In experiment I, The HVC asymmetric (excitatory) and symmetric (inhibitory) synapse subtypes were quantified in their densities (see Results section 2.3.3 and 2.3.4), average sizes, and average Feret diameters (see Results section 2.3.6 and 2.3.7). All these parameters of both the asymmetric and symmetric synapses were measured in the same way, and from the same brain sample for each bird. Therefore, in each bird it is possible to systematically compare on the population level between the HVC asymmetric synapses and the HVC symmetric synapses. In general it is interesting to know the overall excitation and inhibition level in HVC network, and how the balance between them would change under different song learning conditions. So I made use of my neuroanatomical data, and propose here a way to estimate the E/I balance of the HVC network. I compared the E/I balance among groups to investigate if different sensory experiences to the tutor songs shift the E/I balance.
The overall HVC excitation in a given bird can be represented by summing all the HVC asymmetric (excitatory) synapses while considering their sizes as a measure of synaptic weight (see Discussion section 2.4.3). However I did not take the synapse volumes to represent the weight since the volumes of the asymmetric synapses are on average much larger than the symmetric synapses for any given bird (see Results section 2.3.6). If I directly take the synapse volumes to represent the weights, I between the asymmetric synapses and symmetric synapses (see Results section 2.3.7).
An overall HVC excitation level thus can be estimated as the product of three terms:
the average density of HVC asymmetric synapses 𝑵𝑽(𝒂𝒔𝒚) , the HVC volume 𝑽𝒉𝒗𝒄 , and the mean Feret diameter of HVC asymmetric synapses 𝑫𝒊𝒂𝒎𝒆𝒕𝒆𝒓(𝒂𝒔𝒚). The overall HVC inhibition can be expressed in the same terms that are measured in the HVC symmetric synapses of the same bird. The HVC E/I balance can then be defined as follows:
Equation S. 6: 𝑬/𝑰 − 𝒃𝒂𝒍𝒂𝒏𝒄𝒆𝒊𝒏𝒅𝒆𝒙=𝑵𝑵𝑽(𝒂𝒔𝒚) ∗ 𝑽𝒉𝒗𝒄∗𝑫𝒊𝒂𝒎𝒆𝒕𝒆𝒓(𝒂𝒔𝒚)
𝑽(𝒔𝒚𝒎) ∗ 𝑽𝒉𝒗𝒄∗𝑫𝒊𝒂𝒎𝒆𝒕𝒆𝒓(𝒔𝒚𝒎)
189
The HVC volume is the same for the asymmetric and symmetric synapses from the same bird and therefore can be cancelled out of the calculation. The density and Feret diameter of the asymmetric and symmetric synapses were obtained from the measurement results in Experiment I. The resulting E/I-balance index from Equation S. 6 is just a number without a unit and therefore serves as a measure of the E/I balance, with higher value indicating more excitation (less inhibition) in the whole network and vice versa.
The calculated E/I balance index for each bird is summarized in Table S. 9, and illustrated in Figure S. 19. Difference in the HVC E/I balance index among the groups were evaluated with Wilcoxon rank-sum tests, and p values less than 0.05 indicated significant differences.
Table S. 9: Estimation of the E/I balance in the HVC network. The E/I balance was estimated from the HVC synapse density measurments (see Results section 2.3.3 and 2.3.4) and HVC synapse Feret diameter measurements (see Results section 2.3.7), with Equation S. 6. The resulting HVC E/I balance index is shown as a numerical value without a unit for each bird. The group means were calculated by averaging the values across all the birds belonging to the same group, and are presented with SE.
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Figure S. 19: The estimated network E/I balance of HVC in Experiment I. The E/I balance index value of each bird and group are listed in Table S. 9. *p < 0.05 in a Wilcoxon Rank-sum test.
The mean group E/I balance index in the ISO group was 4.14, it decreased in the SHORT group to 2.91 and increased in the LONG group back to 3.84.
Table S. 10: The results of the Wilcoxon rank-sum tests of the HVC E/I balance indexes in the groups in Experiment I. P values less than 0.05, which indicate significance, are written in bold font. Significant differences were found between the ISO and SHORT and SHORT and LONG groups.
The group-wise rank-sum test results are listed Table S. 10. Significant differences were found between the ISO and SHORT groups and between the SHORT and LONG groups.
