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Dissertation.Pdf Population oscillations along the cortico-striatal axis of awake behaving rats Dissertation Zur Erlangung der Würde des Doktors der Naturwissenschaften des Department Biologie der Fakultät für Mathematik, Informatik und Naturwissenschaften der Universität Hamburg vorgelegt von Constantin von Nicolai aus Bonn Hamburg, 2012 Genehmigt vom Fachbereich Biologie der Universitdt Hamburg auf Antrag von Herrn Professor Dr. A. K. Engel Weitere Gutachter der Dissertation: Herr Professor Dr. C. Lohr Tag der Disputation: 17. Februar 2012 Hamburg, den 02. Februar 2n12 b\^,,L'^f d-*^T Professor Dr. J. Fromm Vorsitzender des P romotionsausschusses As in evolution, “what might have been” is not relevant. —Greg Graffin Contents Figures and Tables iv Abbreviations vi Abstract vii 1 Introduction 1 1.1 Cerebral cortex-basal ganglia circuitry . .1 1.1.1 General anatomical outline . .1 1.1.2 Functional anatomy of cortico-basal ganglia loops . .3 1.1.3 Functional role of cortico-basal ganglia systems . .4 1.2 The cortico-striatal axis . .6 1.2.1 Macroscopic and microscopic anatomy of the striatum . .6 1.2.2 Functional anatomy of the cortico-striatal axis . .8 1.2.3 Functional role of the cortico-striatal axis . 11 1.3 Synchrony and oscillations of neuronal activities . 13 1.3.1 General considerations . 13 1.3.2 Synchrony and oscillations in cortico-basal ganglia systems . 18 1.3.3 Synchrony and oscillations along the cortico-striatal axis . 20 1.4 Aims and motivation of the study . 22 2 Methods 23 2.1 Treadmill apparatus and behavioral environment . 23 2.2 Animal care and handling . 25 2.3 Implants and implantations . 26 2.3.1 Target planning . 26 2.3.2 Implant construction . 28 2.3.3 Surgical procedures . 30 2.4 Recording environment and data acquisition . 33 2.4.1 Electrode displacement during rest . 33 2.4.2 Recording conditions during treadmill running . 33 i Contents 2.4.3 Data acquisition, online processing, and storage . 35 2.5 Behavioral task . 35 2.6 Data preprocessing . 37 2.6.1 Signal quality evaluation . 37 2.6.2 Preprocessing of Local Field Potentials (LFP) . 39 2.6.2.1 Resampling and digital filtering . 39 2.6.2.2 Bipolar derivations . 41 2.6.3 Preprocessing of Multi-Unit Activities (MUA) . 42 2.7 Data analysis . 43 2.7.1 Behavioral analysis . 43 2.7.2 Firing rate analysis . 44 2.7.3 Spectral analyses . 44 2.7.3.1 Fourier transform-based frequency analysis . 44 2.7.3.2 Wavelet transform-based time-frequency analysis . 45 2.7.3.3 Power analysis . 50 2.7.3.4 Coherency analysis . 52 2.7.3.5 Phase analysis . 53 2.7.3.6 Phase-amplitude analysis . 56 2.7.3.7 Power correlation analysis . 57 2.7.3.8 Phase-locking–power intercorrelation analysis . 59 2.7.4 Statistical specifications . 59 2.8 Computational implementation . 63 3 Results 64 3.1 Behavior . 64 3.2 Firing rates . 66 3.3 Power ...................................... 67 3.3.1 Power: Local Field Potentials . 68 3.3.1.1 Raw LFP power . 68 3.3.1.2 Percentage LFP power . 70 3.3.2 Power: Multi-Unit Activities (MUA) . 72 3.3.2.1 Raw MUA power . 72 3.3.2.2 Percentage MUA power . 73 3.4 Coherency . 74 3.4.1 Coherency: Local Field Potentials (LFP) . 74 3.4.1.1 Ordinary LFP coherence . 74 3.4.1.2 Imaginary LFP coherence . 77 ii Contents 3.4.2 Coherency: Multi-Unit Activities (MUA) . 78 3.4.3 Spike-Field (LFP-MUA) coherency . 79 3.5 Phase . 82 3.5.1 LFP phase-locking . 82 3.5.2 LFP phase angles . 85 3.5.3 Cross-hemispheric LFP phase-coupling . 85 3.6 Phase-amplitude coupling . 89 3.7 Power correlation . 92 3.8 Phase-locking–power interrelation . 95 3.9 Peak-frequency changes . 98 3.9.1 Power peaks . 99 3.9.2 Phase-locking peaks . 101 4 Discussion 104 4.1 Methodological considerations . 104 4.1.1 Behavioral model . 104 4.1.2 Recording setup . 106 4.1.3 Implantation issues . 106 4.1.4 Electrode positions . 107 4.1.5 Data quality . 108 4.1.6 Volume conduction . 109 4.1.7 Bipolar derivations . 110 4.1.8 Signal analysis . 112 4.1.9 LFP origins . 112 4.2 LFP power characteristics . 113 4.3 LFP phase-coupling characteristics . 117 4.4 LFP cross-frequency interactions . 121 4.4.1 LFP phase-amplitude coupling . 121 4.4.2 LFP power correlations . 122 4.5 LFP coupling interrelations . 124 4.6 Multi-unit activities . 125 4.7 Functional implications . 126 4.8 Future directions . 138 References 140 Appendices 167 iii Figures and Tables List of Figures 1.1 Anatomical outline of the cortico-basal ganglia network . .2 1.2 Canonical microcircuit of the striatum . .7 1.3 Organization of cortico-striatal projections . 10 1.4 Oscillatory synchronization as a means of neuronal communication . 17 2.1 Treadmill device . 24 2.2 Brain slice drawing of electrode implantation sites . 27 2.3 Original and modified implant device . 29 2.4 Illustration of implant placement site . 32 2.5 Treadmill apparatus inside of recording chamber . 34 2.6 Behavioral task protocol during recordings . 36 2.7 Signal quality evaluation: amplitude thresholding . 37 2.8 Signal quality evaluation: stability tests . 38 2.9 Effects of notch-, high-, and low-pass filtering . 40 2.10 Creation of bipolar derivations from LFP recordings . 41 2.11 Spike detection through amplitude thresholding . 43 2.12 Characteristics of continuous wavelet transforms . 48 2.13 Time-frequency analysis using continuous wavelets transforms . 50 2.14 Illustration of power, coherency, and phase analyses . 55 2.15 Principles of phase-amplitude coupling analysis . 56 2.16 Power correlation analysis . 58 2.17 Time series shift-based statistics . 62 3.1 Behavioral performance . 65 3.2 Multi-unit firing rates . 67 3.3 Raw LFP power. 69 3.4 Percentage LFP power . 71 3.5 Raw MUA power . 72 iv List of Tables 3.6 Percentage MUA power . 73 3.7 Ordinary LFP coherence . 75 3.8 Ordinary LFP coherence difference . 76 3.9 Imaginary LFP coherence . 77 3.10 Imaginary LFP coherence difference . 78 3.11 MUA coherence . 79 3.12 MUA coherence difference . 79 3.13 LFP-MUA coherence . 80 3.14 LFP-MUA coherence difference . 81 3.15 LFP phase-locking and coherence–phase-locking ratio . 83 3.16 LFP phase-locking difference . 84 3.17 LFP phase angles . 86 3.18 Cross-hemispheric LFP phase-coupling . 88 3.19 Phase-amplitude.
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