Positive and negative ultrasonic social signals elicit opposing firing patterns in rat amygdala
Open accessAbstract
Rat ultrasonic vocalizations (USVs) are ethologically-essential social signals. Under natural conditions, 22kHz USVs and 50kHz USVs are emitted in association with negative and positive emotional states, respectively. Our first experiment examined freezing behavior elicited in naïve Sprague-Dawley rats by a 22kHz USV, a 50kHz USV, and frequency-matched tones. None of the stimuli elicited freezing, which is the most commonly-used index of fear. The second experiment examined single-unit responses to these stimuli in the amygdala (AM), which is well-known for its role in innate and acquired fear responses. Among 127 well-discriminated single units, 82% were auditory-responsive. Elicited firing patterns were classified using a multi-dimensional scheme that included transient (phasic) responses to the stimulus onsets and/or offsets as well as sustained (tonic) responses during the stimulus. Tonic responses, which are not ordinarily evaluated in AM, were 4.4-times more common than phasic responses. The 22kHz stimuli tended to elicit tonic increases in the firing rates, whereas the 50kHz stimuli more often elicited tonic decreases in firing rates. These opposing tonic responses correspond with the ethological valence of USVs in the two frequency bands. Thus, a relatively-small sample of single-unit responses in AM furnished a more sensitive index of emotional valence than freezing behavior. Latency analysis suggested that stimuli in the two frequency bands are processed through different pathways to AM. One possible interpretation is that phasic responses in AM reflect the detection of a stimulus change, whereas tonic responses indicate the valence of the detected stimulus.
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Rat ultrasonic vocalizations can be categorized into two main groups: positive/"happy" 50 kHz USVs and negative/"distress" 22 kHz USVs.
“USVs in rats can be categorized into 2 main groups: positive/“happy” 50 kHz USVs and negative/“distress” 22 kHz USVs.7-9,24,33,38,39,41”
From Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats (2022) · cites this paper as [33]
Ultrasonic vocalizations are a sensitive method of assessing rodent communication and affective state.
“Ultrasonic vocalizations (USVs) are a sensitive method of assessing rodent communication and affective state9,33”
From Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats (2022) · cites this paper as [33]
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Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Blood, A. J., & Zatorre, R. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.191355898 · Cited by 2,814 · see citing works
Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-01-00411.1998 · Cited by 2,205 · see citing works
A differential neural response in the human amygdala to fearful and happy facial expressions
Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., & Dolan, R. J. (1996) · Nature · doi:10.1038/383812a0 · Cited by 2,013 · see citing works
Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression
Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., Strauss, M. M., Hyman, S. E., & Rosen, B. R. (1996) · Neuron · doi:10.1016/s0896-6273(00)80219-6 · Cited by 1,711 · see citing works
Herdegen, T., & Leah, J. D. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00018-6 · Cited by 1,352 · see citing works
A neuromodulatory role for the human amygdala in processing emotional facial expressions
Morris, J. (1998) · Brain · doi:10.1093/brain/121.1.47 · Cited by 1,291 · see citing works
The neuroanatomical and neurochemical basis of conditioned fear
Fendt, M., & Fanselow, M. S. (1999) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(99)00016-0 · Cited by 1,092 · see citing works
The human amygdala and the emotional evaluation of sensory stimuli
Zald, D. H. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(02)00248-5 · Cited by 1,062 · see citing works
The neural basis of romantic love
Bartels, A., & Zeki, S. (2000) · NeuroReport · doi:10.1097/00001756-200011270-00046 · Cited by 1,020 · see citing works
Pape, H.-C., & Pare, D. (2010) · Physiological Reviews · doi:10.1152/physrev.00037.2009 · Cited by 994 · see citing works
The primate amygdala represents the positive and negative value of visual stimuli during learning
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006) · Nature · doi:10.1038/nature04490 · Cited by 917 · see citing works
Quirk, G. J., Repa, J. C., & LeDoux, J. E. (1995) · Neuron · doi:10.1016/0896-6273(95)90092-6 · Cited by 808 · see citing works
Innate and conditioned reactions to threat in rats with amygdaloid lesions.
Blanchard, D. C., & Blanchard, R. J. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0033521 · Cited by 753 · see citing works
The amygdala, reward and emotion
Murray, E. A. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.08.013 · Cited by 679 · see citing works
The neurobiology of positive emotions
Burgdorf, J., & Panksepp, J. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.001 · Cited by 677 · see citing works
An fMRI study of personality influences on brain reactivity to emotional stimuli.
