Abstract
Rhythmic ability is important for locomotion, communication, and coordination between group members during the daily life of animals. We aimed to examine the rhythm perception and production abilities in rats within the range of a subsecond to a few seconds. We trained rats to respond to audio-visual stimuli presented in regular, isochronous rhythms at six time-intervals (0.5–2 s). Five out of six rats successfully learned to respond to the sequential stimuli. All subjects showed periodic actions. The actions to regular stimuli were faster than randomly presented stimuli in the medium-tempo conditions. In slower and faster tempo conditions, the actions of some subjects were not periodic or phase-matched to the stimuli. The asynchrony regarding the stimulus onset became larger or smaller when the last stimulus of the sequence was presented at deviated timings. Thus, the actions of the rats were tempo matched to the regular rhythm, but not completely anticipative. We also compared the extent of phase-matching and variability of rhythm production among the interval conditions. In interval conditions longer than 1.5 s, variability tended to be larger. In conclusion, rats showed a tempo matching ability to regular rhythms to a certain degree, but maintenance of a constant tempo to slower rhythm conditions was difficult. Our findings suggest that non-vocal learning mammals have the potential to produce flexible rhythms in subsecond timing.
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References
Agostinelli C, Lund U (2017) R package ‘circular’: Circular Statistics (version 0.4-93)
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. https://doi.org/10.18637/jss.v067.i01
Brudzynski SM (2013) Ethotransmission: Communication of emotional states through ultrasonic vocalization in rats. Curr Opin Neurobiol 23:310–317. https://doi.org/10.1016/j.conb.2013.01.014
Connor RC, Smolker R, Bejder L (2006) Synchrony, social behaviour and alliance affiliation in Indian Ocean bottlenose dolphins, Tursiops aduncus. Anim Behav 72:1371–1378. https://doi.org/10.1016/j.anbehav.2006.03.014
Cook P, Rouse A, Wilson M, Reichmuth C (2013) A California sea lion (Zalophus californianus) can keep the beat: motor entrainment to rhythmic auditory stimuli in a non vocal mimic. J Comp Psychol 127:412–427. https://doi.org/10.1037/a0032345
Hasegawa A, Okanoya K, Hasegawa T, Seki Y (2011) Rhythmic synchronization tapping to an audio–visual metronome in budgerigars. Sci Rep 1:120. https://doi.org/10.1038/srep00120
Hattori Y, Tomonaga M, Matsuzawa T (2013) Spontaneous synchronized tapping to an auditory rhythm in a chimpanzee. Sci Rep 3:1566. https://doi.org/10.1038/srep01566
Hoeschele M, Merchant H, Kikuchi Y, Hattori Y, ten Cate C (2015) Searching for the origins of musicality across species. Phil Trans R Soc B 370:20140094. https://doi.org/10.1098/rstb.2014.0094
Kawai R et al (2015) Motor cortex is required for learning but not for executing a motor skill. Neuron 86:800–812. https://doi.org/10.1016/j.neuron.2015.03.024
Kirschner S, Tomasello M (2009) Joint drumming: social context facilitates synchronization in preschool children. J Exp Child Psychol 102:299–314. https://doi.org/10.1016/j.jecp.2008.07.005
Large EW, Gray PM (2015) Spontaneous tempo and rhythmic entrainment in a bonobo (Pan paniscus). J Comp Psychol 129:317–328. https://doi.org/10.1037/com0000011
Larsson M (2012) Incidental sounds of locomotion in animal cognition. Anim Cogn 15:1–13. https://doi.org/10.1007/s10071-011-0433-2
Larsson M (2014) Self-generated sounds of locomotion and ventilation and the evolution of human rhythmic abilities. Anim Cogn 17:1–14. https://doi.org/10.1007/s10071-013-0678-z
Larsson M, Abbott BW (2018) Is the capacity for vocal learning in vertebrates rooted in fish schooling behavior? Evol Biol 45:359–373. https://doi.org/10.1007/s11692-018-9457-8
Lopuch S, Popik P (2011) Cooperative behavior of laboratory rats (Rattus norvegicus) in an instrumental task. J Comp Psychol 125:250–253. https://doi.org/10.1037/a0021532
