Disrupting vagal feedback affects birdsong motor control

Méndez, Jorge; Dall'Asén, Analía G.; Goller, Franz

doi:10.1242/jeb.045369

Cited by 15 publications

(7 citation statements)

References 55 publications

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“…This result is very similar to that reported by Mendez et al, who reported that unilateral vagotomy of adult zebra finches caused alterations in the normal respiratory pattern during song, sometimes leading to acoustic changes such as truncations and interruptions (Mendez et al, 2010). These disruptions occurred within the first few days post-surgery, followed by partial or full recovery, and were highly variable between individual birds, as observed here.…”

Section: Resultssupporting

confidence: 91%

Afferents from Vocal Motor and Respiratory Effectors Are Recruited during Vocal Production in Juvenile Songbirds

Bottjer

2012

J. Neurosci.

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Learned behaviors require coordination of diverse sensory inputs with motivational and motor systems. Although mechanisms underlying vocal learning in songbirds have focused primarily on auditory inputs, it is likely that sensory inputs from vocal effectors also provide essential feedback. We investigated the role of somatosensory and respiratory inputs from vocal effectors of juvenile zebra finches (Taeniopygia guttata) during the stage of sensorimotor integration when they are learning to imitate a previously memorized tutor song. We report that song production induced expression of the immediate early gene product Fos in trigeminal regions that receive hypoglossal afferents from the tongue and syrinx (the main vocal organ). Furthermore, unilateral lesion of hypoglossal afferents greatly diminished singing-induced Fos expression on the side ipsilateral to the lesion, but not on the intact control side. In addition, unilateral lesion of the vagus reduced Fos expression in the ipsilateral nucleus of the solitary tract in singing birds. Lesion of the hypoglossal nerve to the syrinx greatly disrupted vocal behavior, whereas lesion of the hypoglossal nerve to the tongue exerted no obvious disruption and lesions of the vagus caused some alterations to song behavior. These results provide the first functional evidence that somatosensory and respiratory feedback from peripheral effectors is activated during vocal production and conveyed to brainstem regions. Such feedback is likely to play an important role in vocal learning during sensorimotor integration in juvenile birds and in maintaining stereotyped vocal behavior in adults.

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Section: Resultssupporting

confidence: 91%

Afferents from Vocal Motor and Respiratory Effectors Are Recruited during Vocal Production in Juvenile Songbirds

Bottjer

2012

J. Neurosci.

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“…For 150-and 300-cent shifts, the fraction of compensation at the end of the shift epoch similarly decreased with shift size. Such incomplete learning could result from the bird's relying in part on nonauditory inputs such as proprioceptive feedback or the output of an internal model used to predict sensory feedback (13)(14)(15) (1,10). It is therefore unlikely that the plateau in vocal learning shown in Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Such a flexible weighting strategy might account for the inverse relationship between the size of sensory pitch shifts and the magnitude of the behavioral responses. That is, when experiencing large errors, songbirds might reduce their reliance on auditory information and increase their reliance on proprioceptive signals (13,14) or internal models of motor output (15) to estimate vocal pitch. The resulting integrated estimate might then be compared with an internal target to generate an error signal.…”

Section: Discussionmentioning

confidence: 99%

Vocal learning is constrained by the statistics of sensorimotor experience

Sober

Brainard

2012

Proc. Natl. Acad. Sci. U.S.A.

