Role of syringeal muscles in controlling the phonology of bird song
TL;DR: Variation in the phase relationship between AM and EMG bursts during oscillatory airflow suggests complex biomechanical interaction between antagonistic muscles.
Abstract: 1. The contribution of syringeal muscles to controlling the phonology of song was studied by recording bilateral airflow, subsyringeal air sac pressure, electromyograms (EMGs) of six syringeal muscles, and vocal output in spontaneously singing brown thrashers (Toxostoma rufum). 2. EMG activity in musculus syringealis ventralis (vS), the largest syringeal muscle, increases exponentially with the fundamental frequency of the ipsilaterally generated sound and closely parallels frequency modulation. 3. The EMG activity of other syringeal muscles is also positively correlated with sound frequency, but the amplitude of their EMGs changes only a small amount compared with variation in the amplitude of their EMGs correlated with changing syringeal resistance. The elevated activity in all syringeal muscles during high-frequency sounds may reflect an increased need for structural stability during the strong contractions of the largest syringeal muscle (vS). 4. Several syringeal mechanisms are used to generate amplitude modulation (AM). The most common of these involves modulating the rate of syringeal airflow, through activity by adductor (m. syringealis dorsalis and m. tracheobronchialis dorsalis) and abductor (m. tracheobronchialis ventralis) muscles, which change syringeal resistance, switch sound production from one side of the syrinx to the other, or produce rapid oscillatory flow changes. Variation in the phase relationship between AM and EMG bursts during oscillatory airflow suggests complex biomechanical interaction between antagonistic muscles. 5. AM can also arise from acoustic interactions of two independently generated sounds (beat notes) including cross talk signals between the two syringeal halves. In this latter mechanism, sound generated on one side radiates slightly out of phase with the source from the contralateral side, resulting in lateralized AM generation.
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TL;DR: Human speech and birdsong have numerous parallels, with striking similarities in how sensory experience is internalized and used to shape vocal outputs, and how learning is enhanced during a critical period of development.
Abstract: Human speech and birdsong have numerous parallels. Both humans and songbirds learn their complex vocalizations early in life, exhibiting a strong dependence on hearing the adults they will imitate, as well as themselves as they practice, and a waning of this dependence as they mature. Innate predispositions for perceiving and learning the correct sounds exist in both groups, although more evidence of innate descriptions of species-specific signals exists in songbirds, where numerous species of vocal learners have been compared. Humans also share with songbirds an early phase of learning that is primarily perceptual, which then serves to guide later vocal production. Both humans and songbirds have evolved a complex hierarchy of specialized forebrain areas in which motor and auditory centers interact closely, and which control the lower vocal motor areas also found in nonlearners. In both these vocal learners, however, how auditory feedback of self is processed in these brain areas is surprisingly unclear. Finally, humans and songbirds have similar critical periods for vocal learning, with a much greater ability to learn early in life. In both groups, the capacity for late vocal learning may be decreased by the act of learning itself, as well as by biological factors such as the hormones of puberty. Although some features of birdsong and speech are clearly not analogous, such as the capacity of language for meaning, abstraction, and flexible associations, there are striking similarities in how sensory experience is internalized and used to shape vocal outputs, and how learning is enhanced during a critical period of development. Similar neural mechanisms may therefore be involved.
1,519 citations
TL;DR: The results demonstrate that both dietary restriction and elevated corticosterone levels significantly reduced nestling growth rates and that experimentally stressed birds developed songs with significantly shorter song motif duration and reduced complexity.
337 citations
TL;DR: Song production in birds involves the intricate coordination of at least three major groups of muscles: namely, those of the syrinx, the respiratory apparatus, and the upper vocal tract, including the jaw.
