runl I IUI%I/\L Magnetic Resonance Imaging

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1 runl I IUI%I/\L Magnetic Resonance Imaging SECOND EDITION Scott A. HuetteS Brain Imaging and Analysis Center, Duke University Allen W. Song Brain Imaging and Analysis Center, Duke University Gregory McCarthy Yale University Д А 1 Sinauer Associates, Inc Publishers WM} Sunderland, Massachusetts U.S.A.

2 Contents Preface xiii introduction to fmri What Is fmri? 3 Measurement versus manipulation techniques 4 Box 1.1 WHAT IS FMRI USED FOR? 6 Key concept: contrast 9 Key concept: resolution 11 History of fmri 15 Early studies of magnetic resonance 15 NMR in bulk matter: Bloch and Purcell 17 The first MR images 18 Growth of MRI 21 Box 1.2 THE NOBEL CONTROVERSY: SCANNERS OR IMAGES? 22 Organization of the Textbook 24 Physical bases of fmri 25 Principles of BOLD fmri 25 Design and analysis of fmri experiments 26 Applications and future directions 27 Summary 28 I MRI Scanners 31 How MRI Scanners Work 31 Static magnetic field 32 Radiofrequency coils 35 Gradient coils 38 Shimming coils 41 Computer hardware and software 41 Experimental control system 43 Physiological monitoring equipment 43 MRI Safety 44 Effects of static magnetic fields on human physiology 44 Box 2.1 OUTLINE OF AN FMRI EXPERIMENT 45 Translation and torsion 49 Gradient magnetic field effects 50 Radiofrequency field effects 52 Claustrophobia 53 Acoustic noise 54 Summary 54 Suggested Reading 55 Chapter References 55 Suggested Reading 28 Chapter References 29

3 viii Contents 4 Basic Principles of MR Image Formation 89 CONCEPTUAL PATH 90 Slice Selection 91 3 Basic Principles of MR Signal Generation 57 CONCEPTUAL PATH 57 Nuclear Spins 59 Spins in an External Magnetic Field 60 Magnetization of a Spin System 62 Excitation of a Spin System and Signal Reception 64 Relaxation Mechanisms of the MR Signal 65 Conceptual Summary of MR Signal Generation 67 QUANTITATIVE PATH 68 Common Terms and Notations 68 Nuclear Spins 69 Magnetic Moment 69 Angular Momentum 70 Spins in an External Magnetic Field 71 Spin precession 71 Energy Difference between Parallel and Antiparallel States 74 Magnetization of a Spin System 75 Excitation of a Spin System and Signal Reception 77 Spin excitation 78 Box 3.1 A QUANTITATIVE CONSIDERATION OF THE ROTATING REFERENCE FRAME 80 Signal reception 83 Relaxation Mechanisms of a Spin System 85 The Bloch Equation for MR signal generation 87 Summary 87 Suggested Reading 88 5 MR Frequency Encoding 93 Phase Encoding 95 Conceptual Path: Summary of Image Formation 96 QUANTITA TIVE PA TH 97 Analysis of the MR Signal 97 Box 4.1 AN EXAMPLE OF SPATIAL ENCODING 98 Longitudinal magnetization (M z ) 101 Solution for transverse magnetization (M xy ) 102 The MR signal equation 105 Slice Selection, Spatial Encoding, and Image Reconstruction 106 Slice selection 106 Two-dimensional spatial encoding (frequency and phase encoding) 109 Relationship between image space and /c-space 113 Converting from fc-space to image space D Imaging 117 Potential Problems in Image Formation 117 Summary 120 Suggested Reading 120 Contrast Mechanisms and Pulse Sequences 121 Static Contrasts and Related Pulse Sequences 122 Proton-density contrast 123 Tj contrast 126 T 2 contrast 129 T 2 * contrast 131 Chemical contrast 132 Macromolecular contrast 133 Motion Contrasts 135 MR angiography 135 Diffusion-weighted contrast 138 Box 5.1 DIFFUSION TENSOR IMAGING 140 Perfusion-weighted contrast 142