Canli, T., Zhao, Z., Desmond, J., Kang, E., Gross, J., & Gabrieli, J. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.1.33 · Cited by 628 · see citing works
Ultrasonic vocalizations as indices of affective states in rats
Knutson, B., Burgdorf, J., & Panksepp, J. (2002) · Psychological Bulletin · doi:10.1037/0033-2909.128.6.961 · Cited by 618 · see citing works
Amygdala volume and social network size in humans
Bickart, K. C., Wright, C. I., Dautoff, R. J., Dickerson, B. C., & Barrett, L. F. (2011) · Nature Neuroscience · doi:10.1038/nn.2724 · Cited by 556 · see citing works
Ultrasonic Communication by Animals
Sales, G., & Pye, D. (1974) · Springer eBooks · doi:10.1007/978-94-011-6901-1 · Cited by 539 · see citing works
Fear, faces, and the human amygdala
Adolphs, R. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.06.006 · Cited by 502 · see citing works
Amygdala response to happy faces as a function of extraversion
Canli, T., Sivers, H., Whitfield, S. L., Gotlib, I. H., & Gabrieli, J. D. E. (2002) · Science · doi:10.1126/science.1068749 · Cited by 493 · see citing works
Burgdorf, J., Kroes, R. A., Moskal, J. R., Pfaus, J. G., Brudzynski, S. M., & Panksepp, J. (2008) · Journal of Comparative Psychology · doi:10.1037/a0012889 · Cited by 469 · see citing works
“Laughing” rats and the evolutionary antecedents of human joy?
Panksepp, J., & Burgdorf, J. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00159-8 · Cited by 462 · see citing works
Blanchard, R. J., Blanchard, D. C., Agullana, R., & Weiss, S. M. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90423-l · Cited by 461 · see citing works
Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats.
Knutson, B. D., Burgdorf, J. S., & Panksepp, J. (1998) · Journal of comparative psychology · doi:10.1037/0735-7036.112.1.65 · Cited by 456 · see citing works
Two different lateral amygdala cell populations contribute to the initiation and storage of memory
Repa, J. C., Muller, J., Apergis, J., Desrochers, T. M., Zhou, Y., & LeDoux, J. E. (2001) · Nature Neuroscience · doi:10.1038/89512 · Cited by 440 · see citing works
Brain Activation during Human Male Ejaculation
Holstege, G., Georgiadis, J. R., Paans, A. M. J., Meiners, L. C., van der Graaf, F. H. C. E., & Reinders, A. A. T. S. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-27-09185.2003 · Cited by 424 · see citing works
Romanski, L. M., & LeDoux, J. E. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.6.515 · Cited by 398 · see citing works
Winston, J. S., O’Doherty, J. P., & Dolan, R. J. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00303-3 · Cited by 398 · see citing works
Panksepp, J., & Burgdorf, J. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00238-2 · Cited by 362 · see citing works
Furtak, S. C., Wei, S., Agster, K. L., & Burwell, R. D. (2007) · Hippocampus · doi:10.1002/hipo.20314 · Cited by 282 · see citing works
Ultrasound and mating behaviour in rodents with some observations on other behavioural situations
Sales, G. (1972) · Journal of Zoology · doi:10.1111/j.1469-7998.1972.tb01345.x · Cited by 268 · see citing works
Ultrasonic Communication in Rats: Can Playback of 50-kHz Calls Induce Approach Behavior?
Wöhr, M., & Schwarting, R. K. W. (2007) · PLoS ONE · doi:10.1371/journal.pone.0001365 · Cited by 266 · see citing works
Amygdalar activation associated with positive and negative facial expressions
Yang, T. T., Menon, V., D, S. E. M., Blasey, C. M., White, C. D., Reid, A. J., Gotlib, I. H., & Reiss, A. L. (2002) · Neuroreport · doi:10.1097/00001756-200210070-00009 · Cited by 265 · see citing works
Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions
Prather, M. D., Lavenex, P., Mauldin-Jourdain, M. L., Mason, W. A., Capitanio, J. P., Mendoza, S. P., & Amaral, D. G. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00445-6 · Cited by 248 · see citing works
Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats.
