Rodent ultrasonic vocalizations are bound to active sniffing behavior

Frontiers in Behavioral Neuroscience

Volumn 8, Issue NOV, 2014, Pages

  Sirotin, Yevgeniy B ^a   Costa, Martín Elias ^b   Laplagne, Diego A ^a,c  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

Author keywords

Mouse; Orofacial; Rat; Respiration; Rhythm; Speech breathing; Theta; Ultrasonic vocalizations

Indexed keywords

ADULT; ANIMAL EXPERIMENT; BREATHING PATTERN; CHEMICAL BINDING; EXHALATION; HAPLORHINI; HUMAN VERSUS ANIMAL COMPARISON; MOUSE; NONHUMAN; RAT; RHYTHM; RODENT; SNIFFING; ULTRASOUND; VOCALIZATION;

EID: 84979894025     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00399     Document Type: Article

References (55)

1. Andalman, A. S., Foerster, J. N., and Fee, M. S. (2011). Control of vocal and respi­ratory patterns in birdsong: dissection of forebrain and brainstem mechanisms using temperature. PLoS ONE 6:e25461. doi: 10.1371/journal.pone.0025461
2. Assini, R., Sirotin, Y. B., and Laplagne, D. A. (2013). Rapid triggering of vocalizations following social interactions. Curr. Biol. 23, R996-R997. doi: 10.1016/j.cub.2013.10.007
3. Brudzynski, S. M. (2007). Ultrasonic calls of rats as indicator variables of nega­tive or positive states: acetylcholine-dopamine interaction and acoustic coding. Behav. Brain Res. 182, 261-273. doi: 10.1016/j.bbr.2007.03.004
4. Brudzynski, S. M. (2009). Communication of adult rats byultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J. 50, 43-50. doi: 10.1093/ilar.50.1.43
5. Brudzynski, S. M. (2013). Ethotransmission: communication of emotional states through ultrasonic vocalization in rats. Curr. Opin. Neurobiol. 23, 310-317. doi: 10.1016/j.conb.2013.01.014
6. Brudzynski, S. M., and Pniak, A. (2002). Social contacts and production of 50-kHz short ultrasonic calls in adult rats. J. Comp. Psychol. 116, 73-82. doi: 10.1037/0735-7036.116.1.73
7. Chandrasekaran, C., Trubanova, A., Stillittano, S., Caplier, A., and Ghazanfar, A. A. (2009). The natural statistics of audiovisual speech. PLoS Comput. Biol. 5:e1000436. doi: 10.1371/journal.pcbi.1000436
8. Costall, B., and Naylor, R. J. (1975). The behavioural effects of dopamine applied intracerebrally to areas of the mesolimbic system. Eur. J. Pharmacol. 32, 87-92.
9. Cury, K. M., and Uchida, N. (2010). Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570-585. doi: 10.1016/j.neuron.2010.09.040
10. Deschenes, M., Moore, J., and Kleinfeld, D. (2012). Sniffing and whisking in rodents. Curr. Opin. Neurobiol. 22, 243-250. doi: 10.1016/j.conb.2011.11.013
11. Ganguly, K., and Kleinfeld, D. (2004). Goal-directed whisking increases phase-locking between vibrissa movement and electrical activity in primary sen­sory cortex in rat. Proc. Natl. Acad. Sci. U.S.A. 101, 12348-12353. doi: 10.1073/pnas.0308470101
12. Ghazanfar, A., Chandrasekaran, C., and Morrill, R. J. (2010). Dynamic, rhythmic facial expressions and the superior temporal sulcus of macaque monkeys: impli­cations for the evolution of audiovisual speech. Eur. J. Neurosci. 31, 1807-1817. doi: 10.1111/j.1460-9568.2010.07209.x
13. Ghazanfar, A., Morrill, R. J., and Kayser, C. (2013). Monkeys are perceptually tuned to facial expressions that exhibit a theta-like speech rhythm. Proc. Natl. Acad. Sci. U.S.A. 110, 1959-1963. doi: 10.1073/pnas.1214956110
14. Ghitza, O., and Greenberg, S. (2009). On the possible role of brain rhythms in speech perception: intelligibility of time-compressed speech with periodic and aperiodic insertions of silence. Phonetica 66, 113-126. doi: 10.1159/000208934