4 Contents ix Fast Imaging Sequences for fmri 147 Echo-planar imaging 147 Spiral imaging 148 Signal recovery and distortion correction for EPI and spiral images 152 Summary 154 Suggested Reading 156 Chapter References 157 From Neuronal to Hemodynamic Activity 159 Neuronal Activity 160 Ion channels in neurons 162 Neurotransmitters and action potentials 163 Cerebral Metabolism: Neuronal Energy Consumption 165 Adenosine triphosphate (ATP) 166 The Vascular System of the Brain 168 Arteries, capillaries, and veins 170 Arterial and venous anatomy of the human brain 171 Microcirculation 172 Blood Flow 174 Control of blood flow 175 Box 6.1 NEUROVASCULAR COUPLING AND CONTROL OF BLOOD FLOW 176 Effects of increased blood flow on capillaries 179 Box 6.2 PRIMER ON NEUROANATOMY 182 Summary 190 Suggested Reading 190 Chapter References 191 Э BOLD fmri: Origins and Properties 193 History of BOLD fmri 193 Discovery of BOLD contrast 194 The coupling of metabolism and blood flow 196 Box 7.1 PET IMAGING 197 The Growth of BOLD fmri 201 Contributing factors 201 Early fmri studies 203 Box 7.2 FUNCTIONAL STUDIES USING CONTRAST AGENTS 204 The BOLD Hemodynamic Response 208 Box 7.3 NEURONAL ACTIVITY AND BOLD FMRI 209 The initial dip 211 Spatial Resolution 214 Spatial specificity in the vascular system 216 What spatial resolution is needed? 219 Temporal Resolution of fmri 220 What temporal resolution is needed? 223 Effects of stimulus duration and timing 225 Linearity of the Hemodynamic Response 229 Properties of a linear system 230 Evidence for rough linearity 231 Challenges to linearity 233 fmri-adaptation 235 Summary 237 Suggested Reading 238 Chapter References 239 Signal, Noise, and Preprocessing of fmri uata Am Understanding Signal and Noise 245 Signal and noise defined 245 Box 8.1 TERMINOLOGY OF FMRI 246 Functional SNR 248 Effects of Field Strength on fmri Data 250 Field strength and raw SNR 251 Field strength and spatial properties of activation 252 Challenges of high-field fmri 254

5 x Contents Sources of Noise in fmri 255 Thermal noise 256 System noise 258 Motion and physiological noise 259 Non-task-related neural variability 262 Behavioral and cognitive variability in task performance 262 Box 8.2 VARIABILITY IN THE HEMODYNAMIC RESPONSE OVER SUBJECTS AND SESSIONS 264 Preprocessing 267 Quality assurance 267 Slice acquisition time correction 269 Head motion: an overview 271 Prevention of head motion 274 Correction of head motion 276 Distortion correction 277 Functional-Structural Coregistration and Normalization 280 Functional-structural coregistration 280 Spatial normalization 281 Temporal and Spatial Filtering 284 Temporal filtering 285 Spatial filtering 287 Summary 289 Suggested Reading 289 Chapter References 290 Experimental Design 293 Basic Principles of Experimental Design 294 Setting Up a Good Research Hypothesis 296 Are fmri data correlational? 298 Confounding factors 299 Good Practices in fmri Experimental Design 302 Blocked Designs 303 Setting up a blocked design 304 Box 9.1 BASELINE ACTIVATION IN FMRI 306 Advantages and disadvantages of blocked designs 310 Event-Related Designs 313 Principles of event-related fmri 316 Advantages of event-related designs 319 Box 9.2 EFFICIENT FMRI EXPERIMENTAL DESIGN 320 Mixed Designs 325 Summary 327 Suggested Reading 327 Chapter References 328 Statistical Analysis: Basic Analyses 337 Basic Statistical Tests 333 Contrasting experimental conditions: the West 334 Comparing experimental and predicted responses: correlation analyses 338 Box 10.1 IDENTIFYING TASK-RELATED PERIODICITY: FOURIER ANALYSES 341 Regression Analyses 343 The general linear model: an overview 343 Constructing a design matrix: regressors of interest 345 Constructing a design matrix: nuisance regressors 349 Modeling neuronal activity 351 Modeling hemodynamic convolution 352 Contrasts 354 Assumptions of the general linear model 356 Corrections for Multiple Comparisons 357 Calculating the significance threshold 358 Thresholding based on clusters of activation 360 Estimating the number of independent tests 361 Region-of-lnterest Analyses 362 Intersubject Analyses 365 Group and parametric effects 367 Displaying Statistical Results 369 Summary 373 Suggested Reading 373 Chapter References 374

