A California sea lion (Zalophus californianus) can keep the beat: Motor entrainment to rhythmic auditory stimuli in a non vocal mimic.

Abstract

Is the ability to entrain motor activity to a rhythmic auditory stimulus, that is "keep a beat," dependent on neural adaptations supporting vocal mimicry? That is the premise of the vocal learning and synchronization hypothesis, recently advanced to explain the basis of this behavior (A. Patel, 2006, Musical Rhythm, Linguistic Rhythm, and Human Evolution, Music Perception, 24, 99-104). Prior to the current study, only vocal mimics, including humans, cockatoos, and budgerigars, have been shown to be capable of motoric entrainment. Here we demonstrate that a less vocally flexible animal, a California sea lion (Zalophus californianus), can learn to entrain head bobbing to an auditory rhythm meeting three criteria: a behavioral response that does not reproduce the stimulus; performance transfer to a range of novel tempos; and entrainment to complex, musical stimuli. These findings show that the capacity for entrainment of movement to rhythmic sounds does not depend on a capacity for vocal mimicry, and may be more widespread in the animal kingdom than previously hypothesized.

Synchronization and temporal processing

“…In terms of the model of Figure 1, for the most part, only rudimentary (1:1) SMS represented by the inner box has been observed in other species and it is typically of limited flexibility in comparison with human SMS. To date, only a few species (vocal-learning birds and a sea lion) have been shown to be capable of 'Complex SMS' by synchronizing to the beat of more complex, musical stimuli, indicating a capacity to extract a beat from a complex auditory stimulus, and even to map flexibly to different motor outputs [66,69,76]. Evidence for hierarchical metrical perception or other aspects of rich BPS has not yet adequately been examined in nonhuman animals [77,78].…”

“…The origins of human rhythmic abilities are a matter of vigorous debate and speculation. Origin accounts of SMS range from being an adaptation for sexual selection, communication, group cohesion, to being a non-evolved side effect of other evolved traits (reviewed in [65]), and debate has been spurred by a recent spate of comparative studies exploring the limits of SMS in non-human animals including parrots, primates, and sea lions [66][67][68][69][70][71] as well as prior descriptions of naturally occurring SMS behaviors for instance in insects and frogs (reviewed in [72 ]), and temporal sequencing and grouping abilities in other species [73]. There are many recent reviews of comparative SMS, some emphasizing the continuity of human abilities with those of other species, based on shared mechanisms (e.g.…”

Finding the beat: a neural perspective across humans and non-human primates

“…Why is it that the one chimpanzee (out of three tested) who shows any evidence at all for beat perception and synchronization only does so for a single preferred tempo, and does not generalize this behaviour to other tempos [132]? What is it about the brain of parrots or sea lions that, in contrast to these primates, enables them to quite flexibly entrain to rhythmic musical stimuli [133][134][135][136]? Why is it that some very small and apparently simple brains (e.g.…”

The Evolution of Rhythm Cognition: Timing in Music and Speech

“…(1) developmental studies of rhythm that are useful in understanding whether rhythm perception and production involve critical acquisition periods, or instead result mostly from enculturation during the whole lifespan (Hannon and Trehub, 2005), (2) comparative and cross-cultural studies of rhythm that serve to explain whether musical enculturation or exposure to specific languages can affect which specific rhythmic patterns can be produced/perceived and how frequently (Greenberg et al, 1978;Rzeszutek et al, 2012), (3) comparisons of rhythm processing in music and speech, at both behavioral and neural levels that help understanding whether common music-speech networks exist and similar behavioral patterns can be observed when humans engage in music and speech production, (4) evidence and comparison of rhythm processing across modalities and domains that are used to understand whether, for instance, metrical expectation in speech is strictly bound to the speech domain or instead recruits the same capacities for metricality available in music, or even in dance and vision (Iversen et al, 2015), (5) studies of rhythm in interaction and context (Yu and Tomonaga, 2015), explaining how social, affective, and other factors affect the emergence of rhythmic patterns, (6) archaeological findings trying to reconstruct rhythmrelated behavior and cognition in our early hominid ancestors (Morley, 2003), (7) mathematical and computational models (e.g., connectionist, symbolic) of the mechanisms underlying perception and production of rhythmic behavior (Desain and Honing, 1989, 1991, 2003, (8) mathematical and computational models of rhythmic capacities as evolved behaviors (Miranda et al, 2003) in line with a long tradition in evolutionary and theoretical biology, (9) evidence of spontaneous rhythmic behavior in other animals (Fuhrmann et al, 2014;Ravignani et al, 2014a) showing how similar rhythmic traits can evolve via similar pressures in phylogenetically distant species, (10) controlled experiments in non-human animals (Cook et al, 2013) probing the potential for producing/perceiving rhythm (even though these are not usually part of these species' natural behavior); these experiments can show the existence of basic, evolutionary conserved cognitive processes that may have been exapted in humans for rhythmic purposes.…”