Decreased approach behavior and nucleus accumbens immediate early gene expression in response to Parkinsonian ultrasonic vocalizations in rats

References

• Aragona, B. J., Liu, Y., Curtis, J. T., Stephan, F. K., & Wang, Z. (2003). A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles. The Journal of Neuroscience, 23(8), 3483–3490.
   PubMed Web of Science ®Google Scholar
• Aragona, B. J., Liu, Y., Yu, Y. J., Curtis, J. T., Detwiler, J. M., Insel, T. R., & Wang, Z. (2006). Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds. Nature Neuroscience, 9(1), 133–139. doi:10.1038/nn1613
   PubMed Web of Science ®Google Scholar
• Arriaga, G., Zhou, E. P., & Jarvis, E. D. (2012). Of mice, birds, and men: The mouse ultrasonic song system has some features similar to humans and song-learning birds. PLoS One, 7(10), e46610. doi:10.1371/journal.pone.0046610
   PubMedGoogle Scholar
• Barfield, R. J., Auerbach, P., Geyer, L. A., & Mcintosh, T. K. (1979). Ultrasonic vocalizations in rat sexual-behavior. American Zoologist, 19(2), 469–480. doi:10.1093/icb/19.2.469
   Google Scholar
• Becker, J. B., Rudick, C. N., & Jenkins, W. J. (2001). The role of dopamine in the nucleus accumbens and striatum during sexual behavior in the female rat. The Journal of Neuroscience, 21(9), 3236–3241.
   PubMed Web of Science ®Google Scholar
• Bezard, E., & Przedborski, S. (2011). A tale on animal models of Parkinson’s disease. Movement Disorders, 26(6), 993–1002. doi:10.1002/mds.23696
   PubMed Web of Science ®Google Scholar
• Bialy, M., Rydz, M., & Kaczmarek, L. (2000). Precontact 50-kHz vocalizations in male rats during acquisition of sexual experience. Behavioral Neuroscience, 114(5), 983–990. doi:10.1037/0735-7044.114.5.983
   PubMed Web of Science ®Google Scholar
• Bonifati, V., Rohe, C. F., Breedveld, G. J., Fabrizio, E., De Mari, M., Tassorelli, C., … Italian Parkinson Genetics Network. (2005). Early-onset parkinsonism associated with PINK1 mutations: Frequency, genotypes, and phenotypes. Neurology, 65(1), 87–95.
   PubMed Web of Science ®Google Scholar
• Brudzynski, S. M. (2009). Communication of adult rats by ultrasonic vocalization: Biological, sociobiological, and neuroscience approaches. ILAR Journal, 50(1), 43–50. doi:10.1093/ilar.50.1.43
   PubMed Web of Science ®Google Scholar
• Brudzynski, S. M., & Pniak, A. (2002). Social contacts and production of 50-kHz short ultrasonic calls in adult rats. Journal of Comparative Psychology, 116(1), 73–82. doi:10.1037/0735-7036.116.1.73
   PubMed Web of Science ®Google Scholar
• Burgdorf, J., Kroes, R. A., Moskal, J. R., Pfaus, J. G., Brudzynski, S. M., & Panksepp, J. (2008). Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self-administration of playback. Journal of Comparative Psychology, 122(4), 357–367. doi:10.1037/a0012889
   PubMed Web of Science ®Google Scholar
• Cenci, M. A., Whishaw, I. Q., & Schallert, T. (2002). Opinion: Animal models of neurological deficits: How relevant is the rat? Nature Reviews Neuroscience, 3(7), 574–579. doi:10.1038/nrn877
   PubMed Web of Science ®Google Scholar
• Chabout, J., Sarkar, A., Dunson, D. B., & Jarvis, E. D. (2015). Male mice song syntax depends on social contexts and influences female preferences. Frontiers in Behavioral Neuroscience, 9, 76. doi:10.3389/fnbeh.2015.00076
   PubMed Web of Science ®Google Scholar
• Chesselet, M.-F., & Richter, F. (2011). Modelling of Parkinson’s disease in mice. The Lancet Neurology, 10(12), 1108–1118. doi:10.1016/S1474-4422(11)70227-7
   PubMed Web of Science ®Google Scholar
• Ciucci, M. R., Ahrens, A. M., Ma, S. T., Kane, J. R., Windham, E. B., Woodlee, M. T., & Schallert, T. (2009). Reduction of dopamine synaptic activity: Degradation of 50-kHz ultrasonic vocalization in rats. Behavioral Neuroscience, 123(2), 328–336. doi:10.1037/a0014593
