State‐dependent hemispheric specialization in the songbird brain

George, Isabelle; Cousillas, Hugo; Richard, Jean‐Pierre; Hausberger, Martine

doi:10.1002/cne.20584

Cited by 45 publications

(36 citation statements)

References 56 publications

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“…Bilateral asymmetry with either left-sided or right-sided dominance, or differential dual specialization, has been previously observed in songbirds in relation to both central and peripheral control of song production (49)(50)(51)(52). As far as song perception is concerned, increased neuronal responsiveness to behaviorally relevant song stimuli has been observed in the field L complex and HVC on the right side in starlings (53,54). Right hemispheric specialization is seen only in awake birds.…”

Section: Familiar Song Stimuli Show Selective Differential Topographymentioning

confidence: 82%

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

Voss

Tabelow

Polzehl

et al. 2007

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

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Electrophysiological and activity-dependent gene expression studies of birdsong have contributed to the understanding of the neural representation of natural sounds. However, we have limited knowledge about the overall spatial topography of song representation in the avian brain. Here, we adapt the noninvasive functional MRI method in mildly sedated zebra finches (Taeniopygia guttata) to localize and characterize song driven brain activation. Based on the blood oxygenation level-dependent signal, we observed a differential topographic responsiveness to playback of bird's own song, tutor song, conspecific song, and a pure tone as a nonsong stimulus. The bird's own song caused a stronger response than the tutor song or tone in higher auditory areas. This effect was more pronounced in the medial parts of the forebrain. We found left-right hemispheric asymmetry in sensory responses to songs, with significant discrimination between stimuli observed only in the right hemisphere. This finding suggests that perceptual responses might be lateralized in zebra finches. In addition to establishing the feasibility of functional MRI in sedated songbirds, our results demonstrate spatial coding of song in the zebra finch forebrain, based on developmental familiarity and experience.imaging ͉ learning ͉ memory B irdsong is studied as a model of vocal learning, perception, production, and motor abnormalities of speech (1, 2). There are interesting parallels between song development and speech development (3) and between auditory and vocal pathways in the songbird and human brain (4). Therefore, insights from experiments on songbirds may contribute to the understanding of auditory and vocal function in humans. For example, minimal models of speech dyspraxia (5) and dysfluencies such as stuttering are being developed in zebra finches (6). Zebra finches are capable of learning, producing, perceiving, and discriminating complex sound patterns. Birdsong in zebra finches consists of a sequence of distinctive sounds produced by males and is characterized by a consistent and reproducible acoustic profile. Song is learned by imitating the song of an adult conspecific tutor during a sensitive period of development (7-10). Recently, it has been shown that songbirds are able to learn recursive syntactic patterns, presumably a simple form of grammar (11), thus extending the potential applicability of the birdsong model to our understanding of the biological basis of languages. Several brain structures are required for learning, production, and perception of birdsong. It is known from electrophysiological studies that song learning nuclei, such as the lateral magnocellular nucleus of the anterior nidopallium (LMAN) and X (12), play an important role in song development. In parallel with song motor learning, auditory song selectivity gradually emerges during development (13-17). Robust sensory responses to auditory stimuli have been recorded in the primary auditory area in the caudal telencephalic region (field L), the caudomedial nidopallium (N...

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Section: Familiar Song Stimuli Show Selective Differential Topographymentioning

confidence: 82%

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

Voss

Tabelow

Polzehl

et al. 2007

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

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“…Likewise, it has been suggested that there is a functional division of the two hemispheres in songbirds. In starlings, song processing in the left hemisphere might be more focussed on individual recognition of birds far away, while the right hemisphere may be specialised for analysing long and complex song sequences that birds in close proximity sing45. Another hypothesis is that lateralisation improves dual-task performance (i.e., when two tasks are executed simultaneously; Refs.…”

Section: Discussionmentioning

confidence: 99%

Learning-related brain hemispheric dominance in sleeping songbirds

Moorman

Gobes

Kamp

et al. 2015

Sci Rep

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There are striking behavioural and neural parallels between the acquisition of speech in humans and song learning in songbirds. In humans, language-related brain activation is mostly lateralised to the left hemisphere. During language acquisition in humans, brain hemispheric lateralisation develops as language proficiency increases. Sleep is important for the formation of long-term memory, in humans as well as in other animals, including songbirds. Here, we measured neuronal activation (as the expression pattern of the immediate early gene ZENK) during sleep in juvenile zebra finch males that were still learning their songs from a tutor. We found that during sleep, there was learning-dependent lateralisation of spontaneous neuronal activation in the caudomedial nidopallium (NCM), a secondary auditory brain region that is involved in tutor song memory, while there was right hemisphere dominance of neuronal activation in HVC (used as a proper name), a premotor nucleus that is involved in song production and sensorimotor learning. Specifically, in the NCM, birds that imitated their tutors well were left dominant, while poor imitators were right dominant, similar to language-proficiency related lateralisation in humans. Given the avian-human parallels, lateralised neural activation during sleep may also be important for speech and language acquisition in human infants.

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“…The degree to which auditory tuning in the awake bird is selective to the BOS might, however, vary with developmental age and even with the species being studied. For example, HVC neurons in juvenile zebra finches show auditory related responses to both tutor song and the bird’s own song during waking states early in development (Nick and Konishi, 2005) and recordings from HVC in Bengalese finches, starlings and several species of sparrows reveal auditory responses that are selective to the BOS in the awake animal (Margoliash and Konishi, 1985; George et al, 2005; Nealen and Schmidt, 2006; Prather et al, 2008; Sakata and Brainard, 2008; Prather et al, 2009). …”

Section: Auditory Responses In Nif and Hvcmentioning

confidence: 99%

At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing, production and learning

Lewandowski

Vyssotski

Hahnloser

et al. 2013

Journal of Physiology-Paris

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Communication between auditory and vocal motor nuclei is essential for vocal learning. In songbirds, the nucleus interfacialis of the nidopallium (NIf) is part of a sensorimotor loop, along with auditory nucleus avalanche (Av) and song system nucleus HVC, that links the auditory and song systems. Most of the auditory information comes through this sensorimotor loop, with the projection from NIf to HVC representing the largest single source of auditory information to the song system. In addition to providing the majority of HVC’s auditory input, NIf is also the primary driver of spontaneous activity and premotor-like bursting during sleep in HVC. Like HVC and RA, two nuclei critical for song learning and production, NIf exhibits behavioral-state dependent auditory responses and strong motor bursts that precede song output. NIf also exhibits extended periods of fast gamma oscillations following vocal production. Based on the converging evidence from studies of physiology and functional connectivity it would be reasonable to expect NIf to play an important role in the learning, maintenance, and production of song. Surprisingly, however, lesions of NIf in adult zebra finches have no effect on song production or maintenance. Only the plastic song produced by juvenile zebra finches during the sensorimotor phase of song learning is affected by NIf lesions. In this review, we carefully examine what is known about NIf at the anatomical, physiological, and behavioral levels. We reexamine conclusions drawn from previous studies in the light of our current understanding of the song system, and establish what can be said with certainty about NIf’s involvement in song learning, maintenance, and production. Finally, we review recent theories of song learning integrating possible roles for NIf within these frameworks and suggest possible parallels between NIf and sensorimotor areas that form part of the neural circuitry for speech processing in humans.

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State‐dependent hemispheric specialization in the songbird brain

Cited by 45 publications

References 56 publications

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

Functional MRI of the zebra finch brain during song stimulation suggests a lateralized response topography

Learning-related brain hemispheric dominance in sleeping songbirds

At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing, production and learning

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