{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T10:54:06Z","timestamp":1791370446794,"version":"4.3.1"},"reference-count":175,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2024,10,31]],"date-time":"2024-10-31T00:00:00Z","timestamp":1730332800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Institute on Deafness and Communication Disorders","award":["T32DC009401"],"award-info":[{"award-number":["T32DC009401"]}]},{"name":"National Institute on Deafness and Communication Disorders","award":["R01DC018584"],"award-info":[{"award-number":["R01DC018584"]}]},{"name":"National Institute on Deafness and Communication Disorders","award":["1F32DC021367"],"award-info":[{"award-number":["1F32DC021367"]}]},{"name":"National Institute on Deafness and Communication Disorders","award":["R01NS117469"],"award-info":[{"award-number":["R01NS117469"]}]},{"name":"National Institute of Neurological Disorders and Stroke","award":["T32DC009401"],"award-info":[{"award-number":["T32DC009401"]}]},{"name":"National Institute of Neurological Disorders and Stroke","award":["R01DC018584"],"award-info":[{"award-number":["R01DC018584"]}]},{"name":"National Institute of Neurological Disorders and Stroke","award":["1F32DC021367"],"award-info":[{"award-number":["1F32DC021367"]}]},{"name":"National Institute of Neurological Disorders and Stroke","award":["R01NS117469"],"award-info":[{"award-number":["R01NS117469"]}]},{"name":"ASH Foundation New Investigator","award":["T32DC009401"],"award-info":[{"award-number":["T32DC009401"]}]},{"name":"ASH Foundation New Investigator","award":["R01DC018584"],"award-info":[{"award-number":["R01DC018584"]}]},{"name":"ASH Foundation New Investigator","award":["1F32DC021367"],"award-info":[{"award-number":["1F32DC021367"]}]},{"name":"ASH Foundation New Investigator","award":["R01NS117469"],"award-info":[{"award-number":["R01NS117469"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Brain Sciences"],"abstract":"<jats:p>Introduction: Ultrasonic vocalization (USV) can indicate affective states\u2014including psychosocial stress\u2014in mice and rats. However, stress-induced USV changes could be confounded by laboratory experimental variables such as the type of behavioral stress paradigm, the elicitation method, rodent strain, etc. We sought to provide a review of the current literature to delineate how psychosocial stress-altered rodent USVs may be affected by factors of age, sex, strain, species, elicitation paradigm, and stressor. Methods: We used PubMed, Scopus (Elsevier), PsycINFO (EBSCO), and the following Web of Science (Clarivate) databases: Biological Abstracts, CAB Abstracts, Science Citation Index-Expanded, and Emerging Sources Citation Index. The studies identified by our search strategy were independently screened by two authors with the following inclusion criteria: peer-reviewed, in English, reported original data, and described USV in response to stress in rats or mice. The data extracted included USV acoustic parameters (mean peak frequency and mean amplitude (loudness)), details of the stress and USV elicitation paradigms, rodent species, age, and sex variables. Results: The following screening of 5309 titles\/abstracts and 687 full-text articles revealed 148 articles. Footshock (20%), cold exposure (14%), and maternal separation (23.5%) were the most commonly used stress paradigms (duration and type of stressor varied across studies), with the total number of USV calls being the most commonly reported acoustic outcome. In rats, 121 articles described stress-altered USVs, while 25 studies reported the same in mice, and two reported multiple rodent species (rats and mice, alongside other rodent species such as gerbils). With respect to stress-altered USV changes with age, mice and rats increase USV rates after birth, with a peak around 6 to 10 days, and decrease USVs until weanling age. Of the five studies that reported sex-related differences in stress-induced USVs, females had an increased number of calls and lower average peak frequency in response to stress when compared to males. Only two to four studies reported strain-related differences in stress-induced vocalizations in rats and mice, respectively. Conclusions: The data from this review lay the groundwork for better understanding rodent USVs in response to psychosocial stress with effects of elicitation paradigm, stressor, age, and sex.<\/jats:p>","DOI":"10.3390\/brainsci14111109","type":"journal-article","created":{"date-parts":[[2024,10,31]],"date-time":"2024-10-31T06:55:37Z","timestamp":1730357737000},"page":"1109","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Stress-Induced Ultrasonic Vocalization in Laboratory Rats and Mice: A Scoping Review"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4341-9701","authenticated-orcid":false,"given":"Anumitha","family":"Venkatraman","sequence":"first","affiliation":[{"name":"Division of Otolaryngology\u2014Head & Neck Surgery, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53705, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle","family":"Bretl","sequence":"additional","affiliation":[{"name":"Division of Otolaryngology\u2014Head & Neck Surgery, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53705, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Se-in","family":"Kim","sequence":"additional","affiliation":[{"name":"Division of Otolaryngology\u2014Head & Neck Surgery, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53705, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4040-5593","authenticated-orcid":false,"given":"Leslie","family":"Christensen","sequence":"additional","affiliation":[{"name":"Ebling Library for the Health Sciences, University of Wisconsin-Madison, Madison, WI 53705, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6670-2177","authenticated-orcid":false,"given":"Cynthia A.","family":"Kelm-Nelson","sequence":"additional","affiliation":[{"name":"Division of Otolaryngology\u2014Head & Neck Surgery, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53705, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle R.","family":"Ciucci","sequence":"additional","affiliation":[{"name":"Division of Otolaryngology\u2014Head & Neck Surgery, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53705, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9046-4356","authenticated-orcid":false,"given":"Susan L.","family":"Thibeault","sequence":"additional","affiliation":[{"name":"Division of Otolaryngology\u2014Head & Neck Surgery, Department of Surgery, University of Wisconsin-Madison, Madison, WI 53705, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,10,31]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1590\/S0100-879X2012007500038","article-title":"On the relationships between ultrasonic calling and anxiety-related behavior in rats","volume":"45","author":"Schwarting","year":"2012","journal-title":"Braz. J. Med. Biol. Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"808","DOI":"10.1126\/science.119.3101.808","article-title":"The Production of Ultrasonic Sounds by Laboratory Rats and Other Mammals","volume":"119","author":"Anderson","year":"1954","journal-title":"Science"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"164","DOI":"10.2174\/1570159X13999150318113800","article-title":"Rat Ultrasonic Vocalizations and Behavioral Neuropharmacology: From the Screening of Drugs to the Study of Disease","volume":"13","author":"Simola","year":"2015","journal-title":"Curr. Neuropharmacol."},{"key":"ref_4","first-page":"28","article-title":"Types and functions of ultrasonic vocalizations in laboratory rats and mice","volume":"46","author":"Portfors","year":"2007","journal-title":"J. Am. Assoc. Lab. Anim. Sci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1007\/s10071-019-01338-2","article-title":"Social context increases ultrasonic vocalizations during restraint in adult mice","volume":"23","author":"Lefebvre","year":"2020","journal-title":"Anim. Cogn."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1007\/BF02245339","article-title":"Behavioral and autonomic responses to intermittent social stress: Differential protection by clonidine and metoprolol","volume":"116","author":"Tornatzky","year":"1994","journal-title":"Psychopharmacology"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"4136","DOI":"10.1007\/s11434-010-4223-z","article-title":"Effects of isolation after sexual experience on anxiety-like, depressive-like behaviors and affective states in male rats","volume":"55","author":"Wen","year":"2010","journal-title":"Chin. Sci. Bull."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/j.physbeh.2009.07.013","article-title":"The effects of buspirone and diazepam on aversive context- and social isolation-induced ultrasonic vocalisation","volume":"98","author":"Hamed","year":"2009","journal-title":"Physiol. Behav."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"507","DOI":"10.3109\/10253890802673134","article-title":"Strain differences in coping behaviour, novelty seeking behaviour, and susceptibility to socially conditioned fear: A comparison between Wistar and Sprague Dawley rats","volume":"12","author":"Walker","year":"2009","journal-title":"Stress"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.bbr.2006.11.038","article-title":"Rat 22kHz ultrasonic vocalizations as alarm cries","volume":"182","author":"Litvin","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Boeluekbas, I., Mundorf, A., and Freund, N. (2020). Maternal separation in rats induces neurobiological and behavioral changes on the maternal side. Sci. Rep., 10.","DOI":"10.1038\/s41598-020-80087-6"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1002\/dev.21258","article-title":"Effects of maternal deprivation and the duration of reunion time on rat pup ultrasonic vocalization responses to isolation: Possible implications for human infant studies: Effects of Maternal Reunion Time on USV Responses to Isolation","volume":"57","author":"Shair","year":"2015","journal-title":"Dev. Psychobiol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Yin, X., Chen, L., Xia, Y., Cheng, Q., Yuan, J., Yang, Y., Wang, Z., Wang, H., Dong, J., and Ding, Y. (2016). Maternal Deprivation Influences Pup Ultrasonic Vocalizations of C57BL\/6J Mice. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0160409"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"H\u00e5kansson, J., Jiang, W., Xue, Q., Zheng, X., Ding, M., Agarwal, A.A., and Elemans, C.P.H. (2022). Aerodynamics and motor control of ultrasonic vocalizations for social communication in mice and rats. BMC Biol., 20.","DOI":"10.1186\/s12915-021-01185-z"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2580","DOI":"10.1152\/jn.00478.2011","article-title":"Subglottal pressure, tracheal airflow, and intrinsic laryngeal muscle activity during rat ultrasound vocalization","volume":"106","author":"Riede","year":"2011","journal-title":"J. Neurophysiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1002\/jez.1785","article-title":"Stereotypic laryngeal and respiratory motor patterns generate different call types in rat ultrasound vocalization","volume":"319","author":"Riede","year":"2013","journal-title":"J. Exp. Zool. A Ecol. Genet. Physiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.bbr.2019.01.033","article-title":"Emission of 22 kHz vocalizations in rats as an evolutionary equivalent of human crying: Relationship to depression","volume":"363","author":"Brudzynski","year":"2019","journal-title":"Behav. Brain Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00213-010-1859-y","article-title":"Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: Effects of amphetamine and social context","volume":"211","author":"Wright","year":"2010","journal-title":"Psychopharmacology"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Seki, Y. (2023). Acoustic Properties and Biological Significance of Ultrasonic Vocalizations in Rodents: Emotional Expressions. Acoustic Communication in Animals, Springer Nature.","DOI":"10.1007\/978-981-99-0831-8"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.brainres.2017.12.002","article-title":"Characterization of early-onset motor deficits in the Pink1\u2212\/\u2212 mouse model of Parkinson disease","volume":"1680","author":"Brauer","year":"2018","journal-title":"Brain Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1093\/ilar.50.1.43","article-title":"Communication of Adult Rats by Ultrasonic Vocalization: Biological, Sociobiological, and Neuroscience Approaches","volume":"50","author":"Brudzynski","year":"2009","journal-title":"ILAR J."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"8713","DOI":"10.1523\/JNEUROSCI.23-25-08713.2003","article-title":"Central Amygdala Lesions Block Ultrasonic Vocalization and Freezing as Conditional But Not Unconditional Responses","volume":"23","author":"Choi","year":"2003","journal-title":"J. Neurosci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1016\/B978-0-12-809600-0.00039-1","article-title":"Ultrasonic Vocalizations in Rats as a Measure of Emotional Responses to Stress: Models of Anxiety and Depression","volume":"Volume 25","author":"Moskal","year":"2018","journal-title":"Handbook of Behavioral Neuroscience"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/B978-0-12-809600-0.00029-9","article-title":"Effects of Selective Serotonin Reuptake Inhibitors on the Shock-Induced Ultrasonic Vocalization of Rats in Different Experimental Designs","volume":"Volume 25","author":"Kassai","year":"2018","journal-title":"Handbook of Behavioral Neuroscience"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"113514","DOI":"10.1016\/j.bbr.2021.113514","article-title":"Quantification of brainstem norepinephrine relative to vocal impairment and anxiety in the Pink1\u2212\/\u2212 rat model of Parkinson disease","volume":"414","author":"Hoffmeister","year":"2021","journal-title":"Behav. Brain Res."