Merchant H, Honing H (2014) Are non-human primates capable of rhythmic entrainment? Evidence for the gradual audiomotor evolution hypothesis. Front Neurosci 7:274. https://doi.org/10.3389/fnins.2013.00274
Noda T, Amemiya T, Shiramatsu TI, Takahashi H (2017) Stimulus phase locking of cortical oscillations for rhythmic tone sequences in rats. Front Neural Circ 11:2. https://doi.org/10.3389/fncir.2017.00002
Patel AD (2006) Musical rhythm, linguistic rhythm, and human evolution. Music Percep 24:99–103. https://doi.org/10.1525/mp.2006.24.1.99
Patel AD (2014) The evolutionary biology of musical rhythm: was Darwin wrong? PLoS Biol 12:e1001821. https://doi.org/10.1371/journal.pbio.1001821
Patel AD, Iversen JR (2014) The evolutionary neuroscience of musical beat perception: the action simulation for auditory prediction (ASAP) hypothesis. Front Syst Neurosci 8:57. https://doi.org/10.3389/fnsys.2014.00057
Patel AD, Iversen JR, Bregman MR, Schulz I (2009) Studying synchronization to a musical beat in nonhuman animals. Ann N Y Acad Sci 1169:459–469. https://doi.org/10.1111/j.1749-6632.2009.04581.x
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reichmuth C, Casey C (2014) Vocal learning in seals, sea lions, and walruses. Curr Opin Neurobiol 28:66–71. https://doi.org/10.1016/j.conb.2014.06.011
Repp BH (2005) Sensorimotor synchronization: a review of the tapping literature. Psychon B Rev 12:969–992. https://doi.org/10.3758/bf03206433
Rutte C, Taborsky M (2007) The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalised reciprocity. Behav Ecol Sociobiol 62:499–505. https://doi.org/10.1007/s00265-007-0474-3
Schachner A, Brady TF, Pepperberg IM, Hauser MD (2009) Spontaneous motor entrainment to music in multiple vocal mimicking species. Curr Biol 19:831–836. https://doi.org/10.1016/j.cub.2009.03.061
Seffer D, Schwarting RKW, Wöhr M (2014) Pro-social ultrasonic communication in rats: Insights from playback studies. J Neurosci Methods 234:73–81. https://doi.org/10.1016/j.jneumeth.2014.01.023
Tan L, Hackenberg TD (2016) Functional analysis of mutual behavior in laboratory rats (Rattus norvegicus). J Comp Psychol 130:13–23. https://doi.org/10.1037/com0000015
ten Cate C, Spierings M (2018) Rules, rhythm and grouping: auditory pattern perception by birds. Anim Behav 151:249–257. https://doi.org/10.1016/j.anbehav.2018.11.010
Wang T (2015) A hypothesis on the biological origins and social evolution of music and dance. Front Neurosci 9:30. https://doi.org/10.3389/fnins.2015.00030
Wilson M, Cook PF (2016) Rhythmic entrainment: Why humans want to, fireflies can’t help it, pet birds try, and sea lions have to be bribed. Psychon Bull Rev 23:1647–1659. https://doi.org/10.3758/s13423-016-1013-x
Zarco W, Merchant H, Prado L, Mendez JC (2009) Subsecond timing in primates: comparison of interval production between human subjects and rhesus monkeys. J Neurophysiol 102:3191–3202. https://doi.org/10.1152/jn.00066.2009
Acknowledgements
We are grateful to Dr. Yoshimasa Seki for his useful comments on our experiment. We thank the editor and three anonymous reviewers for their useful and constructive comments on the manuscript.
Funding
This study was supported by a JSPS KAKENHI Grant number 17J10994 to N. K., and MEXT/JSPS KAKENHI Grant number #4903, JP17H06380 to K. O.
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The experiments in the present study were conducted in accordance with experimental implementation regulations of the University of Tokyo. The present study was approved by the animal experimental committee at the University of Tokyo, Graduate School of Arts and Sciences (Permission Number: 27-8).
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Katsu, N., Yuki, S. & Okanoya, K. Production of regular rhythm induced by external stimuli in rats. Anim Cogn 24, 1133–1141 (2021). https://doi.org/10.1007/s10071-021-01505-4
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DOI: https://doi.org/10.1007/s10071-021-01505-4