 33:S21-S25.
• [4]Smotherman M, Schwartz C, Metzner W: Vocal-respiratory interactions in the parabrachial nucleus. In Handbook of mammalian vocalization. Edited by Brudzynski SM. Oxford: Academic Press; 2009:383-392.
• [5]Rübsamen R, Betz M: Control of echolocation pulses by neurons of the nucleus ambiguus in the rufous horseshoe bat, Rhinolophus rouxi I. Single unit recordings in the ventral motor nucleus of the laryngeal nerves in spontaneously vocalizing bats. J Comp Physiol A 1986, 159:675-687.
• [6]Lancaster WC, Henson OW Jr, Keating AW: Respiratory muscle activity in relation to vocalization in flying bats. J Exp Biol 1994, 198:175-191.
• [7]Smotherman M, Kobayasi K, Zhang S, Metzner W: A mechanism for vocal-respiratory coupling in the mammalian parabrachial nucleus. J Neurosci 2006, 26:4860-4869.
• [8]Schnitzler HU: The ultrasonic sounds of horseshoe bats (Chiroptera-Rhinolophidae) in different orientation situations. Z Vergl Physiol 1968, 57:376-408. German
• [9]Schnitzler HU, Kalko E, Miller L, Surlykke A: The echolocation and hunting behavior of the bat, Pipistrellus kuhli. J Comp Physiol A 1987, 161:267-274.
• [10]Roberts LH: Correlation of respiration and ultrasound production in rodents and bats. J Zool 1972, 168:439-449.
• [11]Häusler U: Vocalization-correlated respiratory movements in the squirrel monkey. J Acoust Soc Am 2000, 108:1443-1450.
• [12]Larson CR, Yajima Y, Ko P: Modification in activity of medullary respiratory-related neurons for vocalization and swallowing. J Neurophysiol 1994, 71:2294-2304.
• [13]Jürgens U, Hage SR: On the role of the reticular formation in vocal pattern generation. Behav Brain Res 2007, 182:308-314.
• [14]Fischer J, Hammerschmidt K: Ultrasonic vocalizations in mouse models for speech and socio-cognitive disorders: insights into the evolution of vocal communication. Genes Brain Behav 2011, 10:7-27.
• [15]Hammerschmidt K, Reisinger E, Westekemper K, Ehrenreich L, Strenzke N, Fischer J: Mice do not require auditory input for the normal development of their ultrasonic vocalizations. BMC Neurosci 2012, 13:40. BioMed Central Full Text
• [16]Musolf K, Hoffmann F, Penn DJ: Ultrasonic courtship vocalizations in wild house mice, Mus musculus musculus. Anim Behav 2010, 79:757-764.
• [17]Holy TE, Guo Z: Ultrasonic songs of male mice. PLoS Biol 2005, 3:e386.
• [18]Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa HH: Foraging behavior and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka. Behav Ecol Sociobiol 1987, 20:53-67.
• [19]Young DM, Schenk K, Yang SB, Jan YN, Jan LY: Altered ultrasonic vocalizations in a tuberous sclerosis mouse model of autism. Proc Nat Acad Sci USA 2010, 107:11074-11079.
• [20]Shu W, Cho JY, Jiang Y, Zhang M, Weisz D, Elder GA, et al.: Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc Nat Acad Sci USA 2005, 102:9643-9648.
• [21]Jamain S, Radyushkin K, Hammerschmidt K, Granon S, Boretius S, Varoqueaux F, et al.: Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Nat Acad Sci USA 2008, 105:1710-1715.
• [22]Scattoni ML, Crawley J, Ricceri L: Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav Rev 2009, 33:508-515.
• [23]Hage SR, Jürgens U: On the role of the pontine brainstem in vocal pattern generation. A telemetric single-unit recording study in the squirrel monkey. J Neurosci 2006, 26:7105-7115.
• [24]Ma J, Kobayasi K, Zhang S, Metzner W: Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum. J Comp Physiol A 2006, 192:535-550.
• [25]Scattoni ML, Gandhy SU, Ricceri L, Crawley JN: Unusual repertoire of vocalizations in the BTBR T plus tf/J mouse model of autism. PLoS One 2008, 3:e3067.
• [26]Ackermann H, Hage SR, Ziegler W: Brain mechanisms of acoustic communication in humans and nonhuman primates: an evolutionary perspective. Behav Brain Sciin press (Target article)
• [27]Hage SR, Jiang T, Berquist S, Feng J, Metzner W: Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats. Proc Nat Acad Sci USA 2013, 110:4063-4068.
• [28]Schuller G, Beuter K, Schnitzler HU: Response to frequency-shifted artificial echoes in the bat, Rhinolophus ferrumequinum. J Comp Physiol 1974, 89:275-286.