In summary, the HVC E/I balance significantly decreased (more inhibition) by 30%
shortly after initial exposure to the tutor song, which can be observed in the comparison between the ISO and SHORT groups. After longer tutoring, the HVC E/I balance significantly increased (more excitation) by 32% to a level that was similar to the level from before the tutoring, as can be observed in the comparison between the ISO and LONG groups. The HVC E/I balance in the SHORT group significantly shifted towards more inhibition, as shown in comparison to the ISO and LONG groups.
191
Bibliography
Airey, D. C., H. Castillo-Juarez, G. Casella, E. J. Pollak, and T. J. DeVoogd. 2000.
“Variation in the Volume of Zebra Finch Song Control Nuclei Is Heritable:
Developmental and Evolutionary Implications.” Proceedings of the Royal Society B: Biological Sciences 267(1457):2099–2104.
Airey CA, David C. and Timothy J. DeVoogd. 2000. “Greater Song Complexity Is Associated with Augmented Song System Anatomy in Zebra Finches.”
Neuroethology Neuroreport 11(10):959–4965.
Akutagawa, E. and M. Konishi. 1998. “Transient Expression and Transport of
Brain-Derived Neurotrophic Factor in the Male Zebra Finch’s Song System during Vocal Development.” Proceedings of the National Academy of Sciences of the United States of America 95(19):11429–34.
Akutagawa, Eugene and Masakazu Konishi. 2010. “New Brain Pathways Found in the Vocal Control System of a Songbird.” Journal of Comparative Neurology 518(15):3086–3100.
Alsina, B., T. Vu, and S. Cohen-Cory. 2001. “Visualizing Synapse Formation in Arborizing Optic Axons in Vivo: Dynamics and Modulation by BDNF.” Nature Neuroscience 4(11):1093–1101.
Alvarez-Buylla, A., M. Theelen, and F. Nottebohm. 1988. “Birth of Projection Neurons in the Higher Vocal Center of the Canary Forebrain Before, During, and after Song Learning.” Proceedings of the National Academy of Sciences of the United States of America 85(22):8722–26.
Andersen, Susan L. 2003. “Trajectories of Brain Development: Point of Vulnerability or Window of Opportunity?” Pp. 3–18 in Neuroscience and Biobehavioral Reviews, vol. 27.
Anton Reiner, David J.Perkel, Claudio V. Mello, &.Erich D.Jarvi., Anton Reiner, David J. Perkel, Claudio V. Mello, and Erich D. Jarvis. 2004. “Songbirds and the Revised Avian Brain Nomenclature.” Pp. 77–108 in Annals of the New York Academy of Sciences, vol. 1016.
Arellano, Jon I. 2007. “Ultrastructure of Dendritic Spines: Correlation between Synaptic and Spine Morphologies.” Frontiers in Neuroscience 1(1):131–43.
Aronov, D., A. S. Andalman, and M. S. Fee. 2008. “A Specialized Forebrain Circuit for Vocal Babbling in the Juvenile Songbird.” Science 320(5876):630–34.
Bailey, C. H. and E. R. Kandel. 1993. “Structural Changes Accompanying Memory Storage.” Annual Review of Physiology 55(1):397–426.
Banker, G., L. Churchill, and C. W. Cotman. 1974. “Proteins of the Postsynaptic
192
Density.” Journal of Cell Biology 63(2):456–65.
Baumert, M., P. R. Maycox, F. Navone, P. De Camilli, and R. Jahn. 1989.
“Synaptobrevin: An Integral Membrane Protein of 18,000 Daltons Present in Small Synaptic Vesicles of Rat Brain.” Embo J 8(2):379–84.
Beaulieu, Clermont and Marc Colonnier. 1985. “A Laminar Analysis of the Number of Round-asymmetrical and Flat-symmetrical Synapses on Spines, Dendritic Trunks, and Cell Bodies in Area 17 of the Cat.” Journal of Comparative Neurology 231(2):180–89.
Becker, Carlos, Karim Ali, Graham Knott, and Pascal Fua. 2013. “Learning Context Cues for Synapse Segmentation.” IEEE Transactions on Medical Imaging 32(10):1864–77.
Beecher, Michael D. and Eliot A. Brenowitz. 2005. “Functional Aspects of Song Learning in Songbirds.” Trends in Ecology and Evolution 20(3):143–49.
