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Correspondence interested in his diversity of movements One important difference between to music. This was because his owner Snowball’s dancing and human dancing Spontaneity (author I.S.) observed that Snowball is that Snowball danced in short was using new movements to music episodes rather than continuously and diversity of not present in our original study, and (mean duration = 3.69 seconds, std = appeared to be in a period of ‘movement 2.72 seconds; N = 141), consistent with movement to music exploration’. Importantly, this was not earlier reports [2]. Informal observations are not uniquely due to modeling by I.S., who does by author I.S. suggest that Snowball not make a wide range of movements moves more continuously when a human when dancing with Snowball and human dances with him, which we plan tends only to engage in head bobbing to examine in future work. and hand waving. Also, Snowball was To determine if certain moments in R. Joanne Jao Keehn1, John R. Iversen2, never explicitly trained to make specifi c each song triggered specifi c dance Irena Schulz3, and Aniruddh D. Patel4,5,6,* movements to music (for example, movements, time segments during via operant conditioning with food which Snowball danced in all three Spontaneous movement to music rewards, as in [7]). During this period of trials were fi rst identifi ed (Figure S1B). occurs in every human culture and is a exploration, Snowball seemed to favor We then examined each such segment foundation of dance [1]. This response movement diversity over synchronization to see if he used the same dance to music is absent in most species accuracy: his rhythmic movements often movement in all three trials. In both (including monkeys), yet it occurs in seemed not highly synchronized to the songs, there was not a single segment parrots, perhaps because they (like beat, possibly because he was primarily in which all three trials contained the humans, and unlike monkeys) are vocal exploring new movements rather than same dance move. Thus, in addition to learners whose brains contain strong exploiting old ones. the diversity of his movement to music, auditory–motor connections, conferring To quantify Snowball’s movement another sign of Snowball’s fl exibility in sophisticated audiomotor processing diversity we fi lmed him moving to two moving to music is that his movements abilities [2,3]. Previous research has pop songs: “Another One Bites the are not constrained by certain audio shown that parrots can bob their Dust” and “Girls Just Wanna Have features of the music. We also found heads or lift their feet in synchrony Fun”, each presented three times (23 that Snowball used different proportions with a musical beat [2,3], but humans minutes of music in total). Filming took of dance moves in the two songs (Figure move to music using a wide variety of place in September 2008. Snowball S2), though more data would be needed movements and body parts. Is this also was 12 years old and had not danced to determine whether this is a stable true of parrots? If so, it would constrain to these songs with anyone other than difference. theories of how movement to music is his owner. During fi lming, the owner was Snowball is not unique: other controlled by parrot brains. Specifi cally, in the room and gave occasional verbal examples of diversity in parrot as head bobbing is part of parrot encouragement (such as “good boy!”), movement to music can be found on courtship displays [4] and foot lifting but did not dance or move rhythmically. the internet (see links in Supplemental is part of locomotion, these may be Movement coding was performed using Information). A key question, however, is innate movements controlled by central frame-by-frame analysis with the audio how such moves are acquired. Parrots pattern generators which become muted and was conducted by author can imitate movements [9], and if their entrained by auditory rhythms, without R.J.J.K., a cognitive neuroscientist and movements to music are due to imitation the involvement of complex motor classically and contemporarily trained (for example, from seeing humans planning. This would be unlike humans, dancer. The temporal onset and offset dance), it would suggest that parrots where movement to music engages of each movement or sequence of can solve the ‘correspondence problem’ cortical networks including frontal and repeated movements were recorded, [1] in a remarkably sophisticated way parietal areas [5]. Rich diversity in parrot focusing on ‘dance movements’, (watching an individual with a very movement to music would suggest a defi ned (following [8]) as movements different body morphology perform strong contribution of forebrain regions that are clearly intentional but which are a motor pattern, then mapping that to this behavior, perhaps including not an effi cient means of achieving any pattern across modalities onto one’s motor learning regions abutting the plausible external goal, such as basic own motor system, without direct complex vocal-learning ‘shell’ regions locomotion. Our analyses revealed that reinforcement). Another possibility is that that are unique to parrots among vocal Snowball had a diverse repertoire of 14 some moves may refl ect creativity. This learning birds [6]. Here we report that dance movements and two composite would also be remarkable, as creativity a sulphur-crested cockatoo (Cacatua movements (Table 1). An excerpt in nonhuman animals has typically been galerita eleonora) responds to music from one trial annotated with dance documented in behaviors aimed at with remarkably diverse spontaneous movements is provided in Supplemental obtaining an immediate physical benefi t, movements employing a variety of body Video S1 and Figure S1A. A compilation such as access to food or mating parts, and suggest why parrots share of the 14 dance movements is shown opportunities. Snowball does not dance this response with humans. in Supplemental Video S2 (all six videos for food or in order to mate; instead, his Soon after our original study [2] of from the study, annotated by R.J.J.K., dancing appears to be a social behavior synchronization to a musical beat in this are available via a link in Supplemental used to interact with human caregivers parrot (named ‘Snowball’), we became Information.) (his surrogate fl ock).

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Table 1. Dance movements and descriptions.