Burgdorf, J. S., Knutson, B. D., & Panksepp, J. (2000) · Behavioral Neuroscience · doi:10.1037/0735-7044.114.2.320 · Cited by 244 · see citing works
Rat 22kHz ultrasonic vocalizations as alarm cries
Litvin, Y., Blanchard, D. C., & Blanchard, R. J. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.11.038 · Cited by 242 · see citing works
Principles of Rat Communication: Quantitative Parameters of Ultrasonic Calls in Rats
Brudzynski, S. M. (2005) · Behavior Genetics · doi:10.1007/s10519-004-0858-3 · Cited by 242 · see citing works
Brudzyński, S. M. (2009) · ILAR Journal · doi:10.1093/ilar.50.1.43 · Cited by 223 · see citing works
Social Transmission of Fear in Rats: The Role of 22-kHz Ultrasonic Distress Vocalization
Kim, E. J., Kim, E. S., Covey, E., & Kim, J. J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015077 · Cited by 216 · see citing works
Social contacts and production of 50-kHz short ultrasonic calls in adult rats.
Brudzyński, S. M., & Pniak, A. (2002) · Journal of comparative psychology · doi:10.1037/0735-7036.116.1.73 · Cited by 205 · see citing works
Stutzmann, G. E., & LeDoux, J. E. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-11-j0005.1999 · Cited by 198 · see citing works
Redefining the tonotopic core of rat auditory cortex: Physiological evidence for a posterior field
Doron, N. N., LeDoux, J. E., & Semple, M. N. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10412 · Cited by 197 · see citing works
Amygdalar NMDA Receptors Are Critical for the Expression of Multiple Conditioned Fear Responses
Lee, H. J., Choi, J.-S., Brown, T. H., & Kim, J. J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-04116.2001 · Cited by 195 · see citing works
Self-citationShabel, S. J., & Janak, P. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905580106 · Cited by 190 · see citing works
Thomas, D. A., Takahashi, L. K., & Barfield, R. J. (1983) · Journal of Comparative Psychology · doi:10.1037/0735-7036.97.3.201 · Cited by 187 · see citing works
Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala.
Uwano, T., Nishijo, H., Ono, T., & Tamura, R. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00125-3 · Cited by 176 · see citing works
Sadananda, M., Wöhr, M., & Schwarting, R. K. W. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.02.002 · Cited by 169 · see citing works
Tornatzky, W., & Miczek, K. A. (1994) · Psychopharmacology · doi:10.1007/bf02245339 · Cited by 168 · see citing works
Behavioural responses of laboratory rats to playback of 22 kHz ultrasonic calls
Brudzyński, S. M., & Chiu, E. M. C. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(95)00003-2 · Cited by 159 · see citing works
Characterisation of multiple physiological fields within the anatomical core of rat auditory cortex
Rutkowski, R. G., Miasnikov, A. A., & Weinberger, N. M. (2003) · Hearing Research · doi:10.1016/s0378-5955(03)00182-5 · Cited by 151 · see citing works
Maren, S. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00281.x · Cited by 139 · see citing works
Auditory-Evoked Spike Firing in the Lateral Amygdala and Pavlovian Fear Conditioning
Goosens, K. A., Hobin, J. A., & Maren, S. (2003) · Neuron · doi:10.1016/s0896-6273(03)00728-1 · Cited by 135 · see citing works
Pharmacological and behavioral characteristics of 22 kHz alarm calls in rats
Brudzyński, S. M. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00058-6 · Cited by 128 · see citing works
The Production of Ultrasonic Sounds by Laboratory Rats and Other Mammals
Anderson, J. W. (1954) · Science · doi:10.1126/science.119.3101.808 · Cited by 118 · see citing works
SEWELL, G. D. (1967) · Nature · doi:10.1038/215512a0 · Cited by 115 · see citing works
Goosens, K. A., & Maren, S. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03513.x · Cited by 108 · see citing works
Ultrasonic vocalization of the female rat (Rattus norvegicus) during mating
Thomas, D. A., & Barfield, R. J. (1985) · Animal Behaviour · doi:10.1016/s0003-3472(85)80002-6 · Cited by 106 · see citing works
Choi, J.-S., & Brown, T. H. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08713.2003 · Cited by 106 · see citing works
Self-citationMa, S. T., Maier, E. Y., Ahrens, A. M., Schallert, T. J., & Duvauchelle, C. L. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.04.001 · Cited by 100 · see citing works
Central C-Fos Expression Following 20kHz/Ultrasound Induced Defence Behaviour in the Rat
Beckett, S. R. G., Duxon, M. S., Aspley, S., & Marsden, C. A. (1997) · Brain Research Bulletin · doi:10.1016/s0361-9230(96)00332-2 · Cited by 96 · see citing works
Perirhinal Cortex Supports Delay Fear Conditioning to Rat Ultrasonic Social Signals
Lindquist, D. H., Jarrard, L. E., & Brown, T. H. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4839-03.2004 · Cited by 95 · see citing works
Self-citationResponse characteristics of basolateral and centromedial neurons in the primate amygdala
Mosher, C. P., Zimmerman, P. E., & Gothard, K. M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3225-10.2010 · Cited by 92 · see citing works
Handbook of Mammalian Vocalization
(2010) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(10)70001-1 · Cited by 84 · see citing works
Are rats predisposed to learn 22kHz calls as danger-predicting signals?