Blazquez-Llorca, L., E. Hummel, H. Zimmerman, C. Zou, S. Burgold, J. Rietdorf, and J.
Herms. 2015. “Correlation of Two-Photon in Vivo Imaging and FIB/SEM Microscopy.” Journal of Microscopy 259(2):129–36.
Bolhuis, Johan J., Kazuo Okanoya, and Constance Scharff. 2010. “Twitter Evolution:
Converging Mechanisms in Birdsong and Human Speech.” Nature Reviews Neuroscience 11(11):747–59.
Bosch, Miquel, Jorge Castro, Takeo Saneyoshi, Hitomi Matsuno, Mriganka Sur, and Yasunori Hayashi. 2014. “Structural and Molecular Remodeling of Dendritic Spine Substructures during Long-Term Potentiation.” Neuron 82(2):444–59.
Bottjer, S., E. Miesner, and A. Arnold. 1984. “Forebrain Lesions Disrupt Development but Not Maintenance of Song in Passerine Birds.” Science 224(4651):901–3.
Bottjer, S. W., S. L. Glaessner, and a P. Arnold. 1985. “Ontogeny of Brain Nuclei Controlling Song Learning and Behavior in Zebra Finches.” The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 5(6):1556–62.
Bottjer, Sarah W. 2004. “Developmental Regulation of Basal Ganglia Circuitry during the Sensitive Period for Vocal Learning in Songbirds.” Pp. 395–415 in Annals of the New York Academy of Sciences, vol. 1016.
Bottjer, Sarah W., Elizabeth A. Miesner, and Arthur P. Arnold. 1986. “Changes in Neuronal Number, Density and Size Account for Increases in Volume of
Song-Control Nuclei during Song Development in Zebra Finches.” Neuroscience Letters 67(3):263–68.
Brainard, M. S. and A. J. Doupe. 2000. “Auditory Feedback in Learning and Maintenance of Vocal Behaviour.” Nature Reviews. Neuroscience 1(1):31–40.
Brainard, M. S. and a J. Doupe. 2000. “Interruption of a Basal Ganglia-Forebrain Circuit Prevents Plasticity of Learned Vocalizations.” Nature 404(6779):762–66.
Breiman, Leo. 2001. “Random Forests.” Machine Learning 45(1):5–32.
Brenowitz, E. A., K. Lent, and D. E. Kroodsma. 1995. “Brain Space for Learned Song in Birds Develops Independently of Song Learning.” Journal of Neuroscience
193
15(9):6281–86.
Briggman, Kevin L. and Winfried Denk. 2006. “Towards Neural Circuit Reconstruction with Volume Electron Microscopy Techniques.” Current Opinion in Neurobiology 16(5):562–70.
Buchanan, K. L., S. Leitner, K. A. Spencer, A. R. Goldsmith, and C. K. Catchpole. 2004.
“Developmental Stress Selectively Affects the Song Control Nucleus HVC in the Zebra Finch.” Proceedings of the Royal Society B: Biological Sciences
271(1555):2381–86.
Burek, M. J., K. W. Nordeen, and E. J. Nordeen. 1991. “Neuron Loss and Addition in Developing Zebra Finch Song Nuclei Are Independent of Auditory Experience during Song Learning.” Journal of Neurobiology 22(3):215–23.
Buzsáki, György and Kenji Mizuseki. 2014. “The Log-Dynamic Brain: How Skewed Distributions Affect Network Operations.” Nature Reviews Neuroscience 15(4):264–78.
Cane, M., B. Maco, G. Knott, and A. Holtmaat. 2014. “The Relationship between PSD-95 Clustering and Spine Stability In Vivo.” Journal of Neuroscience 34(6):2075–86.
Cardona, Albert, Stephan Saalfeld, Johannes Schindelin, Ignacio Arganda-Carreras, Stephan Preibisch, Mark Longair, Pavel Tomancak, Volker Hartenstein, and Rodney J. Douglas. 2012. “TrakEM2 Software for Neural Circuit Reconstruction”
edited by A. Samuel. PLoS ONE 7(6):e38011.
Cheetham, C. E. J., M. S. L. Hammond, R. McFarlane, and G. T. Finnerty. 2008.
“Altered Sensory Experience Induces Targeted Rewiring of Local Excitatory Connections in Mature Neocortex.” Journal of Neuroscience 28(37):9249–60.