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Krasko, M.N., Hoffmeister, J.D., Schaen-Heacock, N.E., Welsch, J.M., Kelm-Nelson, C.A., and Ciucci, M.R. (2021). Rat Models of Vocal Deficits in Parkinson\u2019s Disease. Brain Sci., 11.","DOI":"10.3390\/brainsci11070925"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1002\/(SICI)1098-2302(199811)33:3<249::AID-DEV5>3.0.CO;2-R","article-title":"Ultrasonic vocalizations by infant laboratory mice: A preliminary spectrographic characterization under different conditions","volume":"33","author":"Branchi","year":"1998","journal-title":"Dev. Psychobiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.neubiorev.2016.03.029","article-title":"Determinants of the mouse ultrasonic vocal structure and repertoire","volume":"65","author":"Heckman","year":"2016","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"E270","DOI":"10.1002\/lary.26561","article-title":"Sexual dimorphism in laryngeal muscle fibers and ultrasonic vocalizations in the adult rat: Sexual Dimorphism of the Adult Rat Larynx","volume":"127","author":"Lenell","year":"2017","journal-title":"Laryngoscope"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Takahashi, N., Kashino, M., and Hironaka, N. (2010). Structure of Rat Ultrasonic Vocalizations and Its Relevance to Behavior. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0014115"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.beproc.2004.09.001","article-title":"Use of ultrasonic vocalizations to assess olfactory detection in mouse pups treated with 3-methylindole","volume":"68","author":"Lemasson","year":"2005","journal-title":"Behav. Process."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"457","DOI":"10.3758\/BF03209701","article-title":"Classical conditioning of vocalizations in the rat: Acoustic characteristics of the CR and UCR","volume":"7","author":"Nitschke","year":"1979","journal-title":"Anim. Learn. Behav."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1002\/dev.420040206","article-title":"Effects of temperature on ultrasound production by infant albino rats","volume":"4","author":"Allin","year":"1971","journal-title":"Dev. Psychobiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2131","DOI":"10.1038\/npp.2013.110","article-title":"Abnormal Stress Responsivity in a Rodent Developmental Disruption Model of Schizophrenia","volume":"38","author":"Zimmerman","year":"2013","journal-title":"Neuropsychopharmacology"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1248\/bpb.b21-00776","article-title":"Cold-Restraint Stress-Induced Ultrasonic Vocalization as a Novel Tool to Measure Anxiety in Mice","volume":"45","author":"Yamauchi","year":"2022","journal-title":"Biol. Pharm. Bull."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"W\u00f6hr, M. (2015). Effect of social odor context on the emission of isolation-induced ultrasonic vocalizations in the BTBR T+tf\/J mouse model for autism. Front. Neurosci., 9.","DOI":"10.3389\/fnins.2015.00073"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1016\/j.bbr.2004.07.001","article-title":"Sex-selective effects of neonatal isolation on fear conditioning and foot shock sensitivity","volume":"157","author":"Kosten","year":"2005","journal-title":"Behav. Brain Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1538\/expanim.51.187","article-title":"A Comparative Study of Isolation-Induced Ultrasonic Vocalization in Rodent Pups","volume":"51","author":"Motomura","year":"2002","journal-title":"Exp. Anim."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"467","DOI":"10.7326\/M18-0850","article-title":"PRISMA Extension for Scoping Reviews (PRISMA-ScR): Checklist and Explanation","volume":"169","author":"Tricco","year":"2018","journal-title":"Ann. Intern. Med."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"240","DOI":"10.3163\/1536-5050.104.3.014","article-title":"De-duplication of database search results for systematic reviews in EndNote","volume":"104","author":"Bramer","year":"2016","journal-title":"J. Med. Libr. Assoc."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"212","DOI":"10.1002\/dev.21906","article-title":"Social experience during adolescence in female rats increases 50 kHz ultrasonic vocalizations in adulthood, without affecting anxiety-like behavior","volume":"62","author":"Emmerson","year":"2020","journal-title":"Dev. Psychobiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.bbr.2007.03.032","article-title":"Short-term and long-term effects of postnatal exposure to an adult male in C57BL\/6J mice","volume":"182","author":"Hefner","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/j.bbr.2012.03.031","article-title":"Rats learn to freeze to 22-kHz ultrasonic vocalizations through autoconditioning","volume":"232","author":"Parsana","year":"2012","journal-title":"Behav. Brain Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.brainres.2005.10.002","article-title":"Single exposure to social defeat increases corticotropin-releasing factor and glucocorticoid receptor mRNA expression in rat hippocampus","volume":"1067","author":"Marini","year":"2006","journal-title":"Brain Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"963","DOI":"10.1016\/j.neuroscience.2009.08.041","article-title":"Effect of Chronic Stress on Behavior and Cerebral Oxidative Metabolism in Rats with High or Low Positive Affect","volume":"164","author":"Maello","year":"2009","journal-title":"Neuroscience"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.pbb.2005.01.020","article-title":"Behavioral, biochemical and histological studies in a model of pilocarpine-induced spontaneous recurrent seizures","volume":"81","author":"Szyndler","year":"2005","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.bbr.2009.03.021","article-title":"Swim stress-induced ultrasonic vocalizations forecast resilience in rats","volume":"202","author":"Drugan","year":"2009","journal-title":"Behav. Brain Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/0031-9384(94)90050-7","article-title":"Stimulus control of behavioral inhibition in the preweanling rat","volume":"55","author":"Takahashi","year":"1994","journal-title":"Physiol. Behav."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/0031-9384(92)90336-Z","article-title":"Ontogeny of behavioral inhibition induced by unfamiliar adult male conspecifics in preweanling rats","volume":"52","author":"Takahashi","year":"1992","journal-title":"Physiol. Behav."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1002\/dev.420240504","article-title":"Development of stress-induced responses in preweanling rats","volume":"24","author":"Takahashi","year":"1991","journal-title":"Dev. Psychobiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1007\/s12038-015-9534-4","article-title":"Strain- and context-based 50 kHz ultrasonic vocalizations and anxiety behaviour in the Wistar-Kyoto rat","volume":"40","author":"Rao","year":"2015","journal-title":"J. Biosci."