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1 Cover Page The handle holds various files of this Leiden University dissertation. Author: Kant, Anne Marie van der Title: Neural correlates of vocal learning in songbirds and humans : cross-species fmri studies into individual differences Issue Date:

2 Neural correlates of vocal learning in songbirds and humans cross-species fmri studies into individual differences Anne M. van der Kant

3 Anne M. van der Kant Neural correlates of vocal learning in songbirds and humans: cross-species fmri studies into individual differences PhD Thesis, Leiden University & University of Antwerp Cover design: Anne van der Kant ISBN: Copyright c 2015 by Anne van der Kant. All rights reserved, except chapter 2 and 3, for which the copyright lies with the publishers of the corresponding research papers.

4 Faculteit der Farmaceutische, Biomedische en Diergeneeskundige Wetenschappen Neural correlates of vocal learning in songbirds and humans cross-species fmri studies into individual differences Neurale correlaten van vocaal leren bij zangvogels en mensen fmri studies naar soortelijke en individuele verschillen (met een samenvatting in het Nederlands) Proefschrift voorgelegd tot het behalen van de graad van doctor in de Biomedische Wetenschappen aan de Universiteit Antwerpen te verdedigen door Anne Marie van der Kant

5

6 Neural correlates of vocal learning in songbirds and humans cross-species fmri studies into individual differences Proefschrift ter verkrijging van de graad van Doctor aan de Universiteit Leiden, op gezag van Rector Magnificus prof. mr. C.J.J.M. Stolker, volgens besluit van het College voor Promoties te verdedigen op woensdag 28 januari 2015 klokke uur door Anne Marie van der Kant geboren 4 mei 1984 te Lelystad

7 Promotie commissie Promotores: Co-promotor: Overige leden prof. dr. A.M. Van der Linden prof. dr. N.O. Schiller prof. dr. C.C. Levelt prof. dr. G. Van Camp prof. dr. M. Giugliano prof. dr. L.L. Cheng prof. dr. C.J. ten Cate prof. dr. D. Clayton

8 Never lose your sense of wonder

9

10 Contents 1 General introduction Birdsong and human language The value of the songbird model for human speech Learning by imitation in songbirds and humans Sensitive periods for birdsong learning and human language acquisition Different brains, similar mechanisms? fmri for comparative studies on vocal learning Methods for songbird and human brain research fmri in songbirds and humans Research questions and hypothesis Contributions I Neural correlates of vocal learning in zebra finches 17 2 Current State-of-the-Art of auditory fmri on Zebra Finches Introduction Functional Magnetic Resonance Imaging (fmri) Auditory fmri of speech and vocal communication BOLD response in the auditory system of a robust songbird Implementation of BOLD fmri in the starling brain Technical challenges BOLD fmri in the zebra finch s auditory system Visualization of the BOLD response in the zebra finch s auditory system BOLD response in zebra finch s auditory system upon robust 1 st order manipulations of conspecific song stimuli 31

11 x BOLD response in the zebra finch auditory system upon 2 nd order spectral and temporal song stimuli manipulations BOLD response in the zebra finch s auditory system upon 2 nd order song manipulations and the bird s own song Further technical refinements of the method Improvements in acquisition protocol voxel-based analysis and development of a zebra finch MRI brain atlas Effect of different anaesthetics on the BOLD response in the zebra finch s auditory system BOLD response to the bird s own song in the zebra finch brain New findings on the role of MLd in tutor song selectivity and memory fmri of zebra finch during ontogeny BOS selectivity: involvement of the noradrenergic system Developments and applications in other research groups Conclusions and future prospects Acknowledgements Representation of early sensory experience in adult MLd Introduction Materials and Methods Ethical Statement Subjects Song Recording and Analysis fmri stimuli Experimental setup and design fmri acquisition Image processing Statistical analysis Results Behavioral results of song tutoring Brain responses in MLd Brain responses in NCM Discussion Acknowledgments Neural correlates of tutor song learning Introduction Materials and methods Subjects fmri procedure Results

12 xi Tutor song selectivity Conspecific song selectivity Discussion II Neural correlates of artificial grammar learning in human adults 83 5 Neural correlates of non-adjacent dependency learning Introduction The role of non-adjacent dependency learning in language acquisition Artificial Grammar Learning in the brain Individual differences in brain and behavior Methods Ethical statement Participants Materials Experimental paradigm MRI data collection and analysis Results Behavioral results Exposure phase fmri results grammaticality judgment task Discussion Differential activation as a precursor for learning Sensitivity to the deviant as an early stage in learning Conclusions Individual differences in AGL brain connectivity Introduction Methods Ethical statement Participants Imaging Procedure Resting State fmri Data analysis DTI Data analysis Results Behavioral results Functional connectivity Structural connectivity Discussion AGL influences functional connectivity Contribution of the dorsal language pathway Conclusion

13 xii 7 Summary and conclusions Summary Processing of learned song in the auditory midbrain of adult and juvenile zebra finches Artificial grammar learning in human adults Discussion Implications Insights from cross-species fmri studies Limitations Conclusions Future Prospects Artificial grammar learning within the sensitive period for language development Different levels of abstraction References List of Figures Glossary Samenvatting in het Nederlands Acknowledgements Curriculum Vitae List of publications

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