Biology subjects

Elemans, C. P.

Publications and source records attributed to Elemans, C. P..

11 recordsLinked to original sources

bioRxiv2025

JiSuJi, a virtual muscle for small animal simulations, accurately predicts force from naturalistic spike trains

Physics-based simulators for neuromechanical control of virtual animals have the potential to significantly enhance our understanding of intricate structure-function relationships in neuromuscular systems, their neural activity and motor control. However, a key challenge is the accurate prediction of the forces that muscle fibers produce based on their complex patterns of electrical activity ("spike trains") while preserving model simplicity for broader applicability. In this study, we present a chemomechanical, three-dimensional finite-element muscle model - JiSuJi (pronounced ji su j[i], meaning "ultrafast muscle" in Chinese) - that efficiently and accurately predicts muscle forces from naturalistic spike trains. The models performance is validated against songbird vocal muscles, a particularly fast and therefore challenging muscle type. Our results demonstrate that JiSuJi accurately predicts both isometric and non-isometric muscle forces across a variety of naturalistic neural activity patterns. JiSuJi furthermore outperforms state-of-the-art muscle simulators for accuracy, while maintaining computational efficiency. Simulating muscle behavior offers a promising approach for investigating the underlying mechanisms of neuro-muscular interactions and precise motor control, especially in the fast-contracting muscles of animal model systems.

neuroscience↗

bioRxiv2025

Mechanisms and control of a novel vocalization: the singing mouse song is a whistle that depends on air sac inflation

Identifying variation in vocal morphology and sound production mechanisms is essential to understanding vocal diversity. Rodents provide an ideal system for exploring this variation as they use multiple sound production mechanisms and have novel vocal structures whose morphology varies interspecifically. Here, we describe the laryngeal morphology and identify the sound production mechanism of Alstons singing mouse (Scotinomys teguina), which produce stereotyped songs. We used micro-computed tomography to examine laryngeal morphology and manipulated excised larynges and surgically ablated a laryngeal muscle to determine sound production mechanism and frequency control. Laryngeal manipulations indicated that a whistle mechanism, likely an edge tone or shallow cavity, produces song. Singing mouse whistles are unique compared to other rodents because they rely on the inflation of an enlarged intralaryngeal air sac called the ventral pouch. Whistle frequency can be controlled by ventral pouch inflation, laryngeal airflow, and by cricothyroid muscle action. Cricothyroid ablation inhibited frequency modulation in vivo, suggesting that singing mice use this muscle during singing. Singing mouse laryngeal morphology and vocal mechanism are distinct from other Neotomids; instead of using vocal fold oscillations for loud, long-distance calls and whistles for close-range interactions, singing mice appear to use whistles for distant and close exchanges by inflating their intralaryngeal air sac. Air sacs have evolved repeatedly among vocalizing mammals and our results indicate a new role for these structures in generating sound. Together, our results expand on an emerging story of how biomechanic and morphological variation contributes to vocal diversity.

physiology↗

bioRxiv2025

Zebra finches produce intralaryngeal laminar flow whistles during panting

Birds and mammals converged upon the same physical mechanism of vocal fold vibration to produce their broad range of voiced sounds critical to communication1. The frequency range of vocal fold vibration is limited per species by biophysical constraints to 3-4 octaves2. However, recent work reported vocalizations in zebra finches with apparent fundamental frequencies of 7-11 kHz3 that far exceed the range of regular calls and song (0.5-1.5 kHz)4,5. These "heat" or "incubation" calls are suggested to have close-range communicative relevance in the global temperature rise context3,6, but their acoustics are poorly described and by what biophysical mechanism they are produced remains unknown. We recorded heat calls in adult zebra finches in vivo and show they are extremely soft, frequency-modulated calls with source levels of 13.9 {+/-} 3.3 dB SPL at one meter with dominant frequencies of 6.8 {+/-} 0.6 kHz. Through a series of in vitro experiments, we establish that these calls are aerodynamic whistles produced inside the avian larynx, not syrinx, during inspiration. Respiratory air flow during whistle production is an order of magnitude higher than song and consistent with thermal panting for evaporative cooling6,7. Laryngeal geometry and dimensional flow analysis suggest that these whistles are laminar flow whistles that occur when a flow boundary layer is in a transition phase from laminar to turbulent flows8,9. Birds, like some rodents10-12, are thus able to produce both voiced sounds and aerodynamical whistles in their vocal tract.