Movementa Description ‘Girls’ ‘Another’ Body Roll (B) Wave passes through head, then body x x Counter-Clockwise Circle (CCW) Head moves in a circular trajectory in counter-clockwise direction x Downward (D) Head bobs up and down xx Head shakes while bobbing down, 3 frames of shaking at lowest Down-Shake (DS) x dip Foot-Lift (F) Foot lifts, body remains stationary x x Foot-Lift Down Swing (FL) Foot lifts while head swings diagonally downward xx Headbang (H) Head is thrown forward and backward, sometimes in pattern-8 x Head-Foot Sync (HF) Head moves in sync with foot xx Headbang w/ Lifted Foot (HL) Foot lifts while head bangs xx Pose (P) Body poses/holds a stationary position x x Side-to-Side (S) Foot lifts while head moves from side-to-side with rebound in neck x x Both feet remain close to or in contact w/ surface; head follows a Semi-Circle Low (SCL) x semi-circle (lower half) trajectory Both feet remain close to or in contact w/ surface; head follows Semi-Circle High (SCH) xx a semi-circle (upper half) trajectory Vogue (V) Head moves from one side of lifted foot to the other xx Head bobs up and down interspersed with head moving in sync with Downward/Head-Foot Sync (D/HF) x foot Headbang/Semi-Circle Low Inter- Head is thrown forward and backward interspersed with head x changed (H/SCL) following a semi-circle (lower half) trajectory aPredominant movements are in bold text. These are movements with durations comprising at least 10% of the overall dance movement duration for any given trial. In right two columns, x = occurred during that song.

Building on ideas articulated in [1], The Neurosciences Institute (San Diego, CA). entrainment to rhythmic auditory stimuli in a non We thank Irene Pepperberg and Erich Jarvis vocal mimic. J. Comp. Psychol. 127, 412–427. we suggest that spontaneous and 8. Schachner, A., and Carey, S. (2013). Reasoning diverse movement to music arises when for their input on issues of parrot behavior and about ‘irrational’ actions: When intentional fi ve traits converge: A) complex vocal neurobiology. movements cannot be explained, the movements themselves are seen as the goal. Cognition 129, learning, B) the capacity for nonverbal 309–327. movement imitation, C) a tendency to AUTHOR CONTRIBUTIONS 9. Heyes, C., and Saggerson, A. (2002). Testing for imitative and nonimitative social learning in the form long-term social bonds, D) the budgerigar using a two-object/two-action test. ability to learn complex sequences J.R.I. and A.D.P. designed the experiments, I.S. Anim. Behav. 64, 851–859. of actions, and E) attentiveness to conducted the experiments, R.J.J.K. analyzed 10. Auersperg, A.M., Kacelnik, A., and von Bayern, the data, R.J.J.K, J.R.I. and A.D.P. wrote the A.M. (2013). Explorative learning and functional communicative movements. Parrots are inferences on a fi ve-step means-means-end unusual in sharing all of these traits with paper. problem in Goffi n’s cockatoos (Cacatua goffi ni). humans [4,9,10], which could explain PLoS One 8, e68979. why (to date) only humans and parrots REFERENCES show spontaneous and diverse dancing 1Brain Development Imaging Labs, Department to music. 1. Laland, K., Wilkins, C., and Clayton, N. (2016). The evolution of dance. Curr. Biol. 26, R5–R9. of Psychology, San Diego State University, 2. Patel, A.D., Iversen, J.R., Bregman, M.R., and 6363 Alvarado Ct. #200, San Diego, CA 92120, 2 SUPPLEMENTAL INFORMATION Schulz, I. (2009). Experimental evidence for USA. University of California San Diego, synchronization to a musical beat in a nonhuman Institute for Neural Computation, 9500 Gilman animal. Curr. Biol. 19, 827–830. Dr. #0559, La Jolla, CA 92093, USA. 3Bird Supplemental Information includes two fi gures, 3. Schachner, A., Brady, T.F., Pepperberg, I.M., two videos, supplemental experimental and Hauser, M.D. (2009). Spontaneous motor Lovers Only Rescue Service Inc., Duncan, SC 29334, USA. 4Department of Psychology, Tufts procedures, and links to other videos of parrots entrainment to music in multiple vocal mimicking species. Curr. Biol. 19, 831–836. University, 490 Boston Ave., Medford, MA moving to music, and can be found with this 4. A.U. Luescher, ed. (2006). Manual of Parrot 02155, USA. 5Azrieli Program in Brain, Mind, article online at https://doi.org/10.1016/j. Behavior (Ames, Iowa: Blackwell). and Consciousness, Canadian Institute for cub.2019.05.035. 5. Karpati, F.J., Giacosa, C., Foster, N.E., Penhune, V.B., and Hyde, K.L. (2015). Dance and the brain: Advanced Research (CIFAR), MaRS Centre, a review. Ann. N.Y. Acad. Sci. 1337, 140–146. West Tower, 661 University Ave., Suite 505, ACKNOWLEDGMENTS 6. Chakraborty, M., and Jarvis, E.D. (2015). Brain Toronto, ON, MG5 1M1, Canada. 6Radcliffe evolution by brain pathway duplication. Philos. Institute for Advanced Study, Harvard Filming and initial data analysis were supported Trans. R. Soc. Lond. B 370, 20150056. University, 10 Garden St., Cambridge, MA 7. Cook, P., Rouse, A., Wilson, M., and Reichmuth, by Neurosciences Research Foundation as C. (2013). A California sea lion (Zalophus 02138, USA. part of its program on music and the brain at californianus) can keep the beat: Motor *E-mail: [email protected]

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