Endres, T., Widmann, K., & Fendt, M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.07.012 · Cited by 78 · see citing works
Ultrasonic vocalizations as indicators of welfare for laboratory rats (Rattus norvegicus)
Burman, O. H. P., Ilyat, A., Jones, G., & Mendl, M. (2006) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2006.04.028 · Cited by 77 · see citing works
The effect of 22 kHz calls and artificial 38 kHz signals on activity in rats
Sales, G. (1991) · Behavioural Processes · doi:10.1016/0376-6357(91)90001-g · Cited by 77 · see citing works
High-frequency ultrasonic vocalization induced by intracerebral glutamate in rats
Fu, X.-W., & Brudzyński, S. M. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90231-3 · Cited by 74 · see citing works
Fear conditioning to discontinuous auditory cues requires perirhinal cortical function.
Kholodar-Smith, D. B., Allen, T. A., & Brown, T. H. (2008) · Behavioral Neuroscience · doi:10.1037/a0012902 · Cited by 72 · see citing works
Self-citationAsymmetrical stimulus generalization following differential fear conditioning
Bang, S. J., Allen, T. A., Jones, L. K., Boguszewski, P. M., & Brown, T. H. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.02.009 · Cited by 45 · see citing works
Self-citationSingle-unit responses to 22kHz ultrasonic vocalizations in rat perirhinal cortex
Allen, T. A., Furtak, S. C., & Brown, T. H. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.03.009 · Cited by 42 · see citing works
Self-citationNeophytou, S. I., Graham, M., Williams, J., Aspley, S., Marsden, C. A., & Beckett, S. R. G. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02334-3 · Cited by 41 · see citing works
Furtak, S. C., Allen, T. A., & Brown, T. H. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1653-07.2007 · Cited by 39 · see citing works
Self-citationPerirhinal cortex supports acquired fear of auditory objects
Bang, S. J., & Brown, T. H. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2009.01.002 · Cited by 39 · see citing works
Self-citationActivation of limbic system structures by replay of ultrasonic vocalization in rats
Wöhr, M., & Schwarting, R. K. W. (2010) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-374593-4.00012-7 · Cited by 34 · see citing works
Fashena, D. (1999) · doi:10.1002/(sici)1096-9861(19990412)406:3
Flagged first, then by citations
Research works printed but not linked: 3
- [30]Sales GD The effect of 22kHz calls and artificial 38kHz signals on activity in rats Behav Processes 1991 24 83 93 24923696
- [67]Morris JS Friston KJ Buchel C Frith CD Young AW Calder AJ Dolan RJ A neuromodulatory role for the human amygdala in processing emotional facial expressions Brain 1998 121 47 57 9549487
- [73]Shi CJ Cassell MD Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat J Comp Neurol 1999 406 299 328 10102498
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Ethotransmission: communication of emotional states through ultrasonic vocalization in rats.
