Franz Goller

• University of Utah

Respiration plays a central role in avian vocal behaviour by providing the airstream that induces vibration of vocal folds. In this role, respiratory movements dictate the coarse temporal pattern of song, while simultaneously fulfilling its vital functions. Whereas these aspects have been investigated in oscines, little information exists in other...

In birds, the sound generated in the syrinx is modified by upper vocal tract filter properties prior to being emitted. Filtering of upper harmonics, for example, allows birds to produce tonal sounds. The main dynamic filter component is the oropharyngeal-esophageal cavity (OEC), whose volume can be adjusted to track the fundamental frequency of mod...

Ducks display a unique and dramatic sexual dimorphism in their vocal organ, the syrinx. Males have a left-sided bulla that is not present in females and that has been long hypothesized to play a role in courtship vocalizations, though this connection has never been tested. The large, hollow morphology of the bulla and its proximity to the sound-pro...

Embryonic morphogenesis is regulated across multiple dimensions. In ducks, the syrinx, the avian vocal organ, undergoes morphogenic processes that result in both left-right asymmetric and sexually dimorphic development. Although these properties are thought to be controlled by the NODAL-PITX2 left-right signaling cascade and the sex steroid pathway...

Sleep replay activity involves the reactivation of brain structures with patterns similar to those observed during waking behavior. In this study, we demonstrate that adult male canaries exhibit spontaneous, song-like peripheral reactivation during night sleep. Our findings include: (1) the presence of activity in respiratory muscles, leading to so...

The acquisition of an acoustic template is a fundamental component of vocal imitation learning, which is used to refine innate vocalizations and develop a species-specific song. In the absence of a model, birds fail to develop species typical songs. In zebra finches (Taeniopygia guttata), tutored birds produce songs with a stereotyped sequence of d...

Birds contribute prominently to the terrestrial soundscapes on Earth. The sounds can arise from different sources, such as drumming by woodpeckers, bill clapping by storks or feather vibrations in the courtship flights of snipes and hummingbirds. However, most avian sounds are generated in the avian vocal organ, the syrinx. Vocal behavior is used i...

Many birds emit tonal song syllables even though the sound sources generate sound with rich upper harmonic energy content. This tonality is thought to arise in part from dynamically adjusted filtering of harmonic content. Here, we compare tonality of song syllables between vocal learners and non-learners to assess whether this characteristic is lin...

Androgens mediate the expression of many reproductive behaviors, including the elaborate displays used to navigate courtship and territorial interactions. In some vertebrates, males can produce androgen-dependent sexual behavior even when levels of testosterone (T) is low in the bloodstream. One idea is that select tissues make their own androgens...

We present a dynamical model for the avian respiratory system and report the measurement of its variables in normal breathing canaries (Serinus canaria). Fitting the parameters of the model, we are able to show that the birds in our study breathe at an aerodynamic resonance of their respiratory system. For different respiratory regimes, such as sin...

During vertical climbing, the gravitational moment tends to pitch the animal's head away from the climbing surface and this may be countered by 1) applying a correcting torque at a discrete contact point, or 2) applying opposing horizontal forces at separate contact points to produce a free moment. We tested these potential strategies in small parr...

Nerves and muscle interact to perform learned motor behavior such as birdsong. Glycosaminoglycans play a major role in the function of muscle as well as the formation and function of the neuromuscular junction. The alteration of GAG chains provides a unique opportunity to alter muscle behavior and thus motor control of a behavior. This chapter prov...

Activation of forebrain circuitry during sleep has been variably characterized as ‘pre- or replay’ and has been linked to memory consolidation. The evolutionary origins of this mechanism, however, are unknown. Sleep activation of the sensorimotor pathways of learned birdsong is a particularly useful model system because the muscles controlling the...

Abstract During secondary contact between two species when hybrids are less fit than parents, mating signals are expected to diverge, while aggressive signals are expected to converge. If a single signal trait is used in both mating and aggression, then the dynamics between these two forces could influence the evolutionary trajectory of that trait....

Birdsong is an important signal used in intra- and intersexual communication in a reproductive context. Strong sexual and natural selective forces act on this behaviour, such that singing individuals can be viewed as vocal athletes whose performance is critical for reproductive success. In this review, I argue and illustrate how a solid understandi...

