Nearest neighbours reveal fast and slow components of motor learning

• Published in: Nature (London) Vol. 577; no. 7791; pp. 526 - 530
• Main Authors: Kollmorgen, Sepp, Hahnloser, Richard H. R., Mante, Valerio
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 23.01.2020; Nature Publishing Group
• Subjects: 631/378/116/2396; 631/378/1595/2638; 631/378/2629/2631; Acoustics; Animal vocalization; Animals; Behavior; Computer Simulation; Consolidation; Data Interpretation, Statistical; Diurnal; Electronic data processing; Finches; Finches - physiology; Frequency; Humanities and Social Sciences; Learning; Learning - physiology; Male; Methods; Models, Neurological; Motor learning; Motor skill learning; multidisciplinary; Physiological aspects; Psychological research; Psychomotor Performance - physiology; Science; Science (multidisciplinary); Song; Songbirds; Sparrows; Syllables; Time Factors; Vocalization behavior; Vocalization, Animal - physiology; Switzerland
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-019-1892-x

Changes in behaviour resulting from environmental influences, development and learning 1 – 5 are commonly quantified on the basis of a few hand-picked features 2 – 4 , 6 , 7 (for example, the average pitch of acoustic vocalizations 3 ), assuming discrete classes of behaviours (such as distinct vocal syllables) 2 , 3 , 8 – 10 . However, such methods generalize poorly across different behaviours and model systems and may miss important components of change. Here we present a more-general account of behavioural change that is based on nearest-neighbour statistics 11 – 13 , and apply it to song development in a songbird, the zebra finch 3 . First, we introduce the concept of ‘repertoire dating’, whereby each rendition of a behaviour (for example, each vocalization) is assigned a repertoire time, reflecting when similar renditions were typical in the behavioural repertoire. Repertoire time isolates the components of vocal variability that are congruent with long-term changes due to vocal learning and development, and stratifies the behavioural repertoire into ‘regressions’, ‘anticipations’ and ‘typical renditions’. Second, we obtain a holistic, yet low-dimensional, description of vocal change in terms of a stratified ‘behavioural trajectory’, revealing numerous previously unrecognized components of behavioural change on fast and slow timescales, as well as distinct patterns of overnight consolidation 1 , 2 , 4 , 14 , 15  across the behavioral repertoire. We find that diurnal changes in regressions undergo only weak consolidation, whereas anticipations and typical renditions consolidate fully. Because of its generality, our nonparametric description of how behaviour evolves relative to itself—rather than to a potentially arbitrary, experimenter-defined goal 2 , 3 , 14 , 16 —appears well suited for comparing learning and change across behaviours and species 17 , 18 , as well as biological and artificial systems 5 . A new method for analysing change in high-dimensional data is based on nearest-neighbour statistics and is applied here to song dynamics during vocal learning in zebra finches, but could potentially be applied to other biological and artificial behaviours.