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"ENEURO.0280-19.2019","DOI":"10.1523\/ENEURO.0280-19.2019","article-title":"Ultrasonic Vocalizations Emitted during Defensive Behavior Alter the Influence of the Respiratory Rhythm on Brain Oscillatory Dynamics in the Fear Circuit of Rats","volume":"6","author":"Carney","year":"2019","journal-title":"eNeuro"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Kaidbey, J.H., Ranger, M., Myers, M.M., Anwar, M., Ludwig, R.J., Schulz, A.M., Barone, J.L., Kolacz, J., and Welch, M.G. (2019). Early Life Maternal Separation and Maternal Behaviour Modulate Acoustic Characteristics of Rat Pup Ultrasonic Vocalizations. Sci. Rep., 9.","DOI":"10.1038\/s41598-019-54800-z"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/0091-3057(89)90233-5","article-title":"Central administration of corticotropin releasing factor alters rat pup isolation calls","volume":"32","author":"Insel","year":"1989","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1002\/dev.10022","article-title":"Developmental differences in temporal patterns and potentiation of isolation-induced ultrasonic vocalizations: Influence of temperature variables","volume":"40","author":"Kraebel","year":"2002","journal-title":"Dev. Psychobiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1038\/s41390-021-01374-0","article-title":"Lactobacillus reuteri effects on maternal separation stress in newborn mice","volume":"90","author":"Park","year":"2021","journal-title":"Pediatr. Res."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Granata, L., Valentine, A., Hirsch, J.L., Honeycutt, J., and Brenhouse, H. (2021). Trajectories of Mother-Infant Communication: An Experiential Measure of the Impacts of Early Life Adversity. Front. Hum. Neurosci., 15.","DOI":"10.3389\/fnhum.2021.632702"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1384","DOI":"10.1037\/0735-7044.119.5.1384","article-title":"Maternally modulated infant separation responses are regulated by D2-family dopamine receptors","volume":"119","author":"Muller","year":"2005","journal-title":"Behav. Neurosci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1983","DOI":"10.1126\/science.1095943","article-title":"Deficit in Attachment Behavior in Mice Lacking the \u00b5-Opioid Receptor Gene","volume":"304","author":"Moles","year":"2004","journal-title":"Science"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1097\/00008877-200509000-00016","article-title":"Differential response to acute and repeated stress in cannabinoid CB1 receptor knockout newborn and adult mice","volume":"16","author":"Fride","year":"2005","journal-title":"Behav. Pharmacol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1002\/dev.21264","article-title":"Effects of neonatal fluoxetine exposure on behavior across development in rats selectively bred for an infantile affective trait: Effects of Neonatal Fluoxetine Exposure","volume":"57","author":"Zimmerberg","year":"2015","journal-title":"Dev. Psychobiol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1037\/0735-7044.116.4.612","article-title":"Effects of selective breeding for infant rat ultrasonic vocalization on cardiac responses to isolation","volume":"116","author":"Brunelli","year":"2002","journal-title":"Behav. Neurosci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1196\/annals.1301.039","article-title":"Early Deprivation Alters the Vocalization Behavior of Neonates Directing Maternal Attention in a Rat Model of Child Neglect","volume":"1008","author":"Zimmerberg","year":"2003","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.brainres.2008.07.079","article-title":"Corticotropin-releasing factor modulates maternal separation-induced ultrasonic vocalization in rat pups via activation of CRF1 receptor","volume":"1234","author":"Ise","year":"2008","journal-title":"Brain Res."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1007\/s002130000556","article-title":"Periodic postpartum separation from the offspring results in long-lasting changes in anxiety-related behaviors and sensitivity to morphine in Long-Evans mother rats","volume":"152","author":"Kalinichev","year":"2000","journal-title":"Psychopharmacology"},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Wilson, K.M., Wagner, V.A., and Saltzman, W. (2022). Specificity of California mouse pup vocalizations in response to olfactory stimuli. Dev. Psychobiol., 64.","DOI":"10.1002\/dev.22261"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/B978-0-12-809600-0.00032-9","article-title":"Sex Differences in Ultrasonic Vocal Expression of Negative Emotional States in Rats","volume":"Volume 25","author":"Inagaki","year":"2018","journal-title":"Handbook of Behavioral Neuroscience"},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Waddell, J., Yang, T., Ho, E., Wellmann, K., and Mooney, S. (2016). Prenatal Ethanol Exposure and Whisker Clipping Disrupt Ultrasonic Vocalizations and Play Behavior in Adolescent Rats. Brain Sci., 6.","DOI":"10.3390\/brainsci6040043"},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Petroni, V., Subashi, E., Premoli, M., W\u00f6hr, M., Crusio, W.E., Lemaire, V., and Pietropaolo, S. (2022). Autistic-like behavioral effects of prenatal stress in juvenile Fmr1 mice: The relevance of sex differences and gene-environment interactions. Sci. Rep., 12.","DOI":"10.1038\/s41598-022-11083-1"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/j.bbr.2012.06.028","article-title":"High-frequency ultrasonic vocalizations in rats in response to tickling: The effects of restraint stress","volume":"234","author":"Popik","year":"2012","journal-title":"Behav. Brain Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.bbr.2013.11.029","article-title":"Inhibition of the glucocorticoid synthesis reverses stress-induced decrease in rat\u2019s 50-kHz ultrasonic vocalizations","volume":"260","author":"Popik","year":"2014","journal-title":"Behav. Brain Res."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Weiner, B., Hertz, S., Perets, N., and London, M. (2016). Social Ultrasonic Vocalization in Awake Head-Restrained Mouse. Front. Behav. Neurosci., 10.","DOI":"10.3389\/fnbeh.2016.00236"},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Fendt, M., Brosch, M., Wernecke, K.E.A., Willadsen, M., and W\u00f6hr, M. (2018). Predator odour but not TMT induces 22-kHz ultrasonic vocalizations in rats that lead to defensive behaviours in conspecifics upon replay. Sci. Rep., 8.","DOI":"10.1038\/s41598-018-28927-4"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1016\/S0149-7634(05)80069-7","article-title":"The characterization and modelling of antipredator defensive behavior","volume":"14","author":"Blanchard","year":"1990","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"967","DOI":"10.1016\/0031-9384(91)90423-L","article-title":"Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems","volume":"50","author":"Blanchard","year":"1991","journal-title":"Physiol. Behav."},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Shionoya, K., Hegoburu, C., Brown, B.L., Sullivan, R.M., Doy\u00e8re, V., and Mouly, A.M. (2013). It\u2019s time to fear! Interval timing in odor fear conditioning in rats. Front. Behav. Neurosci., 7.","DOI":"10.3389\/fnbeh.2013.00128"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.pbb.2016.08.008","article-title":"Predator odor exposure of rat pups has opposite effects on play by juvenile males and females","volume":"152","author":"Stockman","year":"2017","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"955","DOI":"10.3906\/sag-1309-24","article-title":"Behavioural and neurobiological consequences of 2 different chronic stressors in rats","volume":"44","author":"Kaya","year":"2014","journal-title":"Turk. J. Med. Sci."