• Birdsong is used in reproductive context and, consequently, has been shaped by strong natural and sexual selection. The acoustic performance includes a multitude of acoustic and temporal characteristics that are thought to honestly reveal the quality of the singing individual. • One major song feature is frequency and its modulation. Sound freque...

The complex vocalizations found in different bird species emerge from the interplay between morphological specializations and neuromuscular control mechanisms. In this work we study the dynamical mechanisms used by a nonlearner bird from the Americas, the suboscine Pitangus sulphuratus, in order to achieve a characteristic timbre of some of its voc...

Songbirds produce complex vocalizations by coordinating neuromuscular control of syrinx, respiratory system and upper vocal tract. The functional roles of syringeal muscles have been documented mainly with correlative data, which have suggested that synergistic activation plays a role in the fine control of vocal features. However, the specific inv...

Performance trade-offs can dramatically alter an organism's evolutionary trajectory by making certain phenotypic outcomes unattainable. Understanding how these trade-offs arise from an animal's design is therefore an important goal of biology. To explore this topic, we study how androgenic hormones, which regulate skeletal muscle function, influenc...

In this work we study the sound production mechanism of the raspy sounding song of the white-tipped plantcutter (Phytotoma rutila), a species with a most unusual vocalization. The biomechanics involved in the production of this song, and scaling arguments, allowed us to predict the precise way in which body size is encoded in its vocalizations. We...

The gonads (testes) act as the primary organ where androgenic hormones are made to regulate reproductive behavior in male vertebrates. Yet many endocrinologists have also long suspected that other tissues in the body can autonomously synthesize their own androgens to support behavioral output. We examine this idea here by studying whether avian ske...

Studies of avian vocal development without exposure to conspecific song have been conducted in many passerine species, and the resultant isolate song is often interpreted to represent an expression of the genetic code for conspecific song. There is wide recognition that vocal learning exists in oscine songbirds, but vocal learning has only been tho...

The unique avian vocal organ, the syrinx, is located at the caudal end of the trachea. Although a larynx is also present at the opposite end, birds phonate only with the syrinx. Why only birds evolved a novel sound source at this location remains unknown, and hypotheses about its origin are largely untested. Here, we test the hypothesis that the sy...

First and second formants of the physical model can be estimated using the equation [(2n − 1) × c]/(4 × tube length), in which c is speed of sound (350 m/s) and n is the respective resonance frequency. The vocal fold model was coupled with 18 different tracheal lengths. The length of the tracheal tubes were chosen so that the first resonance was ei...

Predictive value of BM for F0. BM, body mass; F0, fundamental frequency. (DOCX)

Excel spreadsheet containing, in separate sheets, the underlying numerical data for Figs 2A, 2B, 2C, 2D, 3A, 3B, 3C, 3D, 3E, 3F, 4A, 4B and 4C. (XLSX)

Physiology's role in speciation is poorly understood. Motor systems, for example, are widely thought to shape this process because they can potentiate or constrain the evolution of key traits that help mediate speciation. Previously, we found that Neotropical manakin birds have evolved one of the fastest limb muscles on record to support innovation...

In its most basic conception, a novelty is simply something new. However, when many previously proposed evolutionary novelties have been illuminated by genetic, developmental, and fossil data, they have refined and narrowed our concept of biological "newness." For example, they show that these novelties can occur at one or multiple levels of biolog...

Significance The study of the integration between sensory inputs and motor commands has greatly benefited from the finding that in sleeping oscine birds, playback of their own song evokes highly specific firing patterns in neurons also involved in the production of that song. Nevertheless, the sparse spiking patterns that can be recorded from few s...

Birdsong production involves the simultaneous and precise control of a set of muscles that change the configuration and dynamics of the vocal organ. Although it has been reported that each one of the different muscles is primarily involved in the control of one acoustic feature, recent advances have shown that they act synergistically to achieve th...

Behavior emerges from the interaction between the nervous system and peripheral devices. In the case of birdsong production, a delicate and fast control of several muscles is required to control the configuration of the syrinx (the avian vocal organ) and the respiratory system. In particular, the syringealis ventralis muscle is involved in the cont...

