Cover Page The handle http://hdl.handle.net/1887/31633 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: 2015-01-28
Neural correlates of vocal learning in songbirds and humans cross-species fmri studies into individual differences Anne M. van der Kant
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: 978-94-6259-519-4 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.
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
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 10.00 uur door Anne Marie van der Kant geboren 4 mei 1984 te Lelystad
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
Never lose your sense of wonder
Contents 1 General introduction 1 1.1 Birdsong and human language................... 2 1.1.1 The value of the songbird model for human speech... 2 1.1.2 Learning by imitation in songbirds and humans..... 4 1.1.3 Sensitive periods for birdsong learning and human language acquisition....................... 6 1.1.4 Different brains, similar mechanisms?........... 7 1.2 fmri for comparative studies on vocal learning.......... 11 1.2.1 Methods for songbird and human brain research..... 11 1.2.2 fmri in songbirds and humans............... 12 1.3 Research questions and hypothesis................. 14 1.4 Contributions............................. 15 I Neural correlates of vocal learning in zebra finches 17 2 Current State-of-the-Art of auditory fmri on Zebra Finches 21 2.1 Introduction.............................. 22 2.1.1 Functional Magnetic Resonance Imaging (fmri)..... 23 2.1.2 Auditory fmri of speech and vocal communication... 24 2.2 BOLD response in the auditory system of a robust songbird.. 26 2.2.1 Implementation of BOLD fmri in the starling brain... 26 2.2.2 Technical challenges..................... 26 2.3 BOLD fmri in the zebra finch s auditory system......... 28 2.3.1 Visualization of the BOLD response in the zebra finch s auditory system........................ 29 2.3.2 BOLD response in zebra finch s auditory system upon robust 1 st order manipulations of conspecific song stimuli 31
x 2.3.3 BOLD response in the zebra finch auditory system upon 2 nd order spectral and temporal song stimuli manipulations.............................. 32 2.3.4 BOLD response in the zebra finch s auditory system upon 2 nd order song manipulations and the bird s own song.............................. 32 2.4 Further technical refinements of the method............ 34 2.4.1 Improvements in acquisition protocol........... 34 2.4.2 voxel-based analysis and development of a zebra finch MRI brain atlas........................ 35 2.4.3 Effect of different anaesthetics on the BOLD response in the zebra finch s auditory system.............. 37 2.5 BOLD response to the bird s own song in the zebra finch brain. 38 2.6 New findings on the role of MLd in tutor song selectivity and memory................................ 40 2.7 fmri of zebra finch during ontogeny................ 41 2.8 BOS selectivity: involvement of the noradrenergic system.... 42 2.9 Developments and applications in other research groups.... 43 2.10 Conclusions and future prospects.................. 44 2.11 Acknowledgements.......................... 45 3 Representation of early sensory experience in adult MLd 47 3.1 Introduction.............................. 47 3.2 Materials and Methods........................ 48 3.2.1 Ethical Statement....................... 48 3.2.2 Subjects............................ 48 3.2.3 Song Recording and Analysis................ 49 3.2.4 fmri stimuli.......................... 49 3.2.5 Experimental setup and design............... 50 3.2.6 fmri acquisition....................... 50 3.2.7 Image processing....................... 52 3.2.8 Statistical analysis...................... 52 3.3 Results................................. 55 3.3.1 Behavioral results of song tutoring............. 55 3.3.2 Brain responses in MLd................... 55 3.3.3 Brain responses in NCM................... 57 3.4 Discussion............................... 58 3.5 Acknowledgments.......................... 65 4 Neural correlates of tutor song learning 67 4.1 Introduction.............................. 68 4.2 Materials and methods........................ 69 4.2.1 Subjects............................ 69 4.2.2 fmri procedure........................ 69 4.3 Results................................. 72
xi 4.3.1 Tutor song selectivity..................... 72 4.3.2 Conspecific song selectivity................. 76 4.4 Discussion............................... 77 II Neural correlates of artificial grammar learning in human adults 83 5 Neural correlates of non-adjacent dependency learning 87 5.1 Introduction.............................. 88 5.1.1 The role of non-adjacent dependency learning in language acquisition....................... 88 5.1.2 Artificial Grammar Learning in the brain......... 88 5.1.3 Individual differences in brain and behavior....... 90 5.2 Methods................................ 90 5.2.1 Ethical statement....................... 90 5.2.2 Participants.......................... 90 5.2.3 Materials............................ 91 5.2.4 Experimental paradigm................... 93 5.2.5 MRI data collection and analysis.............. 94 5.3 Results................................. 95 5.3.1 Behavioral results....................... 95 5.3.2 Exposure phase........................ 96 5.3.3 fmri results grammaticality judgment task........ 97 5.4 Discussion............................... 100 5.4.1 Differential activation as a precursor for learning.... 101 5.4.2 Sensitivity to the deviant as an early stage in learning.. 103 5.4.3 Conclusions.......................... 104 6 Individual differences in AGL brain connectivity 105 6.1 Introduction.............................. 105 6.2 Methods................................ 107 6.2.1 Ethical statement....................... 107 6.2.2 Participants.......................... 108 6.2.3 Imaging Procedure...................... 108 6.2.4 Resting State fmri Data analysis.............. 109 6.2.5 DTI Data analysis....................... 110 6.3 Results................................. 111 6.3.1 Behavioral results....................... 111 6.3.2 Functional connectivity................... 111 6.3.3 Structural connectivity.................... 114 6.4 Discussion............................... 115 6.4.1 AGL influences functional connectivity.......... 116 6.4.2 Contribution of the dorsal language pathway....... 117 6.4.3 Conclusion.......................... 118
xii 7 Summary and conclusions 121 7.1 Summary................................ 122 7.1.1 Processing of learned song in the auditory midbrain of adult and juvenile zebra finches.............. 122 7.1.2 Artificial grammar learning in human adults....... 123 7.2 Discussion............................... 124 7.2.1 Implications.......................... 124 7.2.2 Insights from cross-species fmri studies......... 126 7.2.3 Limitations.......................... 127 7.3 Conclusions.............................. 128 7.4 Future Prospects............................ 129 7.4.1 Artificial grammar learning within the sensitive period for language development.................. 129 7.4.2 Different levels of abstraction................ 129 References.................................... 131 List of Figures.................................. 155 Glossary..................................... 157 Samenvatting in het Nederlands....................... 161 Acknowledgements............................... 165 Curriculum Vitae................................ 167 List of publications............................... 169