Vocal Motor Performance in Birdsong Requires Brain–Body Interaction

Adam, Iris; Elemans, Coen P. H.

doi:10.1523/eneuro.0053-19.2019

Cited by 18 publications

(22 citation statements)

References 75 publications

(102 reference statements)

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“…During postnatal vocal development, gradual body changes, such as lung growth or VF stiffness in marmosets (46,47) or increased muscle speed in songbirds (48), can drive changes in vocal 180 behavior. Embodied human VF models have direct clinical relevance to pathological physical behaviors with abnormal vocal output (1) and patient specific model-assisted phonosurgery (49,50), because most laryngeal human voice disorders are caused by changes in VF geometry, structural integrity, or kinematics (4).…”

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“…Because animal behaviors result from complex system-wide interactions between nervous system, body, and surrounding environment, the activity of neural circuits controlling sound can only be understood by considering the biomechanics of sound generation, muscles, bodies, and the exterior world (43)(44)(45)(46). In vocal behaviors, indeed small tissue changes can lead 190 to state changes in vocal dynamics (47) and changes in muscle performance interact with neural coding in songbirds (48). An embodied approach to voice production as presented here that captures accurate parameterization of vocal organs is essential to further our understanding how underlying neural mechanisms and biomechanics interact to drive vocal behavior, from direct…”

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High-fidelity continuum modeling predicts avian voiced sound production

Jiang

Rasmussen

Xue

et al. 2019

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20Voiced sound production is the primary form of acoustic communication in terrestrial vertebrates, particularly birds and mammals, and including humans. Developing a causal physics-based model that links descending vocal motor control to tissue vibration and sound, requires embodied approaches that include realistic representations of voice physiology. Here we first implement and then experimentally test a high-fidelity three-dimensional continuum model 25 for voiced sound production in birds. Driven by individual-based physiologically quantifiable inputs, combined with non-invasive inverse methods for tissue material parameterization, our model accurately predicts observed key vibratory and acoustic performance traits. These results demonstrate that realistic models lead to accurate predictions supporting the continuum model approach as a critical tool towards a causal model of motor control of voiced sound production. 30

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High-fidelity continuum modeling predicts avian voiced sound production

Jiang

Rasmussen

Xue

et al. 2019

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“…In contrast to the well-described neural circuitry underlying song learning [3], we know surprisingly little how the motor pool controlling the songbird syrinx is organized [4]. 50 Furthermore, even though birdsong is often called a fine-motor skill [13,14] and perturbed auditory feedback can drive small fo changes [15,16], the control resolution of acoustic features remains unknown. Motor control of any behavior is limited to the minimal force step available when activating muscles, which is set by the number and size distribution of MUs and muscle fiber 55 specific force generation [1].…”

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One-to-one innervation of vocal muscles allows precise control of birdsong

Adam

Maxwell

Rößler

et al. 2020

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15SummaryThe motor control resolution of any animal behavior is limited to the minimal force step available when activating muscles, which is set by the number and size distribution of motor units (MUs) and muscle specific force [1,2]. Birdsong is an excellent model system for understanding sequence learning of complex fine motor skills [3], but we know surprisingly 20 little how the motor pool controlling the syrinx is organized [4] and how MU recruitment drives changes in vocal output [5]. Here we combine measurements of syringeal muscle innervation ratios with muscle stress and an in vitro syrinx preparation to estimate MU size distribution and the control resolution of fundamental frequency (fo), a key vocal parameter, in zebra finches. We show that syringeal muscles have extremely small MUs, with 50% 25innervating ≤ 3, and 13 -17% innervating a single muscle fiber. Combined with the lowest specific stress (5 mN/mm 2 ) known to skeletal vertebrate muscle, small force steps by the major fo controlling muscle provide control of 50 mHz to 4.2 Hz steps per MU. We show that the song system has the highest motor control resolution possible in the vertebrate nervous system and suggest this evolved due to strong selection on fine gradation of vocal output. 30Furthermore, we propose that high-resolution motor control was a key feature contributing to the radiation of songbirds that allowed diversification of song and speciation by vocal space expansion. Results & DiscussionVocal communication is of paramount importance for reproduction and survival of songbirds and even drives speciation. This is clearly exemplified by sympatric species that are 40 morphologically indistinguishable, but nevertheless fully separated solely by song [6, 7]. The potential to acoustically separate depends on the number of distinct sounds -or vocal space -that can be produced and perceived. The vocal space is set both by the range available to vary an acoustic feature, and in what steps, or resolution, the feature can be controlled within this range. Thus, both resolution and range expand the vocal space and may form a rich 45 substrate for species diversification [8,9]. While the range of an acoustic feature, for example fo, is typically limited by intrinsic constraints of the vocal organ [10-12], the ability 65 ( Fig 1A, B, Table S1, See Methods). The average total number of muscle fibers was 6995 ± 789 (n = 4), corroborating earlier reported ~6730 [17]. The left side had significantly less muscle fibers (3234 ± 232, range: 2992 -3503, n = 4) than right (3794 ± 334, range 3586 -4286, n = 4) (Welch t-test: t = -2.8, df = 5.4, p-value = 0.04). The number of axons in the tracheosyringeal branch of the hypoglossal nerve (NXIIts), assumed to represent the 70 number of MUs (See Methods), was not significantly different between left (820 ± 187, range: 602 -1162, n = 8) and right (790 ± 148, range: 677 -1045, n = 5) (Welch t-test: t = 0.32, df = 10.2, p-value = 0.76) and lower but within range of the 1026 ± 126 (n = 6) reported earlier [18]. The ...