Acquisition and maintenance of complex vocal behaviors like human speech and oscine birdsong require continuous auditory feedback. The exact way in which this feedback is integrated into the vocal motor programs is not completely understood. Here we show that in sleeping zebra finches ( Taeniopygia guttata ), the activity of the song system selecti...

Brain activity during sleep is fairly ubiquitous and the best studied possible function is a role in memory consolidation, including motor memory. One suggested mechanism of how neural activity effects these benefits is through reactivation of neurons in patterns resembling those of the preceding experience. The specific patterns of motor activatio...

Each syringeal half is controlled by six muscles, two extrinsic (blue labels: m. sternotrachealis, ST, m. tracheolateralis, TL,) and 4 intrinsic (black labels) muscles The four intrinsic muscles are the ventral syringeal (vS), the ventral tracheobronchial (vTB), the dorsal tracheobronchial (dTB) and the dorsal syringeal (dS) muscles. EMG recordings...

Recorded muscles for each bird

Average occurrence of each SLA type with standard error

Many species perform elaborate physical displays to court mates and compete with rivals, but the biomechanical mechanisms underlying such behavior are poorly understood. Here we address this issue by studying the neuromuscular origins of display behavior in a small tropical passerine bird called the golden-collared manakin (Manacus vitellinus). Mal...

In the brain, the extracellular matrix (ECM) plays a central role during neural development and thus modulates critical-period regulated behavioral ontogeny. The major components of the ECM are glycosaminoglycans (GAGs) including chondroitin sulfate (CS). However, the specific roles of GAGs in behavioral development are largely unknown. It has been...

Steroid hormone action in the brain regulates many animals’ elaborate social displays used for courtship and competition, but it is increasingly recognized that the periphery may also be a site for potent steroidal modulation of complex behavior. However, the mechanisms of such “bottom up” regulation of behavioral outflow are largely unclear. To st...

The evolution of complex behavior is driven by the interplay of morphological specializations and neuromuscular control mechanisms [1-3], and it is often difficult to tease apart their respective contributions. Avian vocal learning and associated neural adaptations are thought to have played a major role in bird diversification [4-8], whereas funct...

The avian vocal organ, the syrinx, is located at the base of the trachea and is controlled by 4 intrinsic pairs of muscles, ventral and dorsal tracheobronchial and ventral and dorsal syringeal muscles. These muscles facilitate active regulation of airflow and sound features, and show exceptionally fast contraction kinetics, stemming from superfast...

From complex songs to simple honks, squawks, or caws, birds produce sounds using a unique vocal organ, the syrinx. Located close to the heart at the tracheobronchial junction, vocal folds or membranes attached to modified mineralized rings vibrate to produce sound. Not thought to commonly enter the fossil record, the few reported fossilized parts o...

New & noteworthy: It is largely unknown how fine motor control of acoustic parameters is achieved in vocal organs. Subtle manipulation of syringeal muscle function was used to test how active motor control influences acoustic parameters. Slowed activation kinetics of muscles reduced frequency modulation and, unexpectedly, caused a distinct decreas...

The vocal behavior of birds is remarkable for its diversity, and songs can feature elaborate characteristics such as long duration, rapid temporal pattern, and broad frequency range. The respiratory system plays a central role in generating the complex song patterns that must be integrated with its life-sustaining functions. Here, we explore how pr...

From complex songs to simple honks, birds produce sounds using a unique vocal organ called the syrinx. Located close to the heart at the tracheobronchial junction, vocal folds or membranes attached to modified mineralized rings vibrate to produce sound. Syringeal components were not thought to commonly enter the fossil record, and the few reported...

Most birds vocalize with an open beak, but vocalization with a closed beak into an inflating cavity occurs in territorial or courtship displays in disparate species throughout birds. Closed-mouth vocalizations generate resonance conditions that favor low-frequency sounds. By contrast, open-mouth vocalizations cover a wider frequency range. Here we...

Mean percent recoveries of the main wing muscles at different stimulation frequencies (see Materials and methods) across all species.DOI: http://dx.doi.org/10.7554/eLife.13544.007

ELife digest Many animals court mates and fight with rivals by performing physically elaborate and showy displays. From male fiddler crabs waving their claws to attract females, to the leaping dances of whooping cranes, these displays often involve remarkably fast limb movements. However, in many cases it is puzzling how animals can perform these b...