Cheetham, Claire E. J., Samuel J. Barnes, Giorgia Albieri, Graham W. Knott, and Gerald T. Finnerty. 2014. “Pansynaptic Enlargement at Adult Cortical Connections Strengthened by Experience.” Cerebral Cortex 24(2):521–31.
Chen, Jerry L., Walter C. Lin, Jae Won Cha, Peter T. So, Yoshiyuki Kubota, and Elly Nedivi. 2011. “Structural Basis for the Role of Inhibition in Facilitating Adult Brain Plasticity.” Nature Neuroscience 14(5):587–94.
Chen, Yining, Laura E. Matheson, and Jon T. Sakata. 2016. “Mechanisms Underlying the Social Enhancement of Vocal Learning in Songbirds.” Proceedings of the National Academy of Sciences of the United States of America 113(24):6641–46.
Coleman, Melissa J., Arani Roy, J.Martin Wild, and Richard Mooney. 2007. “Thalamic Gating of Auditory Responses in Telencephalic Song Control Nuclei.” The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 27(37):10024–36.
Colonnier, Marc. 1968. “Synaptic Patterns on Different Cell Types in the Different Laminae of the Cat Visual Cortex. An Electron Microscope Study.” Brain Research 9(2):268–87.
Cummings, Jennifer Anne. 2016. “A Developmental Timeline of
Parvalbumin-Expressing Neuron Addition to the Zebra Finch HVC During the Critical Period.” Honors Theses - All (Wesleyan University) 1532.
194
Day, Nancy F., Amanda K. Kinnischtzke, Murtaza Adam, and Teresa A. Nick. 2009.
“Daily and Developmental Modulation Of ‘premotor’ activity in the Birdsong System.” Developmental Neurobiology 69(12):796–810.
DeFelipe, Javier. 1999. “Estimation of the Number of Synapses in the Cerebral Cortex:
Methodological Considerations.” Cerebral Cortex 9(7):722–32.
Delaloye, Sibylle, Rudolf Kraftsik, Thierry Kuntzer, and Ibtissam Barakat-Walter. 2009.
“Does the Physical Disector Method Provide an Accurate Estimation of Sensory Neuron Number in Rat Dorsal Root Ganglia?” Journal of Neuroscience Methods 176(2):290–97.
Denk, W., J. Strickler, and W. Webb. 1990. “Two-Photon Laser Scanning Fluorescence Microscopy.” Science 248(4951):73–76.
Denk, Winfried and Heinz Horstmann. 2004. “Serial Block-Face Scanning Electron Microscopy to Reconstruct Three-Dimensional Tissue Nanostructure.” PLoS Biology 2(11):e329.
Derégnaucourt, Sébastien, Colline Poirier, Anne Van der Kant, Annemie Van der Linden, and Manfred Gahr. 2013. “Comparisons of Different Methods to Train a Young Zebra Finch (Taeniopygia Guttata) to Learn a Song.” Journal of
Physiology Paris 107(3):210–18.
Devoogd, Timothy J. 2004. “Where Is the Bird?” Annals of the New York Academy of Sciences 1016(1):778–86.
Dobie, F. A. and A. M. Craig. 2011. “Inhibitory Synapse Dynamics: Coordinated Presynaptic and Postsynaptic Mobility and the Major Contribution of Recycled Vesicles to New Synapse Formation.” Journal of Neuroscience 31(29):10481–93.
Dorrn, Anja L., Kexin Yuan, Alison J. Barker, Christoph E. Schreiner, and Robert C.
Froemke. 2010. “Developmental Sensory Experience Balances Cortical Excitation and Inhibition.” Nature 465(7300):932–36.
Doupe, A. J. and M. Konishi. 1991. “Song-Selective Auditory Circuits in the Vocal Control System of the Zebra Finch.” Proceedings of the National Academy of Sciences 88(24):11339–43.
Doupe, Allison J. and Patricia K. Kuhl. 1999. “Birdsong and Human Speech: Common Themes and Mechanisms.” Annual Review of Neuroscience 22(1):567–631.
Doupe, Allison J., David J. Perkel, Anton Reiner, and Edward A. Stern. 2005.
“Birdbrains Could Teach Basal Ganglia Research a New Song.” Trends in Neurosciences 28(7):353–63.