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The brain uses sensory feedback to correct behavioral errors. Larger errors by definition require greater corrections, and many models of learning assume that larger sensory feedback errors drive larger motor changes. However, an alternative perspective is that larger errors drive learning less effectively because such errors fall outside the range of errors normally experienced and are therefore unlikely to reflect accurate feedback. This is especially crucial in vocal control because auditory feedback can be contaminated by environmental noise or sensory processing errors. A successful control strategy must therefore rely on feedback to correct errors while disregarding aberrant auditory signals that would lead to maladaptive vocal corrections. We hypothesized that these constraints result in compensation that is greatest for smaller imposed errors and least for larger errors. To test this hypothesis, we manipulated the pitch of auditory feedback in singing Bengalese finches. We found that learning driven by larger sensory errors was both slower than that resulting from smaller errors and showed less complete compensation for the imposed error. Additionally, we found that a simple principle could account for these data: the amount of compensation was proportional to the overlap between the baseline distribution of pitch production and the distribution experienced during the shift. Correspondingly, the fraction of compensation approached zero when pitch was shifted outside of the song's baseline pitch distribution. Our data demonstrate that sensory errors drive learning best when they fall within the range of production variability, suggesting that learning is constrained by the statistics of sensorimotor experience.multisensory integration | sensorimotor learning | motor variability E rror correction based on sensory feedback is a ubiquitous mechanism for maintaining behavioral performance (1-4). However, sensory information is vulnerable to environmental noise and to errors in sensory encoding arising at the periphery or during central processing of the sensory signal (5). Such contamination can result in large mismatches between the actual and expected sensory feedback that do not necessarily reflect errors in performance. The brain must therefore decide whether to modify behavior based on sensory feedback (and risk "adapting" to signals that do not accurately reflect performance) or ignore sensory input (and risk leaving errors uncorrected). This problem is especially important in vocal behaviors, in which performance can have significant consequences for the success of an organism and auditory feedback is vulnerable to extrinsic acoustic signals and errors in auditory encoding.During development, both humans and songbirds learn by processes of vocal imitation that rely heavily on auditory feedback (2). Early vocalizations bear little resemblance to mature song or speech, resulting in large differences (errors) between experienced auditory feedback and the sensory goal. With practice, vocalizations become m...

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“…Because PAm receives a strong input from the lateral parasolitary nucleus (lPs) of nTS, it is conceivable that the transition from a minibreath to the generation of a new timing signal would be strongly influenced by vagal inputs that relay to PAm, via nTS, afferent signals regarding the internal state of the respiratory periphery (lungs, air sacs). This possibility has only recently been explored in songbirds (Mendez et al, 2010) and a general role for sensory input into vocal control is generally under appreciated. In cats, however, the general role of respiratory input within the context of vocalization, and the specific importance of pulmonary feedback for the ability to vocalize, was explored and demonstrated over 15 years ago (Davis and Zhang, 1996; Davis et al, 1996; Nakazawa et al, 1997).…”

Section: Song Production and The “Respiratory-thalamo-cortical” Patmentioning

confidence: 99%

The respiratory-vocal system of songbirds

Schmidt

Wild

2014

Progress in Brain Research

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This wide-ranging review presents an overview of the respiratory-vocal system in songbirds, which are the only other vertebrate group known to display a degree of respiratory control during song rivalling that of humans during speech; this despite the fact that the peripheral components of both the respiratory and vocal systems differ substantially in the two groups. We first provide a brief description of these peripheral components in songbirds (lungs, air sacs and respiratory muscles, vocal organ (syrinx), upper vocal tract) and then proceed to a review of the organization of central respiratory-related neurons in the spinal cord and brainstem, the latter having an organization fundamentally similar to that of the ventral respiratory group of mammals. The second half of the review describes the nature of the motor commands generated in a specialized “cortical” song control circuit and how these might engage brainstem respiratory networks to shape the temporal structure of song. We also discuss a bilaterally projecting “respiratory-thalamic” pathway that links the respiratory system to “cortical” song control nuclei. This necessary pathway for song originates in the brainstem’s primary inspiratory center and is hypothesized to play a vital role in synchronizing song motor commands both within and across hemispheres.

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Disrupting vagal feedback affects birdsong motor control

Cited by 15 publications

References 55 publications

Afferents from Vocal Motor and Respiratory Effectors Are Recruited during Vocal Production in Juvenile Songbirds

Afferents from Vocal Motor and Respiratory Effectors Are Recruited during Vocal Production in Juvenile Songbirds

Vocal learning is constrained by the statistics of sensorimotor experience

The respiratory-vocal system of songbirds

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