Brudzynski, S. M. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.01.014 · Cited by 416 · see citing works
Wöhr, M., & Schwarting, R. K. W. (2013) · Cell and Tissue Research · doi:10.1007/s00441-013-1607-9 · Cited by 371 · see citing works
Neural circuits of social behaviors: Innate yet flexible
Wei, D., Talwar, V., & Lin, D. (2021) · Neuron · doi:10.1016/j.neuron.2021.02.012 · Cited by 185 · see citing works
Wöhr, M., & Scattoni, M. L. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.047 · Cited by 178 · see citing works
Willuhn, I., Tose, A. J., Wanat, M. J., Hart, A. S., Hollon, N. G., Phillips, P. E. M., Schwarting, R. K. W., & Wöhr, M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1060-14.2014 · Cited by 154 · see citing works
Hickman, D. L., Johnson, J., Vemulapalli, T. H., Crisler, J. R., & Shepherd, R. K. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802151-4.00007-4 · Cited by 150 · see citing works
Pro-social ultrasonic communication in rats: Insights from playback studies
Seffer, D., Schwarting, R. K. W., & Wöhr, M. (2014) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2014.01.023 · Cited by 130 · see citing works
On the relationships between ultrasonic calling and anxiety-related behavior in rats
Schwarting, R. K. W., & Wöhr, M. (2012) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2012007500038 · Cited by 108 · see citing works
Rincón‐Cortés, M., & Sullivan, R. M. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.205 · Cited by 101 · see citing works
A comparison of neural responses to appetitive and aversive stimuli in humans and other mammals
Hayes, D. J., Duncan, N. W., Xu, J., & Northoff, G. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.06.018 · Cited by 98 · see citing works
Willadsen, M., Seffer, D., Schwarting, R. K. W., & Wöhr, M. (2013) · Journal of comparative psychology · doi:10.1037/a0034778 · Cited by 92 · see citing works
Grimsley, J. M. S., Sheth, S. P., Vallabh, N., Grimsley, C. A., Bhattal, J., Latsko, M. S., Jasnow, A. M., & Wenstrup, J. J. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00038 · Cited by 88 · see citing works
Premoli, M., Pietropaolo, S., Wöhr, M., Simola, N., & Bonini, S. A. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15957 · Cited by 78 · see citing works
Yee, N., Schwarting, R. K. W., Fuchs, E., & Wöhr, M. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.05.010 · Cited by 71 · see citing works
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Self-citationGrimsley, J. M. S., Hazlett, E., & Wenstrup, J. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2205-13.2013 · Cited by 63 · see citing works
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Hernandez-Lallement, J., van Wingerden, M., Schäble, S., & Kalenscher, T. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.004 · Cited by 50 · see citing works
Dual functions of perirhinal cortex in fear conditioning
Kent, B. A., & Brown, T. H. (2012) · Hippocampus · doi:10.1002/hipo.22058 · Cited by 49 · see citing works
Self-citationThe incentive value of males’ 50-kHz ultrasonic vocalizations for female rats (Rattus norvegicus).
Snoeren, E. M. S., & Ågmo, A. (2013) · Journal of comparative psychology · doi:10.1037/a0033204 · Cited by 47 · see citing works
Demaestri, C., Brenhouse, H. C., & Honeycutt, J. A. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.12.005 · Cited by 42 · see citing works
Two distinct representations of social vocalizations in the basolateral amygdala
Gadziola, M. A., Shanbhag, S. J., & Wenstrup, J. J. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00953.2015 · Cited by 45 · see citing works
Current emotion research in behavioral neuroscience: the role(s) of the amygdala
Armony, J. L. (2013) · Emotion Review · doi:10.1177/1754073912457208 · Cited by 44 · see citing works
Social Origin of Vocal Communication in Rodents
Brudzyński, S. M. (2013) · Springer eBooks · doi:10.1007/978-94-007-7414-8_5 · Cited by 43 · see citing works
Wöhr, M., Engelhardt, K.-A., Seffer, D., Sungur, A. Ö., & Schwarting, R. K. W. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_410 · Cited by 40 · see citing works
An organization of visual and auditory fear conditioning in the lateral amygdala
Bergstrom, H. C., & Johnson, L. R. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.07.008 · Cited by 45 · see citing works
Affective communication in rodents
Wöhr, M., van Gaalen, M. M., & Schwarting, R. K. W. (2015) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000172 · Cited by 42 · see citing works
Expression of c-Fos in rat auditory and limbic systems following 22-kHz calls