15. Giraud, A.-L., and Poeppel, D. (2012). Cortical oscillations and speech processing: emerging computational principles and operations. Nat. Neurosci. 15, 511-517. doi: 10.1038/nn.3063
16. Grosmaitre, X., Santarelli, L. C., Tan, J., Luo, M., and Ma, M. (2007). Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat. Neurosci. 10, 348-354. doi: 10.1038/nn1856
17. Hegoburu, C., Shionoya, K., Garcia, S., Messaoudi, B., Thévenet, M., and Mouly, A.-M. (2011). The RUB cage: respiration-ultrasonic vocalizations-behavior acquisition setup for assessing emotional memory in rats. Front. Behav. Neurosci. 5:25. doi: 10.3389/fnbeh.2011.00025
18. Holy, T. E., and Guo, Z. (2005). Ultrasonic songs of male mice. PLoS Biol. 3:e386. doi: 10.1371/journal.pbio.0030386
19. Kay, L. M. (2005). Theta oscillations and sensorimotor performance. Proc. Natl. Acad. Sci. U.S.A. 102, 3863. doi: 10.1073/pnas.0407920102
20. Kepecs, A., Uchida, N., and Mainen, Z. F. (2006). The sniff as a unit of olfactory processing. Chem. Senses 31, 167-179. doi: 10.1093/chemse/bjj016
21. Kilgard, M. P., and Merzenich, M. M. (1998). Plasticity of temporal informa­tion processing in the primary auditory cortex. Nat. Neurosci. 1, 727-731. doi: 10.1038/3729
22. Kim, H., and Bao, S. (2009). Selective increase in representations of sounds repeated at an ethological rate. J. Neurosci. 29, 5163-5169. doi: 10.1523/JNEUROSCI.0365-09.2009
23. Komisaruk, B. R. (1970). Synchrony between limbic system theta activity and rhythmical behavior in rats. J. Comp. Physiol. Psychol. 70, 482-492. doi: 10.1037/h0028709
24. Liu, R. C., Miller, K. D., Merzenich, M. M., and Schreiner, C. E. (2003). Acoustic variability and distinguishability among mouse ultrasound vocaliza­tions. J. Acoust. Soc. Am. 114, 3412. doi: 10.1121/1.1623787
25. Macrides, F. (1975). Temporal relationships between hippocampal slow waves and exploratory sniffing in hamsters. Behav. Biol. 14, 295-308.
26. Macrides, F., Eichenbaum, H., and Forbes, W. B. (1982). Temporal relationship between sniffing and the limbic rhythm during odor discrimination reversal learning. J. Neurosci. 2, 1705-1717.
27. McFarland, D. H., and Lund, J. P. (1993). An investigation of the coupling between respiration, mastication, and swallowing in the awake rabbit. J. Neurophysiol. 69, 95-108.
28. MacLarnon, A. M., and Hewitt, G. P. (1999). The evolution of human speech: the role of enhanced breathing control. Am. J. Phys. Anthropol. 109, 341-363. doi: 10.1002/(SICI)1096-8644(199907)109:3<341::AID-AJPA5>3.0.CO;2-2
29. Mitra, P., and Bokil, H. (2007). Observed Brain Dynamics. Oxford: Oxford University Press.
30. Miura, K., Mainen, Z. F., and Uchida, N. (2012). Odor representations in olfactory cortex: distributed rate coding and decorrelated population activity. Neuron 74, 1087-1098. doi: 10.1016/j.neuron.2012.04.021
31. Moore, J. D., Deschénes, M., Furuta, T., Huber, D., Smear, M. C., Demers, M., et al. (2013). Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature 497, 205-210. doi: 10.1038/nature12076
32. Moore, J. D., Kleinfeld, D., and Wang, F. (2014). How the brainstem controls oro­facial behaviors comprised of rhythmic actions. Trends Neurosci. 37, 370-380. doi: 10.1016/j.tins.2014.05.001
33. Nawrot, M. P. (2010). “Analysis and interpretation of interval and count variabil­ity in neural spike trains,” in Analysis of Parallel Spike Trains Springer Series in Computational Neuroscience, eds S. Grün and S. Rotter (New York, NY: Springer), 37-58.
34. Nyby, J., and Whitney, G. (1978). Ultrasonic communication of adult myomorph rodents. Neurosci. Biobehav. Rev. 2, 1-14. doi: 10.1016/0149-7634(78)90003-9
