Spatiotemporal properties of the BOLD response in the songbirds' auditory circuit during a variety of listening tasks

Meir, Vincent Van; Boumans, Tiny; Groof, Geert De; Audekerke, Johan Van; Smolders, Alain; Scheunders, Paul; Sijbers, Jan; Verhoye, Marleen; Balthazart, Jacques; Linden, Annemie Van der

doi:10.1016/j.neuroimage.2004.12.058

Cited by 64 publications

(63 citation statements)

References 48 publications

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“…This method enables us to obtain better spatial resolution and localization of neural representation of birdsong than in electrophysiological recordings and to investigate the effect of various stimuli on the same individual. The feasibility of fMRI on songbirds has been demonstrated recently in anesthetized European starlings (35). It was shown that a sensory BOLD response exists, is stable over time, and causes specific activation of auditory areas of the brain in response to auditory and song stimuli.…”

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confidence: 99%

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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mentioning

confidence: 99%

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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“…This protocol relies on sedation with the b 2 -adrenoreceptor agonist medetomidine (29) and on the non-invasive monitoring of transcutaneous blood gas status for stable physiological conditions and persistent BOLD fMRI contrast (30). Others have successfully used the same anaesthesia in fMRI studies of the visual system of rats (31) and auditory processing in birds (32).…”

Section: Choice Of Anaesthesia and Effect On Brain Activationmentioning

confidence: 99%

“…This imaging tool was recently introduced in a welldocumented small animal model for vocal learning, the songbird. It was demonstrated that fMRI can be used to monitor auditory induced activation representing discriminatory properties of secondary auditory regions of the telencephalon (32). When starlings were presented with white noise, only field L (primary auditory regions) was activated.…”

Section: Cognitive Studies With Fmri In Small Animalsmentioning

confidence: 99%

“…Although working with songbirds introduces new susceptibility problems because of air cavities in the skull, the location of the auditory system in the bird brain averts any potential influence of that kind. (32) fMRI studies of pathophysiological alterations in functional brain activity A large number of studies have provided extensive evidence of the robustness of the coupling mechanisms between neuronal electrical activity and blood flow response in the healthy brain. However, the situation may be different in disease states, where the preservation of such mechanisms can be compromised, hampering the recording of reliable functional brain imaging data.…”

Section: Cognitive Studies With Fmri In Small Animalsmentioning

confidence: 99%

“…In both mammals and songbirds, the BOLD response is characterised, and, although birds have a higher body temperature, the BOLD response seems to be quite similar to the mammalian response (32,124). The only existing fMRI studies on fish (109) are reported in this review and could not rely on a temporal BOLD response pattern mainly because of the nature of the stimulus (acute but persistent cold shock).…”

Section: Advantages and Disadvantages Of Different Animal Models As Smentioning

confidence: 99%

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Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition

et al. 2007

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This review aims to make the reader aware of the potential of functional MRI (fMRI) in brain activation studies in small animal models. As small animals generally require anaesthesia for immobilization during MRI protocols, this is believed to be a serious limitation to the type of question that can be addressed with fMRI. We intend to introduce a fresh view with an in-depth overview of the surprising number of fMRI applications in a wide range of important research domains in neuroscience. These include the pathophysiology of brain functioning, the basic science of activity, and functional connectivity of different sensory circuits, including sensory brain mapping, the challenges when studying the hypothalamus as the major control centre in the central nervous system, and the limbic system as neural substrate for emotions and reward. Finally the contribution of small animal fMRI research to cognitive neuroscience is outlined. This review avoids focusing exclusively on traditional small laboratory animals such as rodents, but rather aims to broaden the scope by introducing alternative lissencephalic animal models such as songbirds and fish, as these are not yet well recognized as neuroimaging study subjects. These models are well established in many other neuroscience disciplines, and this review will show that their investigation with in vivo imaging tools will open new doors to cognitive neuroscience and the study of the autonomous nervous system in experimental animals.

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The development of stimulus‐specific auditory responses requires song exposure in male but not female zebra finches

Maul

Voss

Parra

et al. 2009

Developmental Neurobiology

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Juvenile male zebra finches develop their song by imitation. Females do not sing but are attracted to males' songs. With functional Magnetic Resonance Imaging (fMRI) and Event Related Potentials (ERPs) we tested how early auditory experience shapes responses in the auditory forebrain of the adult bird. Adult male birds kept in isolation over the sensitive period for song learning showed no consistency in auditory responses to conspecific songs, calls, and syllables. Thirty seconds of song playback each day over development, which is sufficient to induce song imitation, was also sufficient to shape stimulus-specific responses. Strikingly, adult females kept in isolation over development showed responses similar to those of males that were exposed to songs. We suggest that early auditory experience with songs may be required to tune perception towards conspecific songs in males, whereas in females song selectivity develops even without prior exposure to song.

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Spatiotemporal properties of the BOLD response in the songbirds' auditory circuit during a variety of listening tasks

Cited by 64 publications

References 48 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

Current status of functional MRI on small animals: application to physiology, pathophysiology, and cognition

The development of stimulus‐specific auditory responses requires song exposure in male but not female zebra finches

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