   PubMed Web of Science ®Google Scholar
• Ciucci, M. R., Ma, S. T., Fox, C., Kane, J. R., Ramig, L. O., & Schallert, T. (2007). Qualitative changes in ultrasonic vocalization in rats after unilateral dopamine depletion or haloperidol: A preliminary study. Behavioural Brain Research, 182(2), 284–289. doi:10.1016/j.bbr.2007.02.020
   PubMed Web of Science ®Google Scholar
• Ciucci, M. R., Ma, S. T., Kane, J. R., Ahrens, A. M., & Schallert, T. (2008). Limb use and complex ultrasonic vocalization in a rat model of Parkinson’s disease: Deficit-targeted training. Parkinsonism & Related Disorders, 14(Suppl 2), S172–175. doi:10.1016/j.parkreldis.2008.04.027
   Google Scholar
• Ciucci, M. R., Vinney, L., Wahoske, E. J., & Connor, N. P. (2010). A translational approach to vocalization deficits and neural recovery after behavioral treatment in Parkinson disease. Journal of Communication Disorders, 43(4), 319–326. doi:10.1016/j.jcomdis.2010.04.004
   PubMed Web of Science ®Google Scholar
• Coffey, K. R., Barker, D. J., Ma, S., Root, D. H., Martinez, L., Horvitz, J. C., & West, M. O. (2013). Effects of varying reinforcement probability on pavlovian approach behavior and ultrasonic vocalizations in rats. Behavioural Brain Research, 237, 256–262. doi:10.1016/j.bbr.2012.09.041
   PubMed Web of Science ®Google Scholar
• Dave, K. D., De Silva, S., Sheth, N. P., Ramboz, S., Beck, M. J., Quang, C., … Frasier, M. A. (2014). Phenotypic characterization of recessive gene knockout rat models of Parkinson’s disease. Neurobiology of Disease, 70, 190–203. doi:10.1016/j.nbd.2014.06.009
   PubMed Web of Science ®Google Scholar
• Dizinno, G., & Whitney, G. (1977). Androgen influence on male mouse ultrasounds during courtship. Hormones and Behavior, 8(2), 188–192. doi:10.1016/0018-506X(77)90035-6
   PubMed Web of Science ®Google Scholar
• Duffy, J. R. (2006). Apraxia of speech in degenerative neurologic disease. Aphasiology, 20(6), 511–527. doi:10.1080/02687030600597358
   Web of Science ®Google Scholar
• Edwards, D. A., & Einhorn, L. C. (1986). Preoptic and midbrain control of sexual motivation. Physiology & Behavior, 37(2), 329–335. doi:10.1016/0031-9384(86)90242-8
   PubMed Web of Science ®Google Scholar
• Ellis, J. M., & Riters, L.V. (2013). Patterns of FOS protein induction in singing female starlings. Behavioral Brain Research, 237, 148–156. doi:10.1016/j.bbbr.2012.09.004
   PubMed Web of Science ®Google Scholar
• Everitt, B. J. (1990). Sexual motivation: A neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neuroscience & Biobehavioral Reviews, 14(2), 217–232. doi:10.1016/S0149-7634(05)80222-2
   PubMed Web of Science ®Google Scholar
• Floresco, S. B., & Ghods-Sharifi, S. (2006). Amygdala-prefrontal cortical circuitry regulates effort-based decision making. Cerebral Cortex, 17(2), 251–260. doi:10.1093/cercor/bhj143
   PubMed Web of Science ®Google Scholar
• Fox, C. M., Ramig, L. O., Ciucci, M. R., Sapir, S., McFarland, D. H., & Farley, B. G. (2006). The science and practice of LSVT/LOUD: Neural plasticity-principled approach to treating individuals with Parkinson disease and other neurological disorders. Seminars in Speech and Language, 27(4), 283–299. doi:10.1055/s-2006-955118
   PubMedGoogle Scholar
• Gingrich, B., Liu, Y., Cascio, C., Wang, Z., & Insel, T. R. (2000). Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster). Behavioral Neuroscience, 114(1), 173–183. doi:10.1037/0735-7044.114.1.173
   PubMed Web of Science ®Google Scholar
• Goberman, A. M., & Blomgren, M. (2008). Fundamental frequency change during offset and onset of voicing in individuals with Parkinson disease. Journal of Voice, 22(2), 178–191. doi:10.1016/j.jvoice.2006.07.006