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"533","DOI":"10.3109\/10253890.2011.646348","article-title":"Juvenile stress potentiates aversive 22-kHz ultrasonic vocalizations and freezing during auditory fear conditioning in adult male rats","volume":"15","author":"Yee","year":"2012","journal-title":"Stress"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"3073","DOI":"10.1007\/s00221-015-4375-9","article-title":"Chronic deep brain stimulation of the medial forebrain bundle reverses depressive-like behavior in a hemiparkinsonian rodent model","volume":"233","author":"Furlanetti","year":"2015","journal-title":"Exp. Brain Res."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1002\/dev.420250705","article-title":"Ultrasonic vocalization by rat pups during recovery from deep hypothermia","volume":"25","author":"Hofer","year":"1992","journal-title":"Dev. Psychobiol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1037\/0735-7044.105.1.41","article-title":"Independence of ultrasonic vocalization and thermogenic responses in infant rats","volume":"105","author":"Hofer","year":"1991","journal-title":"Behav. Neurosci."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1002\/dev.420050409","article-title":"Distress vocalizations of young in three inbred strains of mice","volume":"5","author":"Nitschke","year":"1972","journal-title":"Dev. Psychobiol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1002\/dev.420070307","article-title":"Early experience, ultrasonic vocalizations, and maternal responsiveness in rats","volume":"7","author":"Bell","year":"1974","journal-title":"Dev. Psychobiol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"808","DOI":"10.1037\/0735-7044.104.5.808","article-title":"Ultrasonic vocalizations by rat pups in the cold: An acoustic by-product of laryngeal braking?","volume":"104","author":"Blumberg","year":"1990","journal-title":"Behav. Neurosci."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1037\/0735-7044.113.6.1274","article-title":"Cardiovascular concomitants in ultrasound production during cold exposure in infant rats","volume":"113","author":"Blumberg","year":"1999","journal-title":"Behav. Neurosci."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1023\/A:1019728813891","article-title":"The effects of cold, rotation, and genotype on the production of ultrasonic calls in infant mice","volume":"32","author":"Hahn","year":"2002","journal-title":"Behav. Genet."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/0165-3806(95)00064-K","article-title":"Corticotropin-releasing factor modulation of the ultrasonic vocalization rate of isolated rat pups","volume":"87","author":"Hennessy","year":"1995","journal-title":"Dev. Brain Res."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1538\/expanim.56.315","article-title":"Ontogenetic Changes of Ultrasonic Vocalizations Emitted from Infant Rats","volume":"56","author":"Hashimoto","year":"2007","journal-title":"Exp. Anim."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1364","DOI":"10.1037\/0735-7044.121.6.1364","article-title":"Brain regional neuropeptide changes resulting from social defeat","volume":"121","author":"Panksepp","year":"2007","journal-title":"Behav. Neurosci."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1016\/S0031-9384(99)00131-6","article-title":"Social Stress Effects on Territorial Marking and Ultrasonic Vocalizations in Mice","volume":"67","author":"Lumley","year":"1999","journal-title":"Physiol. Behav."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1523\/JNEUROSCI.21-01-00262.2001","article-title":"Enhanced Cortical Extracellular Levels of Cholecystokinin-Like Material in a Model of Anticipation of Social Defeat in the Rat","volume":"21","author":"Becker","year":"2001","journal-title":"J. Neurosci."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1158","DOI":"10.1016\/j.neuropharm.2004.02.006","article-title":"Melatonin MT1\/2 receptor stimulation reduces cortical overflow of cholecystokinin-like material in a model of anticipation of social defeat in the rat","volume":"46","author":"Becker","year":"2004","journal-title":"Neuropharmacology"},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/s002130051101","article-title":"Interactions between social stress and morphine in the periaqueductal gray: Effects on affective vocal and reflexive pain responses in rats","volume":"146","author":"Vivian","year":"1999","journal-title":"Psychopharmacology"},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"766","DOI":"10.1016\/j.physbeh.2007.11.031","article-title":"Effects of experience and context on 50-kHz vocalizations in rats","volume":"93","author":"Houx","year":"2008","journal-title":"Physiol. Behav."},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Keesom, S.M., Finton, C.J., Sell, G.L., and Hurley, L.M. (2017). Early-Life Social Isolation Influences Mouse Ultrasonic Vocalizations during Male-Male Social Encounters. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0169705"},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Chabout, J., Serreau, P., Ey, E., Bellier, L., Aubin, T., Bourgeron, T., and Granon, S. (2012). Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0029401"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1002\/dev.420110302","article-title":"Neonatal ultrasounds elicited by odor cues","volume":"11","author":"Conely","year":"1978","journal-title":"Dev. Psychobiol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1002\/dev.420200410","article-title":"Isolation distress in two-week-old rats: Influence of home cage, social companions, and prior experience with littermates","volume":"20","author":"Hofer","year":"1987","journal-title":"Dev. Psychobiol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1002\/dev.10112","article-title":"Rat pups reduce ultrasonic vocalization after exposure to an adult male rat","volume":"42","author":"Wiedenmayer","year":"2003","journal-title":"Dev. Psychobiol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.bbr.2007.05.035","article-title":"Neonatal basal forebrain cholinergic hypofunction affects ultrasonic vocalizations and fear conditioning responses in preweaning rats","volume":"183","author":"Ricceri","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1037\/0735-7044.113.1.51","article-title":"Behavioral mechanisms for active maternal potentiation of isolation calling in rat pups","volume":"113","author":"Hofer","year":"1999","journal-title":"Behav. Neurosci."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1037\/0735-7044.109.1.117","article-title":"Effect of isolation conditions on brain regional enkephalin and \u03b2-endorphin levels and vocalizations in 10-day-old rat pups","volume":"109","author":"Shoemaker","year":"1995","journal-title":"Behav. Neurosci."