Abstract: As in humans, song production in birds involves the intricate coordination of at least three major groups of muscles: namely, those of the syrinx, the respiratory apparatus, and the upper vocal tract, including the jaw. The pathway in songbirds that controls the syrinx originates in the telencephalon and projects via the occipitomesencephalic tract directly upon vocal motoneurons in the medulla. Activity in this pathway configures the syrinx into phonatory positions for the production of species typical vocalizations. Another component of this pathway mediates control of respiration during vocalization, since it projects upon both expiratory and inspiratory groups of premotor neurons in the ventrolateral medulla, as well as upon several other nuclei en route. This pathway appears to be primarily involved with the control of the temporal pattern of song, but is also importantly involved in the control of vocal intensity, mediated via air sac pressure. There are extensive interconnections between the vocal and respiratory pathways, especially at brain-stem levels, and it may be these that ensure the necessary temporal coordination of syringeal and respiratory activity. The pathway mediating control of the jaw appears to be different from those mediating control of the syrinx and respiratory muscles. It originates in a different part of the archistriatum and projects upon premotor neurons in the medulla that appear to be separate from those projecting upon the syringeal motor nucleus. The separateness of this pathway may reflect the imperfect correlation of jaw movements with the dynamic and acoustic features of song. The brainstem pathways mediating control of vocalization and respiration in songbirds have distinct similarities to those in mammals such as cats and monkeys. However, songbirds, like humans, but unlike most other non-songbirds, have developed a telencephalic vocal control system for the production of learned vocalizations.
264 citations
TL;DR: The data indicate that the metabolic cost of song production in the songbird species studied is no higher than that for other types of vocal behavior in various bird groups, and is also similar to that of calling in frogs and of human speech production.
Abstract: The metabolic cost of birdsong production has not been studied in detail but is of importance in our understanding of how selective pressures shape song behavior. We measured rates of oxygen consumption during song in three songbird species, zebra finches (Taeniopygia guttata), Waterslager canaries (Serinus canaria) and European starlings (Sturnus vulgaris). These species sing songs with different acoustic and temporal characteristics: short stereotyped song (zebra finch), long song with high temporal complexity (canary) and long song with high acoustic, but low temporal, complexity (starling). In all three species, song slightly increased the rate of oxygen consumption over pre-song levels (1.02-1.36-fold). In zebra finches, the metabolic cost per song motif averaged 1.2 microl g(-1). This cost per motif did not change over the range of song duration measured for the four individuals. Surprisingly, the metabolic cost of song production in the species with the temporally most complex song, the canary, was no greater than in the other two species. In starlings, a 16 dB increase in sound intensity was accompanied by a 1.16-fold increase in the rate of oxygen consumption. These data indicate that the metabolic cost of song production in the songbird species studied is no higher than that for other types of vocal behavior in various bird groups. Our analysis shows that the metabolic cost of singing is also similar to that of calling in frogs and of human speech production. However, difficulties with measurements on freely behaving birds in a small respirometry chamber limit the depth of analysis that is possible.
256 citations
Cites background from "Role of syringeal muscles in contro..."
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...In contrast, the syrinx is typically abducted (m. tracheobronchialis ventralis) to maximize inspiratory airflow during minibreaths (e.g. Goller and Suthers, 1996a)....
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TL;DR: It is suggested that song is driven by a dynamic circuit that operates on a single underlying clock, and that the large convergence of RA neurons to vocal control muscles results in a many-to-one mapping of RA activity to song structure.
Abstract: Zebra finch song is represented in the high-level motor control nucleus high vocal center (HVC) (Reiner et al., 2004) as a sparse sequence of spike bursts. In contrast, the vocal organ is driven continuously by smoothly varying muscle control signals. To investigate how the sparse HVC code is transformed into continuous vocal patterns, we recorded in the singing zebra finch from populations of neurons in the robust nucleus of arcopallium (RA), a premotor area intermediate between HVC and the motor neurons. We found that highly similar song elements are typically produced by different RA ensembles. Furthermore, although the song is modulated on a wide range of time scales (10-100 ms), patterns of neural activity in RA change only on a short time scale (5-10 ms). We suggest that song is driven by a dynamic circuit that operates on a single underlying clock, and that the large convergence of RA neurons to vocal control muscles results in a many-to-one mapping of RA activity to song structure. This permits rapidly changing RA ensembles to drive both fast and slow acoustic modulations, thereby transforming the sparse HVC code into a continuous vocal pattern.