Doupe, Allison J. and Michele M. Solis. 1997. “Song- and Order-Selective Neurons Develop in the Songbird Anterior Forebrain during Vocal Learning.” Journal of Neurobiology 33(5):694–709.
Draganski, B., C. Gaser, G. Kempermann, H. G. Kuhn, J. Winkler, C. Buchel, and A.
May. 2006. “Temporal and Spatial Dynamics of Brain Structure Changes during Extensive Learning.” Journal of Neuroscience 26(23):6314–17.
Eales, Lucy A. 1987. “Song Learning in Female-Raised Zebra Finches: Another Look at the Sensitive Phase.” Animal Behaviour 35(5):1356–65.
195
Efron, B. and C. Stein. 1981. “The Jackknife Estimate of Variance THE JACKKNIFE ESTIMATE OF VARLANCE.” Source: The Annals of Statistics The Annals of Statistics 9(3):586–96.
Elliott, Kevin C., Wei Wu, Richard Bertram, Richard L. Hyson, and Frank Johnson.
2017. “Orthogonal Topography in the Parallel Input Architecture of Songbird HVC.” Journal of Comparative Neurology 525(9):2133–51.
Fagiolini, M. and T. K. Hensch. 2000. “Inhibitory Threshold for Critical-Period Activation in Primary Visual Cortex.” Nature 404(6774):183–86.
Fehér, Olga, Iva Ljubičić, Kenta Suzuki, Kazuo Okanoya, and Ofer Tchernichovski.
2017. “Statistical Learning in Songbirds: From Self-Tutoring to Song Culture.”
Philosophical Transactions of the Royal Society B: Biological Sciences 372(1711):20160053.
Feldman, D. E. 2000. “Inhibition and Plasticity.” Nature Neuroscience 3(4):303–4.
Fiala, J. C. and K. M. Harris. 2001. “Cylindrical Diameters Method for Calibrating Section Thickness in Serial Electron Microscopy.” Journal of Microscopy 202(3):468–72.
Finger, Stanley. 2010. Minds Behind the Brain: A History of the Pioneers and Their Discoveries.
Fletcher, David, Darryl MacKenzie, and Eduardo Villouta. 2005. “Modelling Skewed Data with Many Zeros: A Simple Approach Combining Ordinary and Logistic Regression.” Environmental and Ecological Statistics 12(1):45–54.
Foster, Elizabeth F. and Sarah W. Bottjer. 1998. “Axonal Connections of the High Vocal Center and Surrounding Cortical Regions in Juvenile and Adult Male Zebra Finches.” Journal of Comparative Neurology 397(1):118–38.
Fox, K. 1992. “A Critical Period for Experience-Dependent Synaptic Plasticity in Rat Barrel Cortex.” Journal of Neuroscience 12(5):1826–38.
Frishman, Fred. 1975. “On the Arithmetic Means and Variances of Products and Ratios of Random Variables.” Pp. 401–6 in A Modern Course on Statistical Distributions in Scientific Work. Dordrecht: Springer Netherlands.
Fu, Min, Xinzhu Yu, Ju Lu, and Yi Zuo. 2012. “Repetitive Motor Learning Induces Coordinated Formation of Clustered Dendritic Spines in Vivo.” Nature 483(7387):92–95.
Fujimoto, H., T. Hasegawa, and D. Watanabe. 2011. “Neural Coding of Syntactic Structure in Learned Vocalizations in the Songbird.” Journal of Neuroscience 31(27):10023–33.
Fuxe, Kjell, Tomas Hökfelt, Gösta Jonsson, and Urban Ungerstedt. 1970. “Fluorescence Microscopy in Neuroanatomy.” Pp. 275–314 in Contemporary Research Methods in Neuroanatomy. Berlin, Heidelberg: Springer Berlin Heidelberg.
Gahr, Manfred. 1990. “Delineation of a Brain Nucleus: Comparisons of Cytochemical, Hodological, and Cytoarchitectural Views of the Song Control Nucleus HVC of the Adult Canary.” Journal of Comparative Neurology 294(1):30–36.
196
Geinisman, Yuri, H. J. Gundersen, E. van der Zee, and Mark J. West. 1996. “Unbiased Stereological Estimation of the Total Number of Synapses in a Brain Region.”
Journal of Neurocytology 25(12):805–19.
