Research ArticleNEUROSCIENCE

Limiting parental interaction during vocal development affects acoustic call structure in marmoset monkeys

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Science Advances  11 Apr 2018:
Vol. 4, no. 4, eaar4012
DOI: 10.1126/sciadv.aar4012
  • Fig. 1 Impact of parental interaction on vocal development of distinct call types in marmoset monkeys.

    (A) Left: family relationship of the five siblings. The triplets with limited parental interaction (S1-1, S1-2, and S1-3) were born before the normally raised twins (S2-1 and S2-2). Right: experimental timeline indicating the separation of the S1 siblings and vocal recordings in the S1 and S2 groups, respectively. (B) Examples of main adult call types. (C to E) Distribution of duration (top), frequency (middle), and entropy (bottom) for trill (C), twitter (D), and phee calls (E) across all five animals. Horizontal lines inside the boxes represent the median. Boxes represent the interquartile range (25th to 75th percentile), and whiskers indicate the 3rd and 97th percentiles.

  • Fig. 2 Differences in vocal sequence production between S1 and S2 monkeys.

    (A) From top to bottom: Spectrograms of an exemplar babbling-like sequence of an S1 monkey and exemplar vocal sequences with individual calls of an S1 and an S2 monkey, respectively. White horizontal lines indicate single calls and multisyllabic calls, respectively. (B) Relative distributions of intercall intervals (ICIs) from monkey S1-1 (red), S1-2 (orange), and S1-3 (pink), as well as S2-1 (dark blue) and S2-2 (light blue) (sliding window size, 100 ms; step size, 10 ms). (C) Median entropy distributions of trill, twitter, and phee calls made by S1-1 and S1-2 individually or during babbling-like behavior. Horizontal lines inside the boxes represent the median. Boxes represent the interquartile range (25th to 75th percentile), and whiskers indicate the 3rd and 97th percentiles.

  • Fig. 3 Transformation of infant marmoset calls into adult phee calls.

    (A) Examples of a cry, subharmonic phee, and proper phee call. As recently suggested, infant-specific cries transform to subharmonics and phees, and subharmonics transform to phees during vocal development and coexist to a certain degree during the subadult stages. (B) Median entropy distributions of distinct call types of S1 monkeys indicating different levels of maturity (cries, subharmonic phees, phees produced in babbling-like behavior, and individual phees) and proper phee calls of S2 monkeys. Horizontal lines inside the boxes represent the median entropy of cries, subharmonic phees, phees produced in babbling-like behavior, and individual phees of the S1-1 (red) and S1-2 (orange) subjects and the phees of the S2-1 (blue) and S2-2 subjects (light blue). Boxes represent the interquartile range (25th to 75th percentile), and whiskers indicate the 3rd and 97th percentiles.

  • Fig. 4 Temporary motif-like sequences occur in marmoset babbling-like behavior of S1 monkeys.

    (A) Outline of common call types during babbling-like behavior, such as trills (A), tsiks (B), cries/compound cries (C), subharmonic phees (C−), and phees (−C). According to a suggested model, cries/compound cries and subharmonics are assumed to be immature versions of adult phees. (B) Overall call distribution within babbling-like behavior. (C) Call transition matrices for calls being uttered before cry (C) vocalizations, tsik-cry pairs (BC, dark purple solid line), and trill-tsik-cry sequences (ABC, dashed lilac line). Transition indices are calculated as the observed relative transitions ratios between two call types divided by the transition ratios as expected from the relative occurrence of the respective call type. (D) Spectrograms of babbling-like sequences of S1 monkeys show motif-like structures predominantly showing BABC sequences, which were consecutively repeated and sometimes extended to longer sequences such as BABCAABA (lower trace). (E) In some motif-like sequences, subharmonic phees (C−) and phees (−C−) were occasionally uttered instead of cries (C) within the BABC sequences.

Supplementary Materials

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    • fig. S1. Difference in number of twitter syllables per twitter call in normally raised monkeys and siblings with limited parental interactions.

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