35. Ranade, S., Hangya, B., and Kepecs, A. (2013). Multiple modes of phase lock­ing between sniffing and whisking during active exploration. J. Neurosci. 33, 8250-8256. doi: 10.1523/JNEUROSCI.3874-12.2013
36. Riede, T. (2011). Subglottal pressure, tracheal airflow and intrinsic laryngeal mus­cle activity during rat ultrasound vocalization. J. Neurophysiol., 2580-2592. doi: 10.1152/jn.00478.2011
37. Riede, T. (2013). Stereotypic laryngeal and respiratory motor patterns generate different call types in rat ultrasound vocalization. J. Exp. Zool. A. Ecol. Genet. Physiol. 319,213-224. doi: 10.1002/jez.1785
38. Roberts, L. H. (1972). Correlation of respiration and ultrasound produc­tion in rodents and bats. J. Zool. 168, 439-449. doi: 10.1111/j.1469-7998.1972.tb01360.x
39. Roberts, L. H. (1975a). Evidence for the laryngeal source of ultrasonic and audible cries of rodents. J. Zool. 175, 243-257.
40. Roberts, L. H. (1975b). The rodent ultrasound production mechanism. Ultrasonics 13,83-88.
41. Saberi, K., and Perrott, D. R. (1999). Cognitive restoration of reversed speech. Nature 398, 760. doi: 10.1038/19652
42. Seffer, D., Schwarting, R. K. W., and Wohr, M. (2014). Pro-social ultrasonic com­munication in rats: insights from playback studies. J. Neurosci. Methods 234, 73-81. doi: 10.1016/j.jneumeth.2014.01.023
43. Sewell, G. D. (1970). Ultrasonic signals from rodents. Ultrasonics 8, 26-30.
44. Shusterman, R., Smear, M. C., Koulakov, A. A., and Rinberg, D. (2011). Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039-1044. doi: 10.1038/nn.2877
45. Smotherman, M., Schwartz, C., and Metzner, W. (2010). “Vocal-respiratory inter­actions in the parabrachial nucleus,” Handbook of Mammalian Vocalization—An Integrative Neuroscience Approach. Handbook of Behavioral Neuroscience, Vol. 19 (Amsterdam; Boston: Elsevier), 383-392.
46. Takahashi, N., Kashino, M., and Hironaka, N. (2010). Structure of rat ultra­sonic vocalizations and its relevance to behavior. PLoS ONE 5:e14115. doi: 10.1371/journal.pone.0014115
47. Wachowiak, M. (2011). All in a sniff: olfaction as a model for active sensing. Neuron 71, 962-973. doi: 10.1016/j.neuron.2011.08.030
48. Wang, X., Merzenich, M. M., Beitel, R., and Schreiner, C. E. (1995). Representation of a species-specific vocalization in the primary auditory cortex of the com­mon marmoset: temporal and spectral characteristics. J. Neurophysiol. 74, 2685-2706.
49. Welker, W. I. (1964). Analysis of sniffing of the albino rat. Behaviour 22, 223-244.
50. White, N. R., Prasad, M., Barfield, R. J., and Nyby, J. G. (1998). 40-and 70-kHz vocalizations of mice (Mus musculus) during copulation. Physiol. Behav. 63, 467-73.
51. Willadsen, M., Seffer, D., Schwarting, R. K. W., and Wohr, M. (2014). Rodent ultra­sonic communication: male prosocial 50-kHz ultrasonic vocalizations elicit social approach behavior in female rats (Rattus norvegicus). J. Comp. Psychol. 128, 56-64. doi: 10.1037/a0034778
52. Wohr, M., and Schwarting, R. K. W. (2007). Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior? PLoS ONE 2:e1365. doi: 10.1371/journal.pone.0001365
53. Wolfe, J., Mende, C., and Brecht, M. (2011). Social facial touch in rats. Behav. Neurosci. 125, 900-910. doi: 10.1037/a0026165
54. Wright, J. M., Gourdon, J. C., and Clarke, P. B. S. (2010). Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocal­izations: effects of amphetamine and social context. Psychopharmacology (Berl). 211, 1-13. doi: 10.1007/s00213-010-1859-y
55. Yajima, Y., and Hayashi, Y. (1983). Ambiguous motoneurons discharging syn­chronously with ultrasonic vocalization in rats. Exp. Brain Res. 50, 359-366. doi: 10.1007/BF00239201