physiology↗

bioRxiv2024

Postnatal hearing development limits early parent-to-offspring vocal communication and gates sensorimotor learning in the zebra finch

Acoustic communication relies critically on the receivers ability to hear. In precocial birds, hearing can already be functional during embryonic stages in the egg, whereas in altricial species the limited available data indicate a gradual postnatal development with poor sensitivity in early hatchlings, implying even lower sensitivity in embryos. Recent research suggests that zebra fnnch embryos, despite being altricial, have functional hearing already in the egg to engage in parent-embryo acoustic communication and anthropogenic noise detection. However, their auditory sensitivity during early development remains unknown. Here, we measure auditory brainstem responses (ABR) over early postnatal development and show that zebra fnnch hatchlings have >54 dB lower threshold than adults to loud, broadband clicks. ABR responses emerge between 4-8 days after hatching. Auditory sensitivity develops progressively and reaches adult levels by day 20. Additionally, egg vibrations induced by sound remain far below detection thresholds of vibrotactile senses. Together these data contradict the notion of acoustic perception in embryos and early parent-to-embryo communication in zebra fnnches. The striking timing coincidence between maturation of the peripheral auditory system and the onset of song learning suggests that hearing functionality may gate the onset of vocal learning in zebra fnnches.

physiology↗

bioRxiv2023

Male and female syringeal muscles exhibit superfast shortening velocities in Zebra finches

Vocalisations play a key role in the communication behaviour of many vertebrates. Vocal production requires extremely precise motor control, which is executed by superfast vocal muscles that can operate at cycle frequencies over 100 Hz and up to 250 Hz. The mechanical performance of these muscles has been quantified with isometric performance and the workloop technique, but due to methodological limitations we lack a key muscle property characterising muscle performance, the force-velocity (FV) relationship. Here we establish a method that allows quantification of the FV relationship in extremely fast muscles, and test if the maximal shortening velocity of zebra finch syringeal muscles is different between males and females. We show that syringeal muscles exhibit extremely high maximal shortening velocities of 46 L0 s-1, far exceeding most other vocal and skeletal muscles, and that isometric properties positively correlate with maximal shortening velocities. While male and female muscles differ in isometric speed measures, maximal shortening velocity surprisingly is not sex-dependent. We also show that cyclical methods to measure force-length properties used in classical laryngeal studies give the same result as conventional stepwise methodologies, suggesting either approach is appropriate. Next to force, instantaneous power also trades for speed, further highlighting these muscles are tuned to operate at high frequencies. We argue that the high thermal dependence of superfast vocal muscle performance may impact vocal behaviour. Summary statementZebra finch syringeal muscle exhibits superfast shortening of 46 L0 s-1. Shortening is not sex-specific but correlates with isometric performance - faster twitches and tetani are associated with faster shortening.

zoology↗

bioRxiv2023

Peak performance singing requires daily vocal exercise in songbirds

Vocal signals mediate much of human and non-human communication. Key performance traits - such as repertoire size, speed and accuracy of delivery - affect communication efficacy in fitness-decisive contexts such as mate choice and resource competition1. Specialized fast vocal muscles2,3 are central to accurate sound production4, but it is unknown whether vocal, like limb muscles5,6, need exercise to gain and maintain peak performance7,8. Here, we show that for song development in juvenile songbirds, the closest analogue to human speech acquisition9, regular vocal muscle exercise is crucial to achieve adult peak muscle performance. Furthermore, adult vocal muscle performance reduces within two days of abolishing exercise, leading to downregulation of critical proteins transforming fast to slower muscle fibre types. Daily vocal exercise is thus required to both gain and maintain peak vocal muscle performance, and if absent changes vocal output. We show that conspecifics can detect these acoustic changes and females prefer the song of exercised males. Song thus contains information on recent exercise status of the sender. Daily investment in vocal exercise to maintain peak performance is an unrecognized cost of singing and could explain why many birds sing daily even under adverse conditions10. Because neural regulation of syringeal and laryngeal muscle plasticity is equivalent, vocal output may reflect recent exercise status in all vocalizing vertebrates.