Ouda, L., Jílek, M., & Syka, J. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.04.030 · Cited by 39 · see citing works
Laminar- and Target-Specific Amygdalar Inputs in Rat Primary Gustatory Cortex
Haley, M. S., Fontanini, A., & Maffei, A. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3224-15.2016 · Cited by 37 · see citing works
Female mice exhibit both sexual and social partner preferences for vocalizing males
Nomoto, K., IKUMI, M., OTSUKA, M., Asaba, A., Kato, M., Koshida, N., Mogi, K., & Kikusui, T. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12357 · Cited by 39 · see citing works
Dupin, M., Garcia, S., Boulanger-Bertolus, J., Buonviso, N., & Mouly, A. (2019) · eNeuro · doi:10.1523/eneuro.0065-19.2019 · Cited by 38 · see citing works
Brudzyński, S. M. (2013) · Journal of Molecular Neuroscience · doi:10.1007/s12031-013-0179-1 · Cited by 37 · see citing works
Lesions of the rat basolateral amygdala reduce the behavioral response to ultrasonic vocalizations
Schönfeld, L.-M., Zech, M.-P., Schäble, S., Wöhr, M., & Kalenscher, T. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112274 · Cited by 34 · see citing works
Processing of communication sounds: Contributions of learning, memory, and experience
Poremba, A., Bigelow, J., & Rossi, B. (2013) · Hearing Research · doi:10.1016/j.heares.2013.06.005 · Cited by 33 · see citing works
Studying Socio‐Affective Communication in Rats through Playback of Ultrasonic Vocalizations
Wöhr, M., Seffer, D., & Schwarting, R. K. W. (2016) · Current Protocols in Neuroscience · doi:10.1002/cpns.7 · Cited by 32 · see citing works
Selectivity and persistent firing responses to social vocalizations in the basolateral amygdala
Peterson, D. C., & Wenstrup, J. J. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.069 · Cited by 28 · see citing works
Wöhr, M., Willadsen, M., Kisko, T. M., Schwarting, R. K. W., & Fendt, M. (2019) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2019.109849 · Cited by 27 · see citing works
LTD at amygdalocortical synapses as a novel mechanism for hedonic learning
Haley, M. S., Bruno, S., Fontanini, A., & Maffei, A. (2020) · eLife · doi:10.7554/elife.55175 · Cited by 28 · see citing works
Bonauto, S. M., Greuel, O. M., & Honeycutt, J. A. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105396 · Cited by 24 · see citing works
Changes in acoustic startle reflex in rats induced by playback of 22-kHz calls
Inagaki, H., & Ushida, T. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.11.015 · Cited by 26 · see citing works
Bigelow, L. J., Pope, E., MacDonald, D. S., Rock, J. E., & Bernard, P. B. (2023) · Laboratory Animals · doi:10.1177/00236772221142687 · Cited by 24 · see citing works
A Social Reinforcement Learning Hypothesis of Mutual Reward Preferences in Rats
Hernandez-Lallement, J., van Wingerden, M., Schäble, S., & Kalenscher, T. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_436 · Cited by 23 · see citing works
Matsumoto, J., Nishimaru, H., Takamura, Y., Urakawa, S., Ono, T., & Nishijo, H. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00399 · Cited by 23 · see citing works
Response Calls Evoked by Playback of Natural 50-kHz Ultrasonic Vocalizations in Rats
Berz, A., Wöhr, M., & Schwarting, R. K. W. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.812142 · Cited by 22 · see citing works
Arias, N., Méndez, M., & Arias, J. L. (2015) · Hippocampus · doi:10.1002/hipo.22430 · Cited by 23 · see citing works
Towards an animal model of callousness
Hernandez-Lallement, J., van Wingerden, M., & Kalenscher, T. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.029 · Cited by 22 · see citing works
Rats concatenate 22 kHz and 50 kHz calls into a single utterance
Hernandez, C., Sabin, M., & Riede, T. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.151720 · Cited by 20 · see citing works
Inagaki, H., & Ushida, T. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113251 · Cited by 19 · see citing works
Seidisarouei, M., van Gurp, S., Pranic, N. M., Noguer‐Calabús, I., van Wingerden, M., & Tobias Kalenscher, A. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.693698 · Cited by 18 · see citing works
Joushi, S., Taherizadeh, Z., Esmaeilpour, K., & Sheibani, V. (2021) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2021.173318 · Cited by 18 · see citing works
Hearing, touching, and multisensory integration during mate choice
Lenschow, C., Mendes, A. R. P., & Lima, S. Q. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.943888 · Cited by 17 · see citing works
Rodent Vocalizations: Adaptations to Physical, Social, and Sexual Factors
Okanoya, K., & Screven, L. A. (2018) · Springer handbook of auditory research · doi:10.1007/978-3-319-92495-3_2 · Cited by 16 · see citing works