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1016\/S0028-3908(00)00052-6","article-title":"Pharmacological blockade or genetic deletion of substance P (NK1) receptors attenuates neonatal vocalisation in guinea-pigs and mice","volume":"39","author":"Rupniak","year":"2000","journal-title":"Neuropharmacology"},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/S0091-3057(02)00781-5","article-title":"Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long\u2013Evans rats","volume":"73","author":"Kalinichev","year":"2002","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1016\/S0091-3057(02)00809-2","article-title":"Effects of corticotropin-releasing hormone on distress vocalizations and locomotion in maternally separated mouse pups","volume":"72","author":"Dirks","year":"2002","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/S0143-4179(03)00043-X","article-title":"Long-term effects of short and long periods of maternal separation on brain opioid peptide levels in male Wistar rats","volume":"37","author":"Ploj","year":"2003","journal-title":"Neuropeptides"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1016\/j.bbr.2006.10.027","article-title":"Neurobehavioural disorders in the infant reeler mouse model: Interaction of genetic vulnerability and consequences of maternal separation","volume":"177","author":"Ognibene","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.brainres.2012.07.013","article-title":"Behavioral changes after maternal separation are reversed by chronic constant light treatment","volume":"1480","author":"Dimatelis","year":"2012","journal-title":"Brain Res."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1002\/dev.420230804","article-title":"The effects of opioid and benzodiazepine antagonists on dam-induced reductions in rat pup isolation distress","volume":"23","author":"Carden","year":"1990","journal-title":"Dev. Psychobiol."},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1037\/0735-7044.104.3.457","article-title":"Socially mediated reduction of isolation distress in rat pups is blocked by naltrexone but not by Ro 15-1788","volume":"104","author":"Carden","year":"1990","journal-title":"Behav. Neurosci."},{"key":"ref_112","doi-asserted-by":"crossref","unstructured":"Delwig, A., Logan, A.M., Copenhagen, D.R., and Ahn, A.H. (2012). Light Evokes Melanopsin-Dependent Vocalization and Neural Activation Associated with Aversive Experience in Neonatal Mice. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0043787"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1002\/dev.420110513","article-title":"Ultrasonic vocalization during social interaction and isolation in 2-weeek-old rats","volume":"11","author":"Hofer","year":"1978","journal-title":"Dev. Psychobiol."},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1002\/dev.420270804","article-title":"Potentiation of isolation-induced vocalization by brief exposure of rat pups to maternal cues","volume":"27","author":"Hofer","year":"1994","journal-title":"Dev. Psychobiol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1002\/dev.420220603","article-title":"Isolation distress and maternal comfort responses of two-week-old rat pups reared in social isolation","volume":"22","author":"Hofer","year":"1989","journal-title":"Dev. Psychobiol."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1016\/j.bbr.2007.02.016","article-title":"Acquisition and expression of a socially mediated separation response","volume":"182","author":"Shair","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1037\/0735-7036.118.1.95","article-title":"Brief maternal interaction increases number, amplitude, and bout size of isolation-induced ultrasonic vocalizations in infant rats (Rattus norvegicus)","volume":"118","author":"Myers","year":"2004","journal-title":"J. Comp. Psychol."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1292\/jvms.18-0604","article-title":"Relationship between motor function and ultrasonic vocalizations induced by maternal separation in rat pups","volume":"81","author":"Isobe","year":"2019","journal-title":"J. Vet. Med. Sci."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1016\/S0091-3057(99)00149-5","article-title":"Sex-Dependent Behavioral Effects of the Neurosteroid Allopregnanolone (3\u03b1,5\u03b1-THP) in Neonatal and Adult Rats after Postnatal Stress","volume":"64","author":"Zimmerberg","year":"1999","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"112877","DOI":"10.1016\/j.physbeh.2020.112877","article-title":"Brief but enough: 45-min maternal separation elicits behavioral and physiological responses in neonatal mice and changes in dam maternal behavior","volume":"222","author":"Burenkova","year":"2020","journal-title":"Physiol. Behav."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1016\/j.pbb.2008.04.014","article-title":"Clozapine and olanzapine exhibit an intrinsic anxiolytic property in two conditioned fear paradigms: Contrast with haloperidol and chlordiazepoxide","volume":"90","author":"Mead","year":"2008","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1002\/1098-2302(200011)37:3<121::AID-DEV1>3.0.CO;2-F","article-title":"Conditioned changes in ultrasonic vocalizations to an aversive olfactory stimulus are lateralized in 6-day-old rats","volume":"37","author":"Weber","year":"2000","journal-title":"Dev. Psychobiol."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1292\/jvms.65.1299","article-title":"Conditioned fear-related ultrasonic vocalizations are emitted as an emotional response","volume":"65","author":"Kikusui","year":"2003","journal-title":"J. Vet. Med. Sci."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"1744","DOI":"10.1186\/1744-8069-1-10","article-title":"Contribution of CaMKIV to Injury and Fear-Induced Ultrasonic Vocalizations in Adult Mice","volume":"1","author":"Ko","year":"2005","journal-title":"Mol. Pain."},{"key":"ref_125","doi-asserted-by":"crossref","first-page":"1309","DOI":"10.1016\/j.neuroscience.2005.11.063","article-title":"Behavioral, central monoaminergic and hypothalamo\u2013pituitary\u2013adrenal axis correlates of fear-conditioned analgesia in rats","volume":"138","author":"Finn","year":"2006","journal-title":"Neuroscience"},{"key":"ref_126","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/j.bbr.2007.06.006","article-title":"Effects of chronic footshock, restraint and corticotropin-releasing factor on freezing, ultrasonic vocalization and forced swim behavior in rats","volume":"183","author":"Swiergiel","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_127","doi-asserted-by":"crossref","unstructured":"Kim, E.J., Kim, E.S., Covey, E., and Kim, J.J. (2010). Social Transmission of Fear in Rats: The Role of 22-kHz Ultrasonic Distress Vocalization. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0015077"},{"key":"ref_128","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/j.pbb.2010.02.005","article-title":"Anxiolytic-like property of risperidone and olanzapine as examined in multiple measures of fear in rats","volume":"95","author":"Sun","year":"2010","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_129","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.bbr.2011.09.004","article-title":"Early fear as a predictor of avoidance in a rat model of post-traumatic stress disorder","volume":"226","author":"Chen","year":"2012","journal-title":"Behav. Brain Res."},{"key":"ref_130","doi-asserted-by":"crossref","unstructured":"Bonasera, S.J., Schenk, A.K., Luxenberg, E.J., Wang, X., Basbaum, A., and Tecott, L.H. (2015). Mice Lacking Serotonin 2C Receptors Have increased Affective Responses to Aversive Stimuli. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0142906"},{"key":"ref_131","doi-asserted-by":"crossref","first-page":"104140","DOI":"10.1016\/j.beproc.2020.104140","article-title":"Acute stress differentially affects grooming subtypes and ultrasonic vocalisations in the open-field and home-cage test in rats","volume":"176","author":"Brenes","year":"2020","journal-title":"Behav. Process."},{"key":"ref_132","doi-asserted-by":"crossref","unstructured":"Karwicka, W., Wiatrowska, M., Kondrakiewicz, K., Knapska, E., Kursa, M.B., and Hamed, A. (2021). Relaying Aversive Ultrasonic Alarm Calls Depends on Previous Experience. Empathy, Social Buffering, or Panic?. Brain Sci., 11.","DOI":"10.20944\/preprints202105.0115.v1"},{"key":"ref_133","doi-asserted-by":"crossref","unstructured":"Fendt, M., Gonzalez-Guerrero, C.P., and Kahl, E. (2021). Observational Fear Learning in Rats: Role of Trait Anxiety and Ultrasonic Vocalization. Brain Sci., 11.","DOI":"10.3390\/brainsci11040423"},{"key":"ref_134","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/S0166-4328(02)00321-2","article-title":"22-kHz ultrasonic vocalization in rats as an index of anxiety but not fear: Behavioral and pharmacological modulation of affective state","volume":"141","author":"Jelen","year":"2003","journal-title":"Behav. Brain Res."},{"key":"ref_135","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1007\/BF02245522","article-title":"22-28 kHz ultrasonic vocalizations associated with defensive reactions in male rats do not result from fear or aversion","volume":"111","author":"Portavella","year":"1993","journal-title":"Psychopharmacology"},{"key":"ref_136","doi-asserted-by":"crossref","first-page":"7654","DOI":"10.1523\/JNEUROSCI.1644-04.2004","article-title":"Selective Neurotoxic Lesions of Basolateral and Central Nuclei of the Amygdala Produce Differential Effects on Fear Conditioning","volume":"24","author":"Koo","year":"2004","journal-title":"J. Neurosci."},{"key":"ref_137","doi-asserted-by":"crossref","first-page":"804","DOI":"10.1007\/s10517-012-1831-4","article-title":"Ultrasonic vocalization of rats in various motivational and emotional states","volume":"153","author":"Pertsov","year":"2012","journal-title":"Bull. Exp. Biol. Med."},{"key":"ref_138","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/j.bbr.2011.07.040","article-title":"Activity of cholinergic neurons in the laterodorsal tegmental nucleus during emission of 22 kHz vocalization in rats","volume":"225","author":"Brudzynski","year":"2011","journal-title":"Behav. Brain Res."},{"key":"ref_139","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pbb.2014.01.013","article-title":"Blocking of corticotrophin releasing factor receptor-1 during footshock attenuates context fear but not the upregulation of prepro-orexin mRNA in rats","volume":"120","author":"Chen","year":"2014","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_140","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1016\/j.autneu.2004.08.014","article-title":"Expression of cardiovascular and behavioural components of conditioned fear to context in T4 spinally transected rats","volume":"120","author":"Choi","year":"2005","journal-title":"Auton. Neurosci."},{"key":"ref_141","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/j.jneumeth.2005.10.007","article-title":"Opposite effects of short- and long-duration isolation on ultrasonic vocalization, startle and prepulse inhibition in rats","volume":"153","author":"Tomazini","year":"2006","journal-title":"J. Neurosci. Methods"},{"key":"ref_142","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1177\/0269881112460108","article-title":"Behavioural, neurochemical and neuroendocrine effects of the endogenous \u03b2-carboline harmane in fear-conditioned rats","volume":"27","author":"Smith","year":"2013","journal-title":"J. Psychopharmacol."},{"key":"ref_143","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1016\/j.physbeh.2004.10.006","article-title":"The influence of social environmental condition on the production of stress-induced 22 kHz calls in adult male Wistar rats","volume":"84","author":"Inagaki","year":"2005","journal-title":"Physiol. Behav."},{"key":"ref_144","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1159\/000085820","article-title":"Isolation-induced changes in ultrasonic vocalization, fear-potentiated startle and prepulse inhibition in rats","volume":"51","author":"Nobre","year":"2005","journal-title":"Neuropsychobiology"},{"key":"ref_145","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1017\/neu.2013.6","article-title":"Differential ultrasonic indices of separation distress in the presence and absence of maternal cues in infant rats bred for high and low positive social affect","volume":"25","author":"Iacobucci","year":"2013","journal-title":"Acta Neuropsychiatr."},{"key":"ref_146","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.bbr.2007.03.004","article-title":"Ultrasonic calls of rats as indicator variables of negative or positive states: Acetylcholine\u2013dopamine interaction and acoustic coding","volume":"182","author":"Brudzynski","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_147","doi-asserted-by":"crossref","first-page":"1169","DOI":"10.1016\/j.neubiorev.2005.04.007","article-title":"Acoustic characteristics of air puff-induced 22-kHz alarm calls in direct recordings","volume":"29","author":"Brudzynski","year":"2005","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_148","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/0031-9384(90)90253-Z","article-title":"Startle-inducing acoustic stimuli evoke ultrasonic vocalization in the rat","volume":"48","author":"Kaltwasser","year":"1990","journal-title":"Physiol. Behav."},{"key":"ref_149","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.bbr.2013.07.013","article-title":"Ultrasonic vocalizations, predictability and sensorimotor gating in the rat","volume":"253","author":"Webber","year":"2013","journal-title":"Behav. Brain Res."},{"key":"ref_150","doi-asserted-by":"crossref","unstructured":"Olszy\u0144ski, K.H., Polowy, R., Wardak, A.D., Grymanowska, A.W., and Filipkowski, R.K. (2021). Increased Vocalization of Rats in Response to Ultrasonic Playback as a Sign of Hypervigilance Following Fear Conditioning. Brain Sci., 11.","DOI":"10.3390\/brainsci11080970"},{"key":"ref_151","doi-asserted-by":"crossref","unstructured":"Atsak, P., Orre, M., Bakker, P., Cerliani, L., Roozendaal, B., Gazzola, V., Moita, M., and Keysers, C. (2011). Experience Modulates Vicarious Freezing in Rats: A Model for Empathy. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0021855"},{"key":"ref_152","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1037\/0735-7044.112.1.126","article-title":"A sensory-enhanced context facilitates learning and multiple measures of unconditioned stimulus processing in the preweanling rat","volume":"112","author":"Brasser","year":"1998","journal-title":"Behav. Neurosci."