Gelman, Andrew and Jennifer Hill. 2007. Data Analysis Using Regression and Multilevel/hierarchical Models.
Gerfen, Charles R. and Paul E. Sawchenko. 2016. “An Anterograde Neuroanatomical Tracing Method That Shows the Detailed Morphology of Neurons, Their Axons and Terminals: Immunohistochemical Localization of an Axonally Transported Plant Lectin, Phaseolus Vulgaris-Leucoagglutinin (PHA-L).” Brain Research 1645:42–45.
Gilbert, Marcoita T. and Ken Soderstrom. 2011. “Late-Postnatal Cannabinoid Exposure Persistently Elevates Dendritic Spine Densities in Area X and HVC Song Regions of Zebra Finch Telencephalon.” Brain Research 1405:23–30.
Goldberg, J. H. and M. S. Fee. 2011. “Vocal Babbling in Songbirds Requires the Basal Ganglia-Recipient Motor Thalamus but Not the Basal Ganglia.” Journal of Neurophysiology 105(6):2729–39.
Goodman, Leo A. 1960. “On the Exact Variance of Products.” Journal of the American Statistical Association 55(292):708–13.
Gray, E. G. 1959. “Axo-Somatic and Axo-Dendritic Synapses of the Cerebral Cortex.”
Journal of Anatomy 93(Pt 4):420–33.
Gray, E. G. 1969. “Electron Microscopy of Excitatory and Inhibitory Synapses: A Brief Review.” Progress in Brain Research 31(C):141–55.
Griffiths, Gareth. 1993. Fine Structure Immunocytochemistry. Berlin, Heidelberg:
Springer Berlin Heidelberg.
Groen, M. R., O. Paulsen, E. Perez-Garci, T. Nevian, J. Wortel, M. P. Dekker, H. D.
Mansvelder, A. van Ooyen, and R. M. Meredith. 2014. “Development of Dendritic Tonic GABAergic Inhibition Regulates Excitability and Plasticity in CA1
Pyramidal Neurons.” Journal of Neurophysiology 112(2):287–99.
Grutzendler, Jaime and Wen Biao Gan. 2006. “Two-Photon Imaging of Synaptic Plasticity and Pathology in the Living Mouse Brain.” NeuroRx 3(4):489–96.
Hahnloser, Richard H. R., Alexay a Kozhevnikov, and Michale S. Fee. 2002. “An Ultra-Sparse Code Underlies the Generation of Neural Sequences in a Songbird.”
Nature 419(6902):65–70.
Harris, K. M., J. C. Fiala, and L. Ostroff. 2003. “Structural Changes at Dendritic Spine Synapses during Long-Term Potentiation.” Philosophical Transactions of the Royal Society B: Biological Sciences 358(1432):745–48.
Harris, K. M., E. Perry, J. Bourne, M. Feinberg, L. Ostroff, and J. Hurlburt. 2006.
“Uniform Serial Sectioning for Transmission Electron Microscopy.” Journal of Neuroscience 26(47):12101–3.
Hayashi-Takagi, Akiko, Sho Yagishita, Mayumi Nakamura, Fukutoshi Shirai, Yi I. Wu, Amanda L. Loshbaugh, Brian Kuhlman, Klaus M. Hahn, and Haruo Kasai. 2015.
“Labelling and Optical Erasure of Synaptic Memory Traces in the Motor Cortex.”
197
Nature 525(7569):333–38.
Hayworth, Kenneth J. 2012. “Electron Imaging Technology for Whole Brain Neural Circuit Mapping.” International Journal of Machine Consciousness 4(1):87–108.
Helmchen, Fritjof and Winfried Denk. 2005. “Deep Tissue Two-Photon Microscopy.”
Nature Methods 2(12):932–40.
Helmstaedter, Moritz, Kevin L. Briggman, and Winfried Denk. 2008. “3D Structural Imaging of the Brain with Photons and Electrons.” Current Opinion in Neurobiology 18(6):633–41.
Helmstaedter, Moritz, Kevin L. Briggman, Srinivas C. Turaga, Viren Jain, H.Sebastian Seung, and Winfried Denk. 2013. “Connectomic Reconstruction of the Inner Plexiform Layer in the Mouse Retina.” Nature 500(7461):168–74.