The Amygdala – A Hub of the Social Auditory Brain
Wenstrup, J. J., Ghasemahmad, Z., Hazlett, E., & Shanbhag, S. J. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24194-1 · Cited by 15 · see citing works
Vielle, C., Montanari, C., Pelloux, Y., & Baunez, C. (2021) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2021.2260 · Cited by 13 · see citing works
Revisiting the autoconditioning hypothesis for acquired reactivity to ultrasonic alarm calls
Calub, C. A., Furtak, S. C., & Brown, T. H. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.06.029 · Cited by 15 · see citing works
Self-citationDjerdjaj, A., Ng, A. J., Rieger, N. S., & Christianson, J. P. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114050 · Cited by 14 · see citing works
Social affective behaviors among female rats involve the basolateral amygdala and insular cortex
Djerdjaj, A., Rieger, N. S., Brady, B. H., Carey, B. N., Ng, A. J., & Christianson, J. P. (2023) · PLoS ONE · doi:10.1371/journal.pone.0281794 · Cited by 14 · see citing works
Fujii, T. G., Ikebuchi, M., & Okanoya, K. (2016) · Brain, Behavior and Evolution · doi:10.1159/000447233 · Cited by 12 · see citing works
Stressed rats fail to exhibit avoidance reactions to innately aversive social calls
Shukla, A., & Chattarji, S. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01230-z · Cited by 13 · see citing works
High-anxiety rats are less sensitive to the rewarding affects of amphetamine on 50kHz USV
Lehner, M., Taracha, E., Kaniuga, E., Wisłowska-Stanek, A., Wróbel, J., Sobolewska, A., Turzyńska, D., Skórzewska, A., & Płaźnik, A. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.011 · Cited by 13 · see citing works
Early-life seizures modify behavioral response to ultrasonic vocalization playback in adult rats
Bigelow, L. J., Fiset, C., Jarvis, J. H. M., MacLeod, S. J., Wöhr, M., Benke, T. A., & Bernard, P. B. (2021) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2021.108494 · Cited by 12 · see citing works
Bassi, G. S., de Carvalho, M. C., Almada, R. C., & Brandão, M. L. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.03.026 · Cited by 12 · see citing works
Playback of Ultrasonic Vocalizations to Juvenile and Adult Rats: Behavioral and Neuronal Effects
Schwarting, R. K. W., Kisko, T. M., & Wöhr, M. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00034-2 · Cited by 13 · see citing works
Kagawa, H., Seki, Y., & Okanoya, K. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.02.022 · Cited by 11 · see citing works
Kalenscher, T., Schönfeld, L.-M., Löbner, S., Wöhr, M., van Berkel, M., Zech, M.-P., & van Wingerden, M. (2021) · Language, cognition and mind · doi:10.1007/978-3-030-50200-3_19 · Cited by 11 · see citing works
Tonelli, L. C., Wöhr, M., Schwarting, R. K. W., & Melo-Thomas, L. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.03.013 · Cited by 10 · see citing works
Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats
Bigelow, L. J., Cohen, A. J., Pimm, R., Knight, J. B., & Bernard, P. B. (2022) · Journal of the American Association for Laboratory Animal Science · doi:10.30802/aalas-jaalas-21-000024 · Cited by 9 · see citing works
Bonauto, S. M., Patel, K. A., & Honeycutt, J. A. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.115326 · Cited by 7 · see citing works
Bianco, M. G., Pullano, S. A., Citraro, R., Russo, E., Sarro, G. D., de Villers‐Sidani, E., & Fiorillo, A. S. (2020) · Bioengineering · doi:10.3390/bioengineering7010023 · Cited by 8 · see citing works
Shahrier, M. A., & Wada, H. (2020) · NeuroToxicology · doi:10.1016/j.neuro.2020.03.016 · Cited by 7 · see citing works
Representation of conspecific vocalizations in amygdala of awake marmosets
Jia, G., Bai, S., Lin, Y., Wang, X., Zhu, L., Lyu, C., Sun, G., An, K., Roe, A. W., Li, X., et al. (2023) · National Science Review · doi:10.1093/nsr/nwad194 · Cited by 7 · see citing works
Biomimetic Sonar for Electrical Activation of the Auditory Pathway
Menniti, D., Pullano, S. A., Bianco, M. G., Citraro, R., Russo, E., Sarro, G. D., & Fiorillo, A. S. (2017) · Journal of Sensors · doi:10.1155/2017/2632178 · Cited by 7 · see citing works
O’Connell, K., Rhoads, S. A., & Marsh, A. A. (2024) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780197544754.013.25 · Cited by 5 · see citing works
Brincar na perspectiva psicoetológica: implicações para pesquisa e prática
Otta, E. (2017) · Psicologia USP · doi:10.1590/0103-656420160122 · Cited by 7 · see citing works
Bartsoen, E., & Wöhr, M. (2023) · Physiology & Behavior · doi:10.1016/j.physbeh.2023.114290 · Cited by 5 · see citing works