},{"key":"ref_153","first-page":"A102","article-title":"Air-Puff Induced Vocalizations: A Novel Approach to Detecting Negative Affective State Following Concussion in Rats","volume":"33","author":"Browning","year":"2016","journal-title":"J. Neurotrauma"},{"key":"ref_154","doi-asserted-by":"crossref","first-page":"E9","DOI":"10.1002\/lary.27355","article-title":"Social isolation alters ultrasonic vocalizations but not thyroarytenoid neuromuscular junctions in old rats","volume":"129","author":"Johnson","year":"2019","journal-title":"Laryngoscope"},{"key":"ref_155","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1111\/j.1749-6632.1999.tb07880.x","article-title":"Short- and Long-term Consequences of Corticotropin-releasing Factor in Early Development","volume":"897","author":"Hennessy","year":"1999","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_156","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1023\/A:1023684503883","article-title":"Forskolin as a tool for examining adenylyl cyclase expression, regulation, and G protein signaling","volume":"23","author":"Insel","year":"2003","journal-title":"Cell Mol. Neurobiol."},{"key":"ref_157","doi-asserted-by":"crossref","first-page":"2652","DOI":"10.1038\/sj.npp.1301061","article-title":"Anxiolytic-Like Properties of the Anandamide Transport Inhibitor AM404","volume":"31","author":"Bortolato","year":"2006","journal-title":"Neuropsychopharmacology"},{"key":"ref_158","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.bbr.2006.12.015","article-title":"Substance P injected into the dorsal periaqueductal gray causes anxiogenic effects similar to the long-term isolation as assessed by ultrasound vocalizations measurements","volume":"182","author":"Bassi","year":"2007","journal-title":"Behav. Brain Res."},{"key":"ref_159","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/0091-3057(88)90266-3","article-title":"Milk-induced analgesia and comforting in 10-day-old rats: Opioid mediation","volume":"29","author":"Blass","year":"1988","journal-title":"Pharmacol. Biochem. Behav."},{"key":"ref_160","doi-asserted-by":"crossref","unstructured":"Grimsley, J.M.S., Sheth, S., Vallabh, N., Grimsley, C.A., Bhattal, J., Latsko, M., Jasnow, A., and Wenstrup, J.J. (2016). Contextual Modulation of Vocal Behavior in Mouse: Newly Identified 12 kHz \u201cMid-Frequency\u201d Vocalization Emitted during Restraint. Front. Behav. Neurosci., 10.","DOI":"10.3389\/fnbeh.2016.00038"},{"key":"ref_161","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1007\/BF02257410","article-title":"Effect of clonidine on the responsiveness of infant rats to maternal stimuli","volume":"111","author":"Hansen","year":"1993","journal-title":"Psychopharmacology"},{"key":"ref_162","doi-asserted-by":"crossref","unstructured":"Granata, L.E., Valentine, A., Hirsch, J.L., and Brenhouse, H.C. (2022). Infant ultrasonic vocalizations predict adolescent social behavior in rats: Effects of early life adversity. Dev. Psychobiol., 64.","DOI":"10.1002\/dev.22260"},{"key":"ref_163","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1080\/10253890.2018.1455090","article-title":"Chasing as a model of psychogenic stress: Characterization of physiological and behavioral responses","volume":"21","author":"Lee","year":"2018","journal-title":"Stress"},{"key":"ref_164","doi-asserted-by":"crossref","first-page":"100755","DOI":"10.1016\/j.bbih.2024.100755","article-title":"Chronic variable stress leads to sex specific gut microbiome alterations in mice","volume":"37","author":"Kropp","year":"2024","journal-title":"Brain Behav. Immun. Health"},{"key":"ref_165","unstructured":"US Animal and Plant Health Inspection Service (2022, September 12). Animal Care Tech Note: Categorizing Animal Pain or Distress in Research Facility Annual Reports. Animal Welfare Care Act. Published Online 2023, Available online: https:\/\/www.aphis.usda.gov\/sites\/default\/files\/ac-tech-note-categorizing-animal-pain-or-distress.pdf."},{"key":"ref_166","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1016\/j.conb.2019.12.008","article-title":"Using rat ultrasonic vocalization to study the neurobiology of emotion: From basic science to the development of novel therapeutics for affective disorders","volume":"60","author":"Burgdorf","year":"2020","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_167","doi-asserted-by":"crossref","first-page":"R352","DOI":"10.1152\/ajpregu.00021.2016","article-title":"Long-lasting bradypnea induced by repeated social defeat","volume":"311","author":"Brouillard","year":"2016","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_168","first-page":"207","article-title":"The Mighty Mouse: The impact of rodents on advances in biomedical research","volume":"110","author":"Bryda","year":"2013","journal-title":"Mo. Med."},{"key":"ref_169","doi-asserted-by":"crossref","unstructured":"Burke, K., Screven, L.A., and Dent, M.L. (2018). CBA\/CaJ mouse ultrasonic vocalizations depend on prior social experience. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0197774"},{"key":"ref_170","doi-asserted-by":"crossref","unstructured":"Boulanger-Bertolus, J., and Mouly, A.M. (2021). Ultrasonic Vocalizations Emission across Development in Rats: Coordination with Respiration and Impact on Brain Neural Dynamics. Brain Sci., 11.","DOI":"10.3390\/brainsci11050616"},{"key":"ref_171","doi-asserted-by":"crossref","unstructured":"Lenell, C., Broadfoot, C.K., Schaen-Heacock, N.E., and Ciucci, M.R. (2021). Biological and Acoustic Sex Differences in Rat Ultrasonic Vocalization. Brain Sci., 11.","DOI":"10.3390\/brainsci11040459"},{"key":"ref_172","doi-asserted-by":"crossref","first-page":"R951","DOI":"10.1152\/ajpregu.00528.2013","article-title":"Amygdala mediates respiratory responses to sudden arousing stimuli and to restraint stress in rats","volume":"306","author":"Bondarenko","year":"2014","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_173","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1152\/jn.00590.2019","article-title":"Role of deep breaths in ultrasonic vocal production of Sprague-Dawley rats","volume":"123","author":"Riede","year":"2020","journal-title":"J. Neurophysiol."},{"key":"ref_174","unstructured":"Terjung, R. (2021). Sex-Specific Effects of Stress on Respiratory Control: Plasticity, Adaptation, and Dysfunction. Comprehensive Physiology, Wiley. [1st ed.]."},{"key":"ref_175","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1037\/0735-7044.107.2.354","article-title":"Ultrasonic vocalization, laryngeal braking, and thermogenesis in rat pups: A reappraisal","volume":"107","author":"Hofer","year":"1993","journal-title":"Behav. Neurosci."}],"container-title":["Brain Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-3425\/14\/11\/1109\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:25:02Z","timestamp":1760113502000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-3425\/14\/11\/1109"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,31]]},"references-count":175,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2024,11]]}},"alternative-id":["brainsci14111109"],"URL":"https:\/\/doi.org\/10.3390\/brainsci14111109","relation":{},"ISSN":["2076-3425"],"issn-type":[{"value":"2076-3425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,31]]}}}