Song production in songbirds is controlled by a network of nuclei distributed across several brain regions, which drives respiratory and vocal motor systems to generate sound. We built a model for birdsong production, whose variables are the average activities of different neural populations within these nuclei of the song system. We focus on the p...

The Pectoral Sandpiper (Calidris melanotos) is one of a few highly polygynous shorebirds with strong sexual size dimorphism. The vocal part of the male courtship display has received some attention, but how the sound is generated is largely unknown. To fill this gap, we analyzed video and sound recordings collected on the breeding grounds at Barrow...

Animal activities, such as foraging and reproduction, are constrained by decisions about how to allocate energy and time efficiently. Overall, male moths invest less in reproduction than females, but they are thought to engage in a scramble competition for access to females that advertise readiness to mate by releasing sexual pheromones. However, b...

Ectotherms can attain preferred body temperatures by selecting specific temperature microhabitats within a varied thermal environment. The side-blotched lizard, Uta stansburiana may employ microhabitat selection to thermoregulate behaviorally. It is unknown to what degree habitat structural complexity provides thermal microhabitats for thermoregula...

Acoustic properties of vocalizations arise through the interplay of neural control with the morphology and biomechanics of the sound generating organ, but in songbirds it is assumed that the main driver of acoustic diversity is variation in telencephalic motor control. Here we show, however, that variation in the composition of the vibrating tissue...

Frequency modulation is a salient acoustic feature of birdsong. Its control is usually attributed to the activity of syringeal muscles, which affect the tension of the labia responsible for sound production. We use experimental and theoretical tools to test the hypothesis that for birds producing tonal sounds such as domestic canaries (Serinus cana...

At low ambient temperature Helicoverpa zea male moths engage in warm-up behavior prior to taking flight in response to an attractive female pheromone blend. Male H. zea warm up at a faster rate when sensing the attractive pheromone blend compared to unattractive blends or blank controls (Crespo et al. 2012), but the mechanisms involved in this olfa...

Unidirectional, continuous airflow through the avian lung is achieved through an elaborate air sac system with a sequential, posterior to anterior ventilation pattern. This classical model was established through various approaches spanning passively ventilated systems to mass spec analysis of tracer gas flow into various air sacs during spontaneou...

The nature of telencephalic control over premotor and motor circuits is debated. Hypotheses range from complete usurping of downstream circuitry to highly interactive mechanisms of control. We show theoretically and experimentally, that telencephalic song motor control in canaries is consistent with a highly interactive strategy. As predicted from...

Temperature calibrations of dura surface for the six cooling devices of our experiment right after implantation. Previous calibrations with the same devices in unsuccessful subjects that did not sing are included. Calibrations were divided in two groups: the devices that were used by birds that broke syllables (N = 12) and the ones used by the bird...

Histograms of syllable duration at different HVC temperatures of three canaries that showed broken syllables. Syllables were divided into three groups depending on the number of local minima between two consecutive inspirations. In red we define syllables that are reminiscent of harmonic oscillations, with no minima (first column). Green is used fo...

Individual statistics for broken syllables labeled with “y” as in Figure 2C. These frequently sung syllables present a pattern that could be followed across temperatures. Although they could be further classified in two types (shaded and previous syllable in Figure 2C are slightly different with respect to the three syllables following them), this...

Individual statistics for broken syllable “x”, as labeled in Figure 2C. This common syllable presents a pattern that could be followed across temperatures. (A) Paired panels of sonogram (top, 1–7 kHz) and pressure gestures (bottom, 0–1 a.u.) present on top the syllable at normal temperature and below, the syllable found at −4.7°C. The syllable brea...

The cooling device. (A) Top and side view of a Peltier piece cut from a commercial Thermoelectric Cooler (HB corporation, TEC1-12706) with a Low Speed Diamond Wheel Saw. Its dimensions are 1 cm×1 cm with 4 mm height in thicker part (0.7 g). Only four semiconductor elements were kept and a thin ceramic region for the cool side. Thin wires (Alpha Wir...