neuroscience↗

bioRxiv2021

Aerodynamics and motor control of ultrasonic vocalizations for social communication in mice and rats

Rodent ultrasonic vocalizations (USVs) are crucial to their social communication and a widely used translational tool for linking gene mutations to behavior. To maximize the causal interpretation of experimental treatments, we need to understand how neural control affects USV production. However, both the aerodynamics of USV production and its neural control remain poorly understood. Here we test three intralaryngeal whistle mechanisms - the wall and alar edge impingement, and shallow cavity tone - by combining in vitro larynx physiology and individual-based 3D airway reconstructions with fluid dynamics simulations. Our results show that in the mouse and rat larynx USVs are produced by a glottal jet impinging on the thyroid inner wall. Furthermore, we implemented an empirically based motor control model that predicts motor gesture trajectories of USV call types. Our work provides a quantitative neuromechanical framework to evaluate the contributions of brain and body in shaping USVs, and a first step in linking descending motor control to USV production.

neuroscience↗

bioRxiv2020

Syringeal vocal folds do not have a voice in zebra finch vocal development

Vocal behaviour can be dramatically changed by both neural circuit development and postnatal maturation of the body. During song learning in songbirds, both the song system and syringeal muscles are functionally changing, but it is unknown if maturation of sound generators within the syrinx contributes to vocal development. Here we densely sample the respiratory pressure control space of the zebra finch syrinx in vitro. We show that the syrinx produces sound very efficiently and that key acoustic parameters, minimal fundamental frequency, entropy and source level, do not change over development in both sexes. Thus, our data suggests that the observed acoustic changes in vocal development must be attributed to changes in the motor control pathway, from song system circuitry to muscle force, and not by material property changes in the avian analog of the vocal folds. We propose that in songbirds, muscle use and training driven by the sexually dimorphic song system are the crucial drivers that lead to sexual dimorphism of the syringeal skeleton and musculature. The size and properties of the instrument are thus not changing, while its player is.

neuroscience↗

bioRxiv2020

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

Progressive changes in vocal behavior over the course of vocal imitation leaning are often attributed exclusively to developing neural circuits, but the effects of postnatal body changes remain unknown. In songbirds, the syrinx transforms song system motor commands into sound, and exhibits changes during song learning. Here we test the hypothesis that the transformation from motor commands to force trajectories by syringeal muscles functionally changes over vocal development in zebra finches. Our data collected in both sexes show that only in males, muscle speed significantly increases and that supralinear summation occurs and increases with muscle contraction speed. Furthermore, we show that previously reported sub-millisecond spike timing in the avian cortex can be resolved by superfast syringeal muscles and that the sensitivity to spike timing increases with speed. Because motor neuron and muscle properties are tightly linked, we make predictions on the boundaries of the yet unknown motor code that correspond well with cortical activity. Taken together, we show that syringeal muscles undergo essential transformations during song learning that drastically change how neural commands are translated into force profiles and thereby acoustic features. We propose that the song system motor code must compensate for these changes to achieve its acoustic targets. Our data thus supports the hypothesis that the neuromuscular transformation changes over vocal development and emphasizes the need for an embodied view of song motor learning. Significance statementFine motor skill learning typically occurs in a postnatal period when the brain is learning to control a body that is changing dramatically due to growth and development. How the developing body influences motor code formation and vice versa remains largely unknown. Here we show that vocal muscles in songbirds undergo critical transformations during song learning that drastically change how neural commands are translated into force profiles and thereby acoustic features. We propose that the motor code must compensate for these changes to achieve its acoustic targets. Our data thus support the hypothesis that the neuromuscular transformation changes over vocal development and emphasizes the need for an embodied view of song motor learning.

neuroscience↗

bioRxiv2020

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

The 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 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% innervating [≤] 3, and 13 - 17% innervating a single muscle fiber. Combined with the lowest specific stress (5 mN/mm2) 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. Furthermore, 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.

neuroscience↗

bioRxiv2019

High-fidelity continuum modeling predicts voiced sound production

Voiced sound production is the primary form of acoustic communication in terrestrial vertebrates, particularly birds and mammals, 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 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 and support the continuum model approach as a critical tool towards a causal model of motor control of voiced sound production.

zoology↗