6 Contents xi Statistical Analysis it JL Advanced Approaches 377 Data Exploration Approaches 378 Principal components analysis (PCA) 378 Independent components analysis (ICA) 380 Partial least squares (PLS) 382 Between-Subjects Correlations: Hyperscanning 384 Functional Connectivity Approaches 386 From coactivation to connectivity: a conceptual overview 386 BOX 11.1 INTERSUBJECT CORRELATIONS IN FREE VIEWING 387 Resting-state connectivity 391 Psychophysiological interactions 393 Inferring causality from fmri data 394 Combining fmri and DTI 399 Prediction Approaches 401 Predicting variation among individuals 402 Box 11.2 REAL-TIME FMRI 403 Predicting variation in behavior 407 Pattern classification using machine learning algorithms 408 Capabilities and challenges of fmri pattern classification 412 Summary 415 Suggested Reading 416 Chapter References 416 Advanced fmri Methods 419 Improved Spatial Resolution 420 MR microscopy 420 Parallel imaging 423 Parallel imaging with massive coil arrays 425 Improved Temporal Resolution 426 Multiple-channel acquisition 427 Partial fc-space imaging 427 Efficient fc-space trajectories 430 Improved experimental designs 432 Improved Functional Resolution through New Contrast Mechanisms 433 Temperature-dependent contrast 434 ph-dependent contrast 435 Ion-gated contrast 437 Neuronal magnetic field contrast 438 Lorentz effect contrast 439 Summary 440 Suggested Reading 441 Chapter References 441 Combining fmri with other Techniques 443 Cognitive Neuroscience 443 Strategies for research in cognitive neuroscience 445 Manipulating Brain Function 446 Direct cortical stimulation 446 Functional consequences of direct cortical stimulation 448 Transcranial magnetic stimulation (TMS) 450 Brain lesions 452 Combined lesion and fmri studies 454 Probabilistic brain atlases 455 Brain imaging and genomics 457 Measuring Brain Function 458 Single-unit recording 458 Box 13.1 ELECTROGENESIS 459 Limitations of single-unit recording 462 Properties of electrical field potentials 464 Localizing the neural generators of field potentials 465

7 xii Contents The Future of fmri: Practical and Ethical Issues 485 Introduction 485 Intracranially recorded field potentials 466 Box 13.2 LOCALIZATION OF FUNCTION USING FIELD POTENTIAL RECORDINGS 468 Scalp-recorded field potentials 470 Box 13.3 COMBINING FMRI AND EEG/ERP TECHNIQUES 472 Magnetoencephalography 474 Using fmri with non-human primates 476 Summary 480 Suggested Reading 480 Chapter References 481 Interpreting and Presenting fmri Data 486 Coverage of fmri research in the popular media 487 Core principles for presenting fmri research 489 Box 14.1 REVERSE INFERENCE 490 Conducting fmri Research 494 Proposing and approving fmri research 495 Ensuring the confidentiality of fmri data 497 Box 14.2 INCIDENTAL FINDINGS IN FMRI RESEARCH 498 Safe conduct of fmri studies 502 Pregnancy testing in fmri research 504 Applying fmri to New and Controversial Topics 505 Reading minds 506 Identifying traits 509 The Future of fmri Research (and your role in it) 511 Summary 513 Suggested Reading 515 Chapter References 515 Glossary 517 Index 533

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