Histograms of syllable duration at different HVC temperatures for three canaries that did not show broken syllables. Syllables are divided into 3 groups as specified in Figure S3. Distributions only shift to the right since syllables only get longer with decreasing temperature. (A) Canary #28. Total syllables analyzed are 4161 red, 1033 green and 8...

The courtship and dominance behavior of brown-headed cowbirds (Molothrus ater) consists of a multi-modal display, including song as well as postural and wing movements. The temporal sequences of the acoustic and the visual display are coordinated. In adult male cowbirds the largest wing movements of the display are synchronized with silent periods...

One major feature of the remarkable vocal repertoires of birds is the range of fundamental frequencies across species, but also within individual species. This review discusses four variables that determine the oscillation frequency of the vibrating structures within a bird's syrinx. These are (1) viscoelastic properties of the oscillating tissue,...

Vocal production in songbirds requires the control of the respiratory system, the syrinx as sound source and the vocal tract as acoustic filter. Vocal tract movements consist of beak, tongue and hyoid movements, which change the volume of the oropharyngeal-esophageal cavity (OEC), glottal movements and tracheal length changes. The respective contri...

An essential part of sexual reproduction typically involves the identification of an appropriate mating partner. Males of many moth species utilize the scent of sex pheromones to track and locate conspecific females. However, before males engage in flight, warm-up by shivering of the major flight muscles is necessary to reach a thoracic temperature...

Because of the parallels found with human language production and acquisition, birdsong is an ideal animal model to study general mechanisms underlying complex, learned motor behavior. The rich and diverse vocalizations of songbirds emerge as a result of the interaction between a pattern generator in the brain and a highly nontrivial nonlinear peri...

The mechanisms by which telencephalic areas affect motor activities are largely unknown. They could either take over motor control from downstream motor circuits or interact with the intrinsic dynamics of these circuits. Both models have been proposed for telencephalic control of respiration during learned vocal behavior in birds. The interactive m...

It is well established that there are remarkable similarities between song learning in oscine birds and acquisition of speech in young children. Human speech shows marked changes with senescence, but few studies have evaluated how song changes with advanced age in songbirds. To investigate the effect of old age on song, we compared song of old Beng...

Sexually dimorphic vocal behavior in zebra finches (Taeniopygia guttata) is associated with a 100% larger syrinx in males and other morphological adaptations of the sound source. The songbird syrinx consists of two independent sound sources, whose specialization for different spectral ranges may be reflected in morphological properties, but the mor...

Highlights ► We address methodological problems in Cardoso & Atwell (2011, Animal Behaviour, 82, 831–836). ► We illustrate common problems with taking acoustic measurements from spectrograms. ► Reliable amplitude measurements require calibrated and controlled recordings. ► We explain the interrelationship of frequency and amplitude in animal vocali...

We reconstruct the physiological parameters that control an avian vocal organ during birdsong production using recorded song. The procedure involves fitting the time dependent parameters of an avian vocal organ model. Computationally, the model is implemented as a dynamical system ruling the behavior of the oscillating labia that modulate the air f...

The production of vocalizations is intimately linked to the respiratory system. Despite our understanding of neural circuits that generate normal respiratory patterns, very little is understood regarding how these pontomedullary circuits become engaged during vocal production. Songbirds offer a potentially powerful model system for addressing this...

Bird song is a widely used model in the study of animal communication and sexual selection, and several song features have been shown to reflect the quality of the singer. Recent studies have demonstrated that song amplitude may be an honest signal of current condition in males and that females prefer high amplitude songs. In addition, birds raise...

In songbirds, the ontogeny of singing behavior shows strong parallels with human speech learning. As in humans, development of learned vocal behavior requires exposure to an acoustic model of species-typical vocalizations, and, subsequently, a sensorimotor practice period after which the vocalization is produced in a stereotyped manner. This requir...

Coordination of different motor systems for sound production involves the use of feedback mechanisms. Song production in oscines is a well-established animal model for studying learned vocal behavior. Whereas the online use of auditory feedback has been studied in the songbird model, very little is known about the role of other feedback mechanisms....