   PubMed Web of Science ®Google Scholar
• Gombash, S. E., Manfredsson, F. P., Kemp, C. J., Kuhn, N. C., Fleming, S. M., Egan, A. E., … Sortwell, C. E. (2013). Morphological and behavioral impact of AAV2/5-mediated overexpression of human wildtype alpha-synuclein in the rat nigrostriatal system. PLoS One, 8(11), e81426. doi:10.1371/journal.pone.0081426
   Google Scholar
• Gombash, S. E., Manfredsson, F. P., Mandel, R. J., Collier, T. J., Fischer, D. L., Kemp, C. J., … Sortwell, C. E. (2014). Neuroprotective potential of pleiotrophin overexpression in the striatonigral pathway compared with overexpression in both the striatonigral and nigrostriatal pathways. Gene Therapy, 21(7), 682–693. doi:10.1038/gt.2014.42
   PubMed Web of Science ®Google Scholar
• Goto, Y., & Grace, A. A. (2005). Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nature Neuroscience, 8(6), 805–812. doi:10.1038/nn1471
   PubMed Web of Science ®Google Scholar
• Grant, L. M., Kelm-Nelson, C. A., Hilby, B. L., Blue, K. V., Rajamanickam, E. S., Pultorak, J. D., … Ciucci, M. R. (2015). Evidence for early and progressive ultrasonic vocalization and oromotor deficits in a PINK1 gene knockout rat model of Parkinson’s disease. Journal of Neuroscience Research. Advance online publication. doi:10.1002/jnr.23625
   Google Scholar
• Grant, L. M., Richter, F., Miller, J. E., White, S. A., Fox, C. M., Zhu, C., … Ciucci, M. R. (2014). Vocalization deficits in mice over-expressing alpha-synuclein, a model of pre-manifest Parkinson’s disease. Behavioral Neuroscience, 128(2), 110–121. doi:10.1037/a0035965
   PubMed Web of Science ®Google Scholar
• Hammerschmidt, K., Radyushkin, K., Ehrenreich, H., & Fischer, J. (2009). Female mice respond to male ultrasonic ‘songs’ with approach behaviour. Biology Letters, 5(5), 589–592. doi:10.1098/rsbl.2009.0317
   PubMed Web of Science ®Google Scholar
• Harel, B., Cannizzaro, M., & Snyder, P. J. (2004). Variability in fundamental frequency during speech in prodromal and incipient Parkinson’s disease: A longitudinal case study. Brain and Cognition, 56(1), 24–29. doi:10.1016/j.bandc.2004.05.002
   PubMed Web of Science ®Google Scholar
• Ho, A. K., Iansek, R., Marigliani, C., Bradshaw, J. L., & Gates, S. (1999). Speech impairment in a large sample of patients with Parkinson’s disease. Behavioural Neurology, 11(3), 131–137. doi:10.1155/1999/327643
   PubMed Web of Science ®Google Scholar
• Holmes, R. J., Oates, J. M., Phyland, D. J., & Hughes, A. J. (2000). Voice characteristics in the progression of Parkinson’s disease. International Journal of Language & Communication Disorders, 35(3), 407–418. doi:10.1080/136828200410654
   PubMed Web of Science ®Google Scholar
• Holy, T. E., & Guo, Z. (2005). Ultrasonic songs of male mice. PLoS Biology, 3(12), e386. doi:10.1371/journal.pbio.0030386
   PubMed Web of Science ®Google Scholar
• Jennions, M. D., & Moller, A. P. (2003). A survey of the statistical power of research in behavioral ecology and animal behavior. Behavioral Ecology, 14(3), 438–445. doi:10.1093/beheco/14.3.438
   Web of Science ®Google Scholar
• Johnson, A. M., Doll, E. J., Grant, L. M., Ringel, L., Shier, J. N., & Ciucci, M. R. (2011). Targeted training of ultrasonic vocalizations in aged and Parkinsonian rats. Journal of Visualized Experiments, 54, e2835. doi:10.3791/2835
   Google Scholar
• Johnson, A. M., Grant, L. M., Schallert, T., & Ciucci, M. R. (2015). Changes in rat 50-kHz ultrasonic vocalizations during dopamine denervation and aging: Relevance to neurodegeneration. Current Neuropharmacology, 13(2), 211–219. doi:10.2174/1570159X1302150525122416
