USVSEG: A robust method for segmentation of ultrasonic vocalizations in rodents

Rodents’ ultrasonic vocalizations (USVs) provide useful information for assessing their social behaviors. Despite previous efforts in classifying subcategories of time-frequency patterns of USV syllables to study their functional relevance, methods for detecting vocal elements from continuously recorded data have remained sub-optimal. Here, we propose a novel procedure for detecting USV segments in continuous sound data containing background noise recorded during the observation of social behavior. The proposed procedure utilizes a stable version of the sound spectrogram and additional signal processing for better separation of vocal signals by reducing the variation of the background noise. Our procedure also provides precise time tracking of spectral peaks within each syllable. We demonstrated that this procedure can be applied to a variety of USVs obtained from several rodent species. Performance tests showed this method had greater accuracy in detecting USV syllables than conventional detection methods.

[1]  Kazuo Okanoya,et al.  Cross Fostering Experiments Suggest That Mice Songs Are Innate , 2011, PloS one.

[2]  R. Froemke,et al.  Oxytocin Enables Maternal Behavior by Balancing Cortical Inhibition , 2015, Nature.

[3]  V. J. De Ghett,et al.  Developmental changes in the rate of ultrasonic vocalization in the mongolian gerbil. , 1974 .

[4]  R. Schwarting,et al.  Rat ultrasonic vocalization in aversively motivated situations and the role of individual differences in anxiety-related behavior , 2006, Behavioural Brain Research.

[5]  J. Nyby,et al.  Ultrasonic vocalizations during sex behavior of male house mice (Mus musculus): a description. , 1983, Behavioral and neural biology.

[6]  Kazuo Okanoya,et al.  Cognitive bias in rats evoked by ultrasonic vocalizations suggests emotional contagion , 2016, Behavioural Processes.

[7]  Jacqueline N. Crawley,et al.  Unusual Repertoire of Vocalizations in the BTBR T+tf/J Mouse Model of Autism , 2008, PloS one.

[8]  Peter Balazs,et al.  Automatic mouse ultrasound detector (A-MUD): A new tool for processing rodent vocalizations , 2017, PloS one.

[9]  Kenny Q. Ye,et al.  Structure and function of neonatal social communication in a genetic mouse model of autism , 2015, Molecular Psychiatry.

[10]  Elodie Ey,et al.  The Autism ProSAP1/Shank2 mouse model displays quantitative and structural abnormalities in ultrasonic vocalisations , 2013, Behavioural Brain Research.

[11]  G. Sales.  Strain Differences in the Ultrasonic Behavior of Rats (Rattus Norvegicus) , 1979 .

[12]  R. L. FRANCIS.  22-kHz calls by isolated rats , 1977, Nature.

[13]  E Alleva,et al.  Translating mouse vocalizations: prosody and frequency modulation 1 , 2011, Genes, brain, and behavior.

[14]  Kevin R Coffey,et al.  DeepSqueak: a deep learning-based system for detection and analysis of ultrasonic vocalizations , 2019, Neuropsychopharmacology.

[15]  G Whitney,et al.  Social status and ultrasonic vocalizations of male mice. , 1976, Behavioral biology.

[16]  J. Michael Bowers,et al.  Foxp2 Mediates Sex Differences in Ultrasonic Vocalization by Rat Pups and Directs Order of Maternal Retrieval , 2013, The Journal of Neuroscience.

[17]  K. Hammerschmidt,et al.  Ultrasonic vocalizations in mouse models for speech and socio-cognitive disorders: insights into the evolution of vocal communication , 2011, Genes, brain, and behavior.

[18]  K. Mogi,et al.  Sexual attractiveness of male chemicals and vocalizations in mice , 2014, Front. Neurosci..

[19]  B. Zimmerberg,et al.  Neonatal social isolation alters both maternal and pup behaviors in rats. , 2003, Developmental psychobiology.

[20]  Hiroshi Riquimaroux,et al.  Vocalization control in Mongolian gerbils (Meriones unguiculatus) during locomotion behavior. , 2011, The Journal of the Acoustical Society of America.

[21]  Takefumi Kikusui,et al.  Effect of Sociosexual Experience and Aging on Number of Courtship Ultrasonic Vocalizations in Male Mice , 2018, Zoological Science.

[22]  Gillian Sales,et al.  Ultrasound and mating behaviour in rodents with some observations on other behavioural situations , 2009 .

[23]  Duncan C. Blanchard,et al.  Risk assessment in animal models of anxiety , 1991 .

[24]  P. Clarke,et al.  Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context , 2010, Psychopharmacology.

[25]  Donald B. Percival,et al.  Spectral Analysis for Physical Applications , 1993 .

[26]  Marilyn Y McGinnis,et al.  Characterization of 50-kHz ultrasonic vocalizations in male and female rats , 2003, Physiology & Behavior.

[27]  G. Sales,et al.  Ultrasonic calls of wild and wild-type rodents , 2010 .

[28]  Francis Rl,et al.  22-kHz calls by isolated rats , 1977 .

[29]  Daniel H. Geschwind,et al.  VoICE: A semi-automated pipeline for standardizing vocal analysis across models , 2015, Scientific Reports.

[30]  Naoya Oosugi,et al.  Semi-Automatic Classification of Birdsong Elements Using a Linear Support Vector Machine , 2014, PloS one.

[31]  Edwin W Rubel,et al.  Engineered Deafness Reveals That Mouse Courtship Vocalizations Do Not Require Auditory Experience , 2013, The Journal of Neuroscience.