Reflections on a footnote: implications for the study of emotions in animals
Otta, E. (2015) · Psicologia USP · doi:10.1590/0103-656420140079 · Cited by 4 · see citing works
Freeman, A. R., Hare, J. F., & Caldwell, H. K. (2020) · Brain and Behavior · doi:10.1002/brb3.1629 · Cited by 4 · see citing works
Packheiser, J., Soyman, E., Paradiso, E., Michon, F., Ramaaker, E., Sahin, N., Muralidharan, S., Wöhr, M., Gazzola, V., & Keysers, C. (2023) · Communications Biology · doi:10.1038/s42003-023-05474-x · Cited by 4 · see citing works
Limbic-System Involvement in Rat Ultrasonic Communications
Furtak, S. C., & Brown, T. H. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00009-3 · Cited by 4 · see citing works
Self-citationEvaluation of auditory cortex tonotopical organization in rats Through Principal Component Analysis
Bianco, M. G., Pullano, S. A., Menniti, D., Fiorillo, A. S., & de Villers‐Sidani, E. (2017) · IEEE International Symposium on Medical Measurements and Applications (MeMeA) · doi:10.1109/memea.2017.7985879 · Cited by 4 · see citing works
The Concept of Ethotransmission: Rapid Emotional Communication
Brudzyński, S. M. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00010-x · Cited by 4 · see citing works
“Neural correlates of social signaling in rodents: An acoustic perspective”
Grijseels, D. M., Lemazina, A., López‐Jury, L., & Barker, A. J. (2024) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2024.102927 · Cited by 3 · see citing works
Development and heterogeneity of rat 22 kHz vocalizations
Brudzyński, S. M. (2025) · Behavioural Brain Research · doi:10.1016/j.bbr.2025.115822 · Cited by 4 · see citing works
Oliveira, P., Daniel, A. N., Nunes, P. T., Costa, K. A., Yehia, H. C., & Ribeiro, Â. M. (2015) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2015.52003 · Cited by 3 · see citing works
Voytenko, S. V., Shanbhag, S. J., Wenstrup, J. J., & Galazyuk, A. V. (2023) · Journal of Neurophysiology · doi:10.1152/jn.00103.2023 · Cited by 3 · see citing works
Nesterova, Y. V., Vsyakikh, O. V., Валерьевич, К. П., Поветьева, Т. Н., Zyuz’kov, G. N., Иннокентьевич, С. Н., Вадимович, Ж. В., & Losev, E. A. (2024) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-024-06242-5 · Cited by 3 · see citing works
Evidence for a vocal signature in the rat and its reinforcing effectsPreprint
Vielle, C., Montanari, C., Pelloux, Y., & Baunez, C. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.07.447373 · Cited by 3 · see citing works
Effects of Physical Stress and Pain on Emission of Ultrasonic Vocalizations and Social Interactions
Drugan, R. C., & Stafford, N. P. (2018) · Handbook of behavioral neuroscience · doi:10.1016/b978-0-12-809600-0.00033-0 · Cited by 2 · see citing works
Neural mechanisms underlying orofacial prosocial behavior in rodents
Wang, J., Huang, M., Ni, Z., Zhi, Z., & Cao, P. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106572 · Cited by 1 · see citing works
Packheiser, J., Soyman, E., Paradiso, E., Ramaaker, E., Sahin, N., Muralidharan, S., Wöhr, M., Gazzola, V., & Keysers, C. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.27.497737 · Cited by 1 · see citing works
Bonauto, S. M., Greuel, O. M., & Honeycutt, J. A. (2022) · doi:10.31234/osf.io/e5sm7 · Cited by 1 · see citing works
What is Cognition? An evolutionary perspectivePreprint
Faghani, V., Sahraee, M., Sarkesh, F., & Katouzian, A.-R. (2024) · doi:10.22541/au.170665387.79875499/v1 · Cited by 1 · see citing works
PhasicDopamineReleaseintheNucleusAccumbensin ResponsetoPro-Social50kHzUltrasonicVocalizationsin Rats
Wanat, M. J., Hart, A. S., Hollon, N. G., Phillips, M. E., & Schwarting, W. (2014)
- Authors
- Parsana, A. J., Li, N., & Brown, T. H.
- Affiliations
- Yale University (US)
- Corresponding author
- Brown, Thomas H.
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2012-01
- Volume
- 226
- Issue
- 1
- Pages
- 77-86
- ISSN
- 0166-4328 (ISSN-L)
- PMC
- PMC3197767
- OpenAlex
- W2150062107
- Cited by
- 108
- References
- 78
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 5 · 2023: 9 · 2022: 7 · 2021: 8 · 2020: 8 · 2019: 4 · 2018: 10 · 2017: 8 · 2016: 12 · 2015: 7 · 2014: 6 · 2013: 10 · 2012: 8
- FWCI
- 3.90
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH058405)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
- Keywords
- ultrasonic vocalizations, social signals, amygdala, single-unit responses, emotional valence, freezing behavior, fear, auditory processing, rats
- MeSH terms
- Acoustic Stimulation, Amygdala, Animals, Behavior, Animal, Fear, Male, Neurons, Social Behavior, Vocalization, Animal, Rats, Sprague-Dawley, Freezing Reaction, Cataleptic, Rats
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