208 citations
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TL;DR: Central nervous pathways controlling bird son in the canary are traced using a combination of behavioral and anatomical techniques and direct connections were found onto the cells of the motor nucleus innervating the syrinx, the organ of song production.
Abstract: We have traced central nervous pathways controlling bird son in the canary using a combination of behavioral and anatomical techniques. Unilateral electrolytic brain lesions were made in adult male canaries whose son had been previously recorded and analysed on a sound spectrograph. After severral days of postoperative recording, the birds were sacrificed and their brains processed histologically for degeneration staining with the Fink-Heimer technique. Although large lesions in the neostriatum and rostral hyperstriatum had no effect on song, severe song deficits followed damage to a discrete large-celled area in the caudal hyperstriatum ventrale (HVc). Degenerating fibers were traced from this region to two other discrete nuclei in the forebrain: one in the parolfactory lobe (area X, a teardrop-shaped small-celled nucleus) and a round large-celled nucleus in the archistriatum (RA). Unilateral lesions of X had no effect on song; lesions of RA, however, caused severe song deficits. Degenerating fibers from RA joined the occipitomesencephalic tract and had widespread ipsilateral projections to the thalamus, nucleus intercollicularis of the midbrain, reticular formation, and medulla. It is of particular interest that direct connections were found onto the cells of the motor nucleus innervating the syrinx, the organ of song production. Unilateral lesions of n. intercollicularis (previously implicated in the control of vocal behavior) had little effect on song.
One bilateral lesion of HVc resulted in permanent (9 months) and complete elimination of the audible components of song, although the bird assumed the posture and movements typical of song. Preliminary data suggest that lesions of the left hemisphere result in greater deficits than lesions of the right one. This finding is consistent with earlier reports that the left syrinx controls the majority of song components. Results reported here suggest a localization of vocal control in the canary brain with an overlying left hemispheric dominance.
1,664 citations
TL;DR: This review shall examine critically the major current issues and ideas in this field, placing special emphasis on the topics related to the development, learning, and neural control of song.
Abstract: The study of birdsong has made significant contributions to the development of modern ethology. Concepts such as species-specificity in animal signals, innate predisposition in learning, and sensory templates for motor development were put forth first in birdsong research (Marler 1957, 1 964, Konishi 1965b, Hinde 1982). Also, it was the study of song development that elevated the much debated issue of instinct versus learning from the realm of semantic discourse and confusion to an experimentally tractable subject (Marler 1983). The recent discovery of neural substrates for song has introduced a new dimension to the study of birdsong, making integration of behavioral and neurobiological studies feasible (Nottebohm et aI1976). Neurobiological concepts and methods are now directly applicable to this field. This integrated approach can address not only some of the outstanding issues that arose in behavioral studies and that are refractory to further behavioral analysis, but it also makes birdsong an attractive subject for the study of such basic issues as
neural coding, learning, memory, developmental plasticity, and sensorimotor coordination. In this review I shall examine critically the major current issues and ideas in this field, placing special emphasis on the topics related to the development, learning, and neural control of song. Because extensive listings and reviews of recent literature on birdsongs are available (Kroodsma & Miller 1982a,b), the references cited are limited to those essential for the discussion of facts and theories on selected topics.
479 citations
TL;DR: It is suggested that the learned features of oscine songbird vocalizations are controlled by a telencephalic pathway that acts in concert with other pathways responsible for simpler, unlearned vocalizations.