Like human infants, songbirds acquire their song by imitation and eventually generate sounds that result from complicated neural networks and intrinsically nonlinear physical processes. Signatures of low-dimensional chaos such as subharmonic bifurcations have been reported in adult and developing zebra finch song. Here, we use methods from nonlinea...

Vocal learning, a key behavior in human speech development, occurs only in a small number of animal taxa. Ontogeny of vocal behavior in humans and songbirds involves acquisition of an acoustic model, which guides the development of self-generated vocalizations (sensorimotor period). How vocal development proceeds in the absence of an acoustic model...

Female zebra finch syrinx frontal sections (H&E stain) in ventral aspect of the organ. A: Schematic external ventral view of the excised organ in the upper part and of a frontal section of the syrinx (at mid-organ level indicated by the vertical plate in the upper part). The dotted square indicates the aspect that is shown in B through G. TL, trach...

A female zebra finch syrinx frontal section stained with alcian blue before (A) and after Hyaluronidase digestion (B). Pessulus (P), medial labium (ML), medial tympaniform membrane (MTM), lateral labium (LL), the second and third bronchial half ring (A2, A3), bronchial ring (B). Bars are 100 µm. (8.97 MB TIF)

Female zebra finch syrinx frontal sections (H&E stain). A: Section come from the ventral aspect of the syrinx, B: from mid-organ and C: from the dorsal syrinx. Pessulus (P), medial labium (ML), medial tympaniform membrane (MTM), lateral labium (LL), the first, second and third bronchial half ring (A1, A2, A3), interclavicular air sac (ICAS). Bars a...

A and B: Frontal section area measurements of medial (ML) and lateral labia (LL) in female syringes. Squares (left syrinx) and triangles (right syrinx) indicate means (error bars are standard deviation). C and D: Cranio-caudal length of the medial labium (ML) and the medial tympaniform membrane (MTM). Squares (left syrinx) and diamonds (right syrin...

Results: The histological composition of the labia as well as the dorso-ventral and left-right asymmetry of the syrinx comparing males and females. (0.03 MB DOC)

Masson's Trichrome stain of a zebra finch syrinx cross section. A: Section of a female syrinx showing the pessulus (P), medial labium (ML), medial tympaniform membrane (MTM) and first bronchial cartilage ring (B1). The square indicates the location of the higher magnification image in B and C. B: Part of the medial labium at larger magnification fr...

Elastica-van-Giesson stain of a zebra finch syrinx frontal section. A: Section of a female syrinx showing the pessulus (P), medial labium (ML), medial tympaniform membrane (MTM), lateral labium (LL), the second and third bronchial half ring (A2, A3), and the first bronchial ring (B1). The squares indicate the location of the higher magnification im...

In many songbirds the larger vocal repertoire of males is associated with sexual dimorphism of the vocal control centers and muscles of the vocal organ, the syrinx. However, it is largely unknown how these differences are translated into different acoustic behavior. Here we show that the sound generating structures of the syrinx, the labia and the...

Syntactical cues play an important role in song learning in songbirds. White-crowned sparrows (Zonotrichia leucophrys), whose song typically consists of four to five different phrases, fail to construct normal songs if exposed to all phrase types presented singly (Plamondon, Goller, & Rose, 2008; Soha & Marler 2001b). The specific role of acquired...

DOI:https://doi.org/10.1103/PhysRevE.81.049905

The songbird vocal organ, the syrinx, is composed of two sound generators, which are independently controlled by sets of two extrinsic and four intrinsic muscles. These muscles rank among the fastest vertebrate muscles, but the molecular and morphological foundations of this rapid physiological performance are unknown. Here we show that the four in...

Optical techniques in conjunction with fluorescent markers have revolutionized the investigation of dynamical cellular processes, such as studies of calcium ion (Ca^2+) dynamics in muscles. Recently, it was shown that songbirds have superfast syringeal muscles, which can modulate song acoustics up to 250 Hz. Such rapid contraction cycles most likel...

In this work, we build an electronic syrinx, i.e., a programmable electronic device capable of integrating biomechanical model equations for the avian vocal organ in order to synthesize song. This vocal prosthesis is controlled by the bird's neural instructions to respiratory and the syringeal motor systems, thus opening great potential for studyin...