   PubMed Web of Science ®Google Scholar
• Karlsen, K. H., Tandberg, E., Arsland, D., & Larsen, J. P. (2000). Health related quality of life in Parkinson’s disease: A prospective longitudinal study. Journal of Neurology, Neurosurgery & Psychiatry, 69(5), 584–589. doi:10.1136/jnnp.69.5.584
   PubMed Web of Science ®Google Scholar
• Kawajiri, S., Saiki, S., Sato, S., & Hattori, N. (2011). Genetic mutations and functions of PINK1. Trends in Pharmacological Sciences, 32(10), 573–580. doi:10.1016/j.tips.2011.06.001
   PubMed Web of Science ®Google Scholar
• Kim, Y., Kent, R. D., & Weismer, G. (2011). An acoustic study of the relationships among neurologic disease, dysarthria type, and severity of dysarthria. Journal of Speech Language and Hearing Research, 54(2), 417–429. doi:10.1044/1092-4388(2010/10-0020)
   PubMed Web of Science ®Google Scholar
• Knutson, B., Burgdorf, J., & Panksepp, J. (1998). Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. Journal of Comparative Psychology, 112(1), 65–73. doi:10.1037/0735-7036.112.1.65
   PubMed Web of Science ®Google Scholar
• Kroodsma, D. E. (1989). Suggested experimental-designs for song playbacks. Animal Behaviour, 37, 600–609. doi:10.1016/0003-3472(89)90039-0
   Web of Science ®Google Scholar
• Larson, C. R. (1985). The midbrain periaqueductal gray: A brainstem structure involved in vocalization. Journal of Speech and Hearing Research, 28(2), 241–249. doi:10.1044/jshr.2802.241
   PubMedGoogle Scholar
• Larson, C. R., & Kistler, M. K. (1986). The relationship of periaqueductal gray neurons to vocalization and laryngeal EMG in the behaving monkey. Experimental Brain Research, 63(3), 596–606. doi:10.1007/bf00237482
   PubMed Web of Science ®Google Scholar
• Logemann, J. A., Fisher, H. B., Boshes, B., & Blonsky, E. R. (1978). Frequency and cooccurrence of vocal tract dysfunctions in the speech of a large sample of Parkinson patients. The Journal of Speech and Hearing Disorders, 43(1), 47–57. doi:10.1044/jshd.4301.47
   PubMedGoogle Scholar
• Mas, M., Gonzalez-Mora, J. L., Louilot, A., Solé, C., & Guadalupe, T. (1990). Increased dopamine release in the nucleus accumbens of copulating male rats as evidenced by in vivo voltammetry. Neuroscience Letters, 110(3), 303–308. doi:10.1016/0304-3940(90)90864-6
   PubMed Web of Science ®Google Scholar
• McGinnis, M. Y., & Vakulenko, M. (2003). Characterization of 50-kHz ultrasonic vocalizations in male and female rats. Physiology & Behavior, 80(1), 81–88. doi:10.1016/S0031-9384(03)00227-0
   PubMed Web of Science ®Google Scholar
• Mogenson, G. J., Jones, D. L., & Yim, C. Y. (1980). From motivation to action: Functional interface between the limbic system and the motor system. Progress in Neurobiology, 14(2–3), 69–97. doi:10.1016/0301-0082(80)90018-0
   PubMed Web of Science ®Google Scholar
• Musolf, K., Hoffmann, F., & Penn, D. J. (2010). Ultrasonic courtship vocalizations in wild house mice, Mus musculus musculus. Animal Behaviour, 79(3), 757–764. doi:10.1016/j.anbehav.2009.12.034
   Web of Science ®Google Scholar
• Nakagawa, S. (2004). A farewell to Bonferroni: The problems of low statistical power and publication bias. Behavioral Ecology, 15(6), 1044–1045. doi:10.1093/beheco/arh107
   Web of Science ®Google Scholar
• Narayana, S., Jacks, A., Robin, D. A., Poizner, H., Zhang, W., Franklin, C., … Fox, P. T. (2009). A noninvasive imaging approach to understanding speech changes following deep brain stimulation in Parkinson’s disease. American Journal of Speech-Language Pathology, 18(2), 146–161. doi:10.1044/1058-0360(2008/08-0004)
   PubMed Web of Science ®Google Scholar
• Paxinos, G., & Watson, G. (2005). The rat brain in stereotaxic coordinates (5th ed.). Burlington, MA: Elsevier.
