Elsevier

Animal Behaviour

Volume 78, Issue 5, November 2009, Pages 1195-1203
Animal Behaviour

Motor planning for vocal production in common marmosets

https://doi.org/10.1016/j.anbehav.2009.07.038Get rights and content

The vocal motor plan is one of the most fundamental and poorly understood elements of primate vocal production. Here we tested whether a single vocal motor plan comprises the full length of a vocalization. We hypothesized that if a single motor plan was determined at vocal onset, the acoustic features early in the call should be predictive of the subsequent call structure. Analyses were performed on two classes of features in marmoset phee calls: continuous and discrete. We first generated correlation matrices of all the continuous features of phee calls. Results showed that the start frequency of a phee's first pulse significantly correlated with all subsequent spectral features. Moreover, significant correlations were evident within both the spectral and temporal features, but there was little relationship between these feature classes. Using a discrete feature, ‘the number of pulses in the phee call’, a discriminant function was able to correctly classify the number of pulses in the calls well above chance based solely on the acoustic structure of the call's first pulse. Together, these data suggest that a vocal motor plan for the complete call structure is established at call onset. These findings provide a key insight into the mechanisms underlying vocal production in nonhuman primates.

Section snippets

Subjects

We recorded 1701 phee calls produced by 10 adult common marmosets (6 male, 4 female). The common marmoset is a small-bodied (∼400 g), New World primate endemic to the rainforests of northeastern Brazil (Rylands 1993). Subjects are housed in social groups consisting of pair-bonded mates and up to two generations of offspring. This highly vocal primate has been the subject of several previous behavioural and neural studies of vocal communication (Norcross and Newman, 1993, Wang and Kadia, 2001,

Continuous Feature Analysis

We analysed 1701 naturally produced phee calls from 10 adult common marmosets. The data set consisted of 507 one-pulse phees, 1052 two-pulse phees and 142 three-pulse phees. As discussed above, we used only two-pulse phees in the continuous feature analysis. To test the extent to which the spectral and temporal features of phee calls were correlated across phee calls, we performed the following cross-correlation analyses. For this analysis, we only tested those measured acoustic features that

Discussion

The aim of this study was to test the structure of one of the most fundamental aspects of vocal production, the vocal motor plan. Motor plans are common in deliberate motor acts for determining the sequence of actions prior to their initiation (Sternbert et al., 1978, Zingale and Kowler, 1987, Sarlegna and Sainburg, 2008). Its existence in the vocal motor system, however, has not been addressed. We asked the following question. When a vocalization is produced, does the motor plan comprise all

Acknowledgments

We thank Mark Bee, Asif Ghazanfar, Judith Scarl, Yi Zhou and two referees for helpful comments on this manuscript. This work was supported by grants from the National Institutes of Health to C.T.M. (K99 DC009007) and X.W. (R01 DC005808).

References (36)

  • S.E.R. Egnor et al.

    Noise-induced vocal modulation in cotton-top tamarins

    American Journal of Primatology

    (2006)
  • S.E.R. Egnor et al.

    Perturbation of auditory feedback causes systematic pertubation in vocal structure in adult cotton-top tamarins

    Journal of Experimental Biology

    (2006)
  • S.E.R. Egnor et al.

    Tracking silence: adjusting vocal production to avoid acoustic interference

    Journal of Comparative Physiology A

    (2007)
  • S.J. Eliades et al.

    Sensory–motor interaction in the primate auditory cortex during self-initiated vocalizations

    Journal of Neurophysiology

    (2003)
  • S.J. Eliades et al.

    Neural substrates of vocalization feedback monitoring in primate auditory cortex

    Nature

    (2008)
  • K. Hammerschmidt et al.

    Constraints in primate vocal production

  • V.M. Janik

    Whistle matching in wild bottlenose dolphins (Tursiops truncatus)

    Science

    (2000)
  • M.I. Jordan et al.

    Computational motor control

  • Cited by (22)

    • The role of auditory feedback on vocal pattern generation in marmoset monkeys

      2020, Current Opinion in Neurobiology
      Citation Excerpt :

      For example, behavioral experiments have shown that monkeys can stop sequences of calls immediately after acoustic perturbation, but cannot interrupt the acoustic structure of ongoing vocalizations [11,12]. These findings suggested that calls consist of single discrete pulses [11,12] and that the vocal motor plan is already present before vocal onset [13]. In accordance with neurophysiological and anatomical studies, these vocalizations were found to be produced by a vocal pattern-generating network (VPGN) situated in the brainstem [2•,6,14] that is capable of producing rather fixed, inflexible, and discrete utterances.

    • Precise Motor Control Enables Rapid Flexibility in Vocal Behavior of Marmoset Monkeys

      2018, Current Biology
      Citation Excerpt :

      This behavior was consistent and did not differ between onset time groups (p = 0.8175, Kruskal-Wallis test; n = 250), showing that the median time point of call interruption was independent of whether perturbing noise was early, intermediate, or late after call onset. These results show that, in contrast to earlier findings [17, 18, 21], monkeys are capable of interrupting ongoing vocalizations in response to a perturbing acoustic signal. What does this mean for vocal pattern generation?

    • Neuroanatomy of the marmoset

      2018, The Common Marmoset in Captivity and Biomedical Research
    • Ultrasonic Components of Vocalizations in Marmosets

      2018, Handbook of Behavioral Neuroscience
      Citation Excerpt :

      Filtering out high frequencies from a broadband noise signal also degraded sound-localization performance for vertical localization in monkeys (Brown, Schessler, Moody, & Stebbins, 1982). The biological significance attributed to auditory localization has led to numerous neurophysiological, neuroanatomical, and psychophysical experiments on marmosets and other species (Aitkin, Merzenich, Irvine, Clarey, & Nelson, 1986; Bendor & Wang, 2005, 2006, 2008, 2010; Eliades & Wang, 2003, 2005, 2008; Miller, Beck, Meade, & Wang, 2009; Miller, Eliades, & Wang, 2009; Miller, Mandel, & Wang, 2010; Miller & Wang, 2006). The term “ultrasonic” refers to frequencies above the nominal upper hearing limit of humans, which is 20 kHz.

    • Marmosets: A Neuroscientific Model of Human Social Behavior

      2016, Neuron
      Citation Excerpt :

      Marmosets will cease to interact with callers who deviate from the correct temporal pattern (Miller et al., 2009a). Callers exert control over several aspects of signal production during this behavior, ranging from a motor plan about the structure of the vocalization to avoiding sources of acoustic interference (Miller et al., 2009b; Roy et al., 2011). During an experiment in which noise was broadcast with different periodicities, for example, pairs of marmosets coordinated the timing of their behavior to both avoid the interference and maintain turn taking within the constraints of the environment (Roy et al., 2011).

    • Receiver psychology turns 20: Is it time for a broader approach?

      2012, Animal Behaviour
      Citation Excerpt :

      While all antiphonal calls in common marmosets are the species-typical phee call, decisions about the specific form this call will take (i.e. what to produce) are somewhat more complicated. Callers appear to plan specific spectral and temporal features of the vocalization prior to call production, such as the frequency contour and duration of each pulse (Miller et al. 2009a). The resulting acoustic structure may then have an impact on subsequent interactions.

    View all citing articles on Scopus
    1

    S. J. Eliades and X. Wang are at the Laboratory of Auditory Neurophysiology, Department of Biomedical Engineering, Johns Hopkins University, School of Medicine, 720 Rutland Avenue, Traylor 412, Baltimore, MD 21205, U.S.A.

    View full text