[32]  Takefumi Kikusui,et al.  Importance of mother-infant communication for social bond formation in mammals. , 2012, Animal science journal = Nihon chikusan Gakkaiho.

[33]  M. Brecht,et al.  Neural correlates of ticklishness in the rat somatosensory cortex , 2016, Science.

[34]  D. Thomson,et al.  Spectrum estimation and harmonic analysis , 1982, Proceedings of the IEEE.

[35]  C. A. Marsden,et al.  Pharmacological manipulation of ultrasound induced defence behaviour in the rat , 2008, Psychopharmacology.

[36]  Takefumi Kikusui,et al.  Mutual mother-infant recognition in mice: The role of pup ultrasonic vocalizations , 2017, Behavioural Brain Research.

[37]  C. A. Marsden,et al.  Central C-Fos Expression Following 20kHz/Ultrasound Induced Defence Behaviour in the Rat , 1997, Brain Research Bulletin.

[38]  David J Perkel,et al.  The role of ultrasonic vocalizations in mouse communication , 2014, Current Opinion in Neurobiology.

[39]  T. Holy,et al.  Ultrasonic Songs of Male Mice , 2005, PLoS biology.

[40]  Hiroshi Riquimaroux,et al.  Phonotactic responses to vocalization in adult Mongolian gerbils (Meriones unguiculatus) , 2013, Journal of Ethology.

[41]  Shrikanth Narayanan,et al.  MUPET—Mouse Ultrasonic Profile ExTraction: A Signal Processing Tool for Rapid and Unsupervised Analysis of Ultrasonic Vocalizations , 2017, Neuron.

[42]  Hiroshi Riquimaroux,et al.  Audiovisual integration in the primary auditory cortex of an awake rodent , 2013, Neuroscience Letters.

[43]  V J De Ghett,et al.  Developmental changes in the rate of ultrasonic vocalization in the mongolian gerbil. , 1974, Developmental psychobiology.

[44]  S. Brudzyński,et al.  Ethotransmission: communication of emotional states through ultrasonic vocalization in rats , 2013, Current Opinion in Neurobiology.

[45]  Jeffrey R Alberts,et al.  Stimulus control of maternal responsiveness to Norway rat (Rattus norvegicus) pup ultrasonic vocalizations. , 2002, Journal of comparative psychology.

[46]  Takefumi Kikusui,et al.  Pup odor and ultrasonic vocalizations synergistically stimulate maternal attention in mice. , 2013, Behavioral neuroscience.

[47]  David B. Dunson,et al.  A Foxp2 Mutation Implicated in Human Speech Deficits Alters Sequencing of Ultrasonic Vocalizations in Adult Male Mice , 2016, Front. Behav. Neurosci..

[48]  Jaak Panksepp,et al.  Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self-administration of playback. , 2008, Journal of comparative psychology.

[49]  S. Brudzyński,et al.  Handbook of mammalian vocalization : an integrative neuroscience approach , 2010 .

[50]  A. J. Pretlove,et al.  Developmental changes in several parameters of ultrasonic calling by young Mongolian gerbils (Meriones unguiculatus) , 2009 .

[51]  Genevieve Konopka,et al.  Animal Models of Speech and Vocal Communication Deficits Associated With Psychiatric Disorders , 2016, Biological Psychiatry.

[52]  D. A. Thomas,et al.  Male-produced postejaculatory 22-kHz vocalizations and the mating behavior of estrous female rats. , 1982, Behavioral and neural biology.

[53]  David B. Dunson,et al.  Male mice song syntax depends on social contexts and influences female preferences , 2015, Front. Behav. Neurosci..

[54]  Tobias Riede,et al.  Laryngeal airway reconstruction indicates that rodent ultrasonic vocalizations are produced by an edge-tone mechanism , 2017, Royal Society Open Science.

[55]  Markus Wöhr,et al.  Ultrasonic Communication in Rats: Can Playback of 50-kHz Calls Induce Approach Behavior? , 2007, PloS one.

[56]  Takefumi Kikusui,et al.  A Role for Strain Differences in Waveforms of Ultrasonic Vocalizations during Male–Female Interaction , 2011, PloS one.

[57]  R. Elwood,et al.  Paternal and maternal behaviour in the Mongolian gerbil , 1975, Animal Behaviour.

[58]  Rudolf Rübsamen,et al.  Vocal behavior of the Mongolian gerbil in a seminatural enclosure , 2012 .

[59]  Stefan M. Brudzynski,et al.  Pharmacology of Ultrasonic Vocalizations in adult Rats: Significance, Call Classification and Neural Substrate , 2015, Current neuropharmacology.

[60]  Kazuo Okanoya,et al.  Mice modulate ultrasonic calling bouts according to sociosexual context , 2018, Royal Society Open Science.

[61]  J. Fleiss.  Measuring nominal scale agreement among many raters. , 1971 .

[62]  Kelly M Seagraves,et al.  The contribution of ultrasonic vocalizations to mouse courtship , 2016, Current Opinion in Neurobiology.

[63]  Jacob Cohen.  A Coefficient of Agreement for Nominal Scales , 1960 .

[64]  Kazuo Okanoya,et al.  Phase-Specific Vocalizations of Male Mice at the Initial Encounter during the Courtship Sequence , 2016, PloS one.

[65]  Hiroshi Riquimaroux,et al.  Classification of vocalizations in the Mongolian gerbil, Meriones unguiculatus. , 2012, The Journal of the Acoustical Society of America.

[66]  J. Zagrodzka,et al.  22-kHz Ultrasonic vocalization in rats as an index of anxiety but not fear: behavioral and pharmacological modulation of affective state , 2003, Behavioural Brain Research.