   Google Scholar
• Pfaus, J. G., Damsma, G., Nomikos, G. G., Wenkstern, D. G., Blaha, C. D., Phillips, A. G., & Fibiger, H. C. (1990). Sexual behavior enhances central dopamine transmission in the male rat. Brain Research, 530(2), 345–348. doi:10.1016/0006-8993(90)91309-5
   PubMed Web of Science ®Google Scholar
• Pfaus, J. G., Damsma, G., Wenkstern, D., & Fibiger, H. C. (1995). Sexual activity increases dopamine transmission in the nucleus accumbens and striatum of female rats. Brain Research, 693(1–2), 21–30. doi:10.1016/0006-8993(95)00679-K
   PubMed Web of Science ®Google Scholar
• Pomerantz, S. M., Nunez, A. A., & Bean, N. J. (1983). Female behavior is affected by male ultrasonic vocalizations in house mice. Physiology & Behavior, 31(1), 91–96. doi:10.1016/0031-9384(83)90101-4
   PubMed Web of Science ®Google Scholar
• R-Core-Team. (2014). R: A language and environment for statistical computing (3.1.2). Vienna: Austria R Foundation for Statistical Computing. Retrieved from http://www.R-project.org
   Google Scholar
• Riede, T. (2011). Subglottal pressure, tracheal airflow, and intrinsic laryngeal muscle activity during rat ultrasound vocalization. Journal of Neurophysiology, 106(5), 2580–2592. doi:10.1152/jn.00478.2011
   PubMed Web of Science ®Google Scholar
• Ringel, L. E., Basken, J. N., Grant, L. M., & Ciucci, M. R. (2013). Dopamine D1 and D2 receptor antagonism effects on rat ultrasonic vocalizations. Behavioural Brain Research, 252, 252–259. doi:10.1016/j.bbr.2013.06.006
   PubMed Web of Science ®Google Scholar
• Robbins, T. W., & Everitt, B. J. (1982). Functional studies of the central catecholamines. In R. S. John & J. B. Ronald (Eds.), International Review of Neurobiology (Vol. 23, pp. 303–365). San Diego, CA: Academic Press.
   Google Scholar
• Roger, M., & Arnault, P. (1989). Anatomical study of the connections of the primary auditory area in the rat. The Journal of Comparative Neurology, 287(3), 339–356. doi:10.1002/cne.902870306
   PubMed Web of Science ®Google Scholar
• Sadananda, M., Wöhr, M., & Schwarting, R. K. W. (2008). Playback of 22-kHz and 50-kHz ultrasonic vocalizations induces differential c-Fos expression in rat brain. Neuroscience Letters, 435(1), 17–23. doi:10.1016/j.neulet.2008.02.002
   PubMed Web of Science ®Google Scholar
• Sales, G. D. (1991). The effect of 22 kHz calls and artificial 38 kHz signals on activity in rats. Behavioural Processes, 24(2), 83–93. doi:10.1016/0376-6357(91)90001-G
   PubMed Web of Science ®Google Scholar
• Sapir, S. (2014). Multiple factors are involved in the dysarthria associated with Parkinson’s disease: A review with implications for clinical practice and research. Journal of Speech, Language, and Hearing Research, 57(4), 1330–1343. doi:10.1044/2014_JSLHR-S-13-0039
   PubMed Web of Science ®Google Scholar
• Seffer, D., Schwarting, R. K. W., & Wöhr, M. (2014). Pro-social ultrasonic communication in rats: Insights from playback studies. Journal of Neuroscience Methods, 234(2014), 73–81. doi:10.1016/j.jneumeth.2014.01.023
   PubMed Web of Science ®Google Scholar
• Sewell, G. D. S. (2009). Ultrasound and mating behaviour in rodents with some observations on other behavioural situations. Journal of Zoology, 168(2), 149–164. doi:10.1111/j.1469-7998.1972.tb01345.x
   Google Scholar
• Snoeren, E. M. S., & Ågmo, A. (2013). Female ultrasonic vocalizations have no incentive value for male rats. Behavioral Neuroscience, 127(3), 439–450. doi:10.1037/a0032027
   PubMed Web of Science ®Google Scholar
• Snoeren, E. M. S., & Ågmo, A. (2014). The incentive value of males’ 50-kHz ultrasonic vocalizations for female rats (Rattus norvegicus). Journal of Comparative Psychology, 128(1), 40–55. doi:10.1037/a0033204
   PubMed Web of Science ®Google Scholar