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“…30 31 Introduction 40 Animal behavior results from system-wide interactions between nervous system, muscles, body, and surrounding 41 environment (Chiel and Beer, 1997;Nishikawa et al, 2007). During motor skill learning the brain strives to generate 42 activation patterns to reliably cause behaviors while the body exhibits large changes due to growth and training 43 (Adam and Elemans, 2019). Because of the long extent (months to years) of fine motor skill learning little is known 44 about how motor code changes and how the developing body contributes to behavioral changes.…”

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“…Vocal output is controlled by well-characterized 52 neural circuitry (aka the song system) that consists of two main pathways: i) the anterior forebrain pathway (AFP) 53 necessary to learn and maintain song (Scharff and Nottebohm, 1991) and ii) the motor pathway, which encodes 54 the learned vocalizations and is needed throughout life to produce them. In the avian cortex, the motor pathway 55 produces millisecond-scale precisely-timed complex sequences of motor commands (Chi and Margoliash, 2001;56 Hahnloser et al, 2002) that result in force trajectories by respiratory and superfast vocal muscles (Elemans et al, 57 4 changes (Adam and Elemans, 2019). One change directly influencing the NMT is that force responses of syringeal 66 muscles double in speed when stimulated by single spikes (Mead et al, 2017).…”

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Increasing muscle speed drives changes in the neuromuscular transform of motor commands during postnatal development in songbirds

Adam

Elemans

2020

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15Progressive changes in vocal behavior over the course of vocal imitation leaning are often attributed exclusively 16 to developing neural circuits, but the effects of postnatal body changes remain unknown. In songbirds, the syrinx 17 transforms song system motor commands into sound, and exhibits changes during song learning. Here we test 18 the hypothesis that the transformation from motor commands to force trajectories by syringeal muscles functionally 19 changes over vocal development in zebra finches. Our data collected in both sexes show that only in males, 20 muscle speed significantly increases and that supralinear summation occurs and increases with muscle 21 contraction speed. Furthermore, we show that previously reported sub-millisecond spike timing in the avian cortex 22 Significance statement 32Fine motor skill learning typically occurs in a postnatal period when the brain is learning to control a body that is 33 changing dramatically due to growth and development. How the developing body influences motor code formation 34 and vice versa remains largely unknown. Here we show that vocal muscles in songbirds undergo critical 35 transformations during song learning that drastically change how neural commands are translated into force 36 profiles and thereby acoustic features. We propose that the motor code must compensate for these changes to 37 achieve its acoustic targets. Our data thus support the hypothesis that the neuromuscular transformation changes 38 over vocal development and emphasizes the need for an embodied view of song motor learning. 39 2008; Elemans, 2014). The transform from spikes to force is often referred to as the neuromuscular transform 58 (NMT) (e.g. (Zhurov and Brezina, 2006)). During song, these force trajectories directly modulate pressure in the 59 respiratory system (Srivastava et al., 2017), and the position and tension of vibrating structures in the sound-60 producing organ, the syrinx, thereby altering the vocal output (Riede and Goller, 2010; Elemans, 2014). Thus, via 61 the NMT, motor commands of the song system directly drive the acoustic features of song. 62The changes in song observed over the course of vocal imitation learning are typically attributed to 63 changes in neural drive (Jarvis, 2004; Fitch et al., 2010). However, in this same period the syrinx and particularly 64 the syringeal muscles that execute motor commands from the song system are also undergoing significant 65

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Vocal Motor Performance in Birdsong Requires Brain–Body Interaction

Cited by 18 publications

References 75 publications

High-fidelity continuum modeling predicts avian voiced sound production

High-fidelity continuum modeling predicts avian voiced sound production

One-to-one innervation of vocal muscles allows precise control of birdsong

Increasing muscle speed drives changes in the neuromuscular transform of motor commands during postnatal development in songbirds

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