Abstract: Male zebra finches sing, females do not. However, both sexes produce the “long call”when placed in visual isolation. This call is sexually dimorphic; it includes learned components in males but not in females. The 3 learned features of the male long call are a high fundamental frequency, a fast frequency modulation, and a short, stable duration. These features are learned by the male during development, as is song. Since similar features are also found in song syllables, we wanted to know whether long-call production depends on the same CNS pathway that controls song production. Three critical components of the song pathway are telencephalic nuclei HVC, RA, and the tracheosyringeal (ts) nerves innervating the syrinx. In male zebra finches, bilateral section of the ts nerves affected the fundamental frequency and fast frequency modulations of both the long call and song but left the temporal features intact. Ts nerve section had no effect on the female long call. Bilateral lesions of either HVC or RA in males affected the fundamental frequency, fast frequency modulations, and temporal structure of both the long call and song. Similar lesions had no effect on the female long call. These results demonstrate that HVC, RA, and the ts nerves make critical contributions to the acoustic features of the male long call and song, while the temporal pattern depends on HVC and RA but not the ts nerves. HVC and RA lesions remove all the learned features that distinguish the male call and reveal a simple unlearned vocalization shared by both sexes. We suggest that the learned features of oscine songbird vocalizations are controlled by a telencephalic pathway that acts in concert with other pathways responsible for simpler, unlearned vocalizations.
368 citations
TL;DR: The study of the motor control system for birdsong has provided the most direct evidence to date for localizing the programming of a skilled motor sequence to the telencephalon and the observation that unilateral forebrain perturbation was sufficient to alter the pattern of this bilaterally organized behavior suggests that (non-auditory) feedback pathways to the forebrain exist to coordinate the two hemispheres during singing.
Abstract: The stereotyped delivery of sequences of vocalizations by singing zebra finches is thought to be mediated by a “central motor program.” We hypothesized that electrically stimulating, and thus perturbing, the neural components of this motor program during singing should alter the subsequent singing pattern. In contrast, perturbing the activity of other neurons in the song motor pathway that do not participate directly in generating the song temporal pattern should not affect the singing pattern. We found that unilaterally stimulating the forebrain area RA of singing birds with chronically implanted electrodes distorted ongoing syllables without changing the order or timing of ensuing syllables. However, stimulating forebrain area HVc, which projects directly to RA, altered both ongoing syllables and the ensuing song pattern. These findings indicate that syllable sequencing during singing is organized in forebrain areas above RA (including HVc) and that the resulting pattern is imposed on lower structures of the motor pathway. Furthermore, the observation that unilateral forebrain perturbation was sufficient to alter the pattern of this bilaterally organized behavior suggests that (non-auditory) feedback pathways to the forebrain exist to coordinate the two hemispheres during singing. We suggest that the study of the motor control system for birdsong has provided the most direct evidence to date for localizing the programming of a skilled motor sequence to the telencephalon.
346 citations
25 Feb 2014
TL;DR: This chapter discusses the neurobiology of learning and memory in Rats with an emphasis on the role of the Hippocampal Formation, and some of the implications for future generations of researchers.
Abstract: Contents: Part I:Introduction. W. Hodos, C.B.G. Campbell, Evolutionary Scales and Comparative Studies of Animal Cognition. Part II:Neurobiology of Communication. B. Gordon, Human Language. U. J rgens, Vocal Communication in Primates. H. Williams, Bird Song. Part III:Neurobiology of Learning and Memory. E.A. Murray, Representational Memory in Nonhuman Primates. A.S. Powers, Brain Mechanisms of Learning in Reptiles. R.P. Kesner, Learning and Memory in Rats With an Emphasis on the Role of the Hippocampal Formation. J.B. Overmier, K.L. Hollis, Fish in the Think Tank: Learning, Memory, and Integrated Behavior. R. Menzel, Learning, Memory, and "Cognition" in Honey Bees. J.H. Byrne, Learning and Memory in Aplysia and Other Invertebrates. Part IV.Neurobiology of Spatial Organization. F.J. Friedrich, Frameworks for the Study of Human Spatial Impairments. E.T. Rolls, Functions of the Primate Hippocampus in Spatial Processing and Memory. B. Leonard, B.L. McNaughton, Spatial Representation in the Rat: Conceptual, Behavioral, and Neurophysiological Perspectives. V.P. Bingman, Spatial Navigation in Birds.
303 citations