• Stewart, C., Winfield, L., Hunt, A., Bressman, S. B., Fahn, S., Blitzer, A., & Brin, M. F. (1995). Speech dysfunction in early Parkinson’s disease. Movement Disorders, 10(5), 562–565. doi:10.1002/mds.870100506
   PubMed Web of Science ®Google Scholar
• Tan, E.-K., Yew, K., Chua, E., Puvan, K., Shen, H., Lee, E., … Tan, L. (2006). PINK1 mutations in sporadic early-onset Parkinson’s disease. Movement Disorders, 21(6), 789–793. doi:10.1002/mds.20810
   PubMed Web of Science ®Google Scholar
• Tramontin, A. D., Smith, G. T., Breuner, C. W., & Brenowitz, E. A. (1998). Seasonal plasticity and sexual dimorphism in the avian song control system: Stereological measurement of neuron density and number. The Journal of Comparative Neurology, 396(2), 186–192. doi:10.1002/(ISSN)1096-9861
   PubMed Web of Science ®Google Scholar
• Valente, E. M., Abou-Sleiman, P. M., Caputo, V., Muqit, M. M., Harvey, K., Gispert, S., & Wood, N. W. (2004). Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science, 304(5674), 1158–1160. doi:10.1126/science.1096284
   PubMed Web of Science ®Google Scholar
• Wan, H., Warburton, E. C., Kusmierek, P., Aggleton, J. P., Kowalska, D. M., & Brown, M. W. (2001). Fos imaging reveals differential neuronal activation of areas of rat temporal cortex by novel and familiar sounds. The European Journal of Neuroscience, 14(1), 118–124. doi:10.1046/j.0953-816x.2001.01625.x
   PubMed Web of Science ®Google Scholar
• Willadsen, M., Seffer, D., Schwarting, R. K. W., & Wöhr, M. (2014). Rodent ultrasonic communication: Male prosocial 50-kHz ultrasonic vocalizations elicit social approach behavior in female rats (Rattus norvegicus). Journal of Comparative Psychology, 128(1), 56–64. doi:10.1037/a0034778
   PubMed Web of Science ®Google Scholar
• Willuhn, I., Tose, A., Wanat, M. J., Hart, A. S., Hollon, N. G., Phillips, P. E., … Wohr, M. (2014). Phasic dopamine release in the nucleus accumbens in response to pro-social 50 kHz ultrasonic vocalizations in rats. Journal of Neuroscience, 34(32), 10616–10623. doi:10.1523/JNEUROSCI.1060-14.2014
   PubMed Web of Science ®Google Scholar
• Wöhr, M., Houx, B., Schwarting, R. K. W., & Spruijt, B. (2008). Effects of experience and context on 50-kHz vocalizations in rats. Physiology & Behavior, 93(4–5), 766–776. doi:10.1016/j.physbeh.2007.11.031
   PubMed Web of Science ®Google Scholar
• Wöhr, M., & Schwarting, R. K. W. (2007). Ultrasonic communication in rats: Can playback of 50-kHz calls induce approach behavior? PLoS One, 2(12), e1365. doi:10.1371/journal.pone.0001365
   PubMed Web of Science ®Google Scholar
• Wöhr, M., & Schwarting, R. K. W. (2012). Testing social acoustic memory in rats: Effects of stimulus configuration and long-term memory on the induction of social approach behavior by appetitive 50-kHz ultrasonic vocalizations. Neurobiology of Learning and Memory, 98(2), 154–164. doi:10.1016/j.nlm.2012.05.004
   PubMed Web of Science ®Google Scholar
• Wöhr, M., & Schwarting, R. K. W. (2013). Affective communication in rodents: Ultrasonic vocalizations as a tool for research on emotion and motivation. Cell and Tissue Research, 354(1), 81–97. doi:10.1007/s00441-013-1607-9
   PubMed Web of Science ®Google Scholar
• Wright, J. M., Dobosiewicz, M. R. S., & Clarke, P. B. S. (2013). The role of dopaminergic transmission through D1-like and D2-like receptors in amphetamine-induced rat ultrasonic vocalizations. Psychopharmacology (Berl), 225(4), 853–868. doi:10.1007/s00213-012-2871-1
   PubMed Web of Science ®Google Scholar
• Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001). Cellular mechanisms of social attachment. Hormones and Behavior, 40(2), 133–138. doi:10.1006/hbeh.2001.1691
   PubMed Web of Science ®Google Scholar
• Young, L. J., & Wang, Z. (2004). The neurobiology of pair bonding. Nature Neuroscience, 7(10), 1048–1054. doi:10.1038/nn1327
   PubMed Web of Science ®Google Scholar