Hensch, T. K. 1998. “Local GABA Circuit Control of Experience-Dependent Plasticity in Developing Visual Cortex.” Science 282(5393):1504–8.
Hensch, Takao K. 2004. “Critical Period Regulation.” Annual Review of Neuroscience 27:549–79.
Hensch, Takao K. 2005. “Critical Period Plasticity in Local Cortical Circuits.” Nature Reviews Neuroscience 6(11):877–88.
Hensch, Takao K. and Michela Fagiolini. 2004. “Excitatory-Inhibitory Balance and Critical Period Plasticity in Developing Visual Cortex.” Progress in Brain Research 147(SPEC. ISS.):115–24.
Herbst, Joshua Aaron. 2013. “The Role of Spontaneous Neural Activity for Song Development.” Diss., Eidgenössische Technische Hochschule ETH Zürich, Nr.
21216.
Herrmann, Kathrin and Hans-Joachim Bischof. 1986. “Delayed Development of Song Control Nuclei in the Zebra Finch Is Related to Behavioral Development.” Journal of Comparative Neurology 245(2):167–75.
Hofer, S. B., T. D. Mrsic-Flogel, T. Bonhoeffer, and M. Hübener. 2009. “Experience Leaves a Lasting Structural Trace in Cortical Circuits.” Nature 457(January):313–
17.
Holtmaat, Anthony and Karel Svoboda. 2009. “Experience-Dependent Structural Synaptic Plasticity in the Mammalian Brain.” Nature Reviews Neuroscience 10(10):759–759.
Holtmaat, Anthony, Linda Wilbrecht, Graham W. Knott, Egbert Welker, and Karel Svoboda. 2006. “Experience-Dependent and Cell-Type-Specific Spine Growth in the Neocortex.” Nature 441(7096):979–83.
Hubel, D. H. and T. N. Wiesel. 1970. “The Period of Susceptibility to the Physiological Effects of Unilateral Eye Closure in Kittens.” The Journal of Physiology
206(2):419–36.
Immelmann, K. 1969. “Song Development in the Zebra Finch and Other Estrildid Finches.” Bird Vocalizations 61–74.
Iwai, Youichi, Michela Fagiolini, Kunihiko Obata, and Takao K. Hensch. 2003. “Rapid
198
Critical Period Induction by Tonic Inhibition in Visual Cortex.” The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 23(17):6695–
6702.
Janata, P. and D. Margoliash. 1999. “Gradual Emergence of Song Selectivity in Sensorimotor Structures of the Male Zebra Finch Song System.” The Journal of Neuroscience : The Official Journal of the Society for Neuroscience 19(12):5108–
18.
Johnson, Frank, Ken Soderstrom, and Osceola Whitney. 2002. “Quantifying Song Bout Production during Zebra Finch Sensory-Motor Learning Suggests a Sensitive Period for Vocal Practice.” Behavioural Brain Research 131(1–2):57–65.
Kandel, Eric R., James H. Schwartz, and Thomas M. Jessell. 2013. Principles of Neural Science.
Keller, Georg B. and Richard H. R. Hahnloser. 2009. “Neural Processing of Auditory Feedback during Vocal Practice in a Songbird.” Nature 457(7226):187–90.
Kirkwood, A., H. K. Lee, and Mark F. Bear. 1995. “Co-Regulation of Long-Term Potentiation and Experience-Dependent Synaptic Plasticity in Visual Cortex by Age and Experience.” Nature 375(6529):328–31.
Klemann, Cornelius J. H. M. and Eric W. Roubos. 2011. “The Gray Area between Synapse Structure and Function-Gray’s Synapse Types I and II Revisited.”
Synapse 65(11):1222–30.
Knott, G., H. Marchman, D. Wall, and B. Lich. 2008. “Serial Section Scanning Electron Microscopy of Adult Brain Tissue Using Focused Ion Beam Milling.” Journal of Neuroscience 28(12):2959–64.
Knott, Graham, Stéphanie Rosset, and Marco Cantoni. 2011. “Focussed Ion Beam Milling and Scanning Electron Microscopy of Brain Tissue.” Journal of Visualized Experiments (53):3–6.
Knott, Graham W., Anthony Holtmaat, Linda Wilbrecht, Egbert Welker, and Karel
Knott, Graham W., Anthony Holtmaat, Linda Wilbrecht, Egbert Welker, and Karel