Midbrain fMRI: Applications, Limitations and Challenges

The human midbrain and pons contain nuclei of major neurotransmitter systems that send long-range projections to regulate brain activity in cortical and subcortical structures. Despite being small structures, these nuclei are critically implicated in a very wide range of cognitive and bodily functions, and their dysfunction plays an important role in a number of neurological and neuropsychiatric conditions. Hence, there is a considerable interest to develop functional MRI approaches that allow to image their activity in health and disease.

[1]  E. Düzel,et al.  Personality Traits Are Differentially Associated with Patterns of Reward and Novelty Processing in the Human Substantia Nigra/Ventral Tegmental Area , 2009, Biological Psychiatry.

[2]  H. Heinze,et al.  Reward-Related fMRI Activation of Dopaminergic Midbrain Is Associated with Enhanced Hippocampus- Dependent Long-Term Memory Formation , 2005, Neuron.

[3]  Olivia K. Faull,et al.  Physiological Noise in Brainstem fMRI , 2013, Front. Hum. Neurosci..

[4]  R. Dolan,et al.  Structural integrity of the substantia nigra and subthalamic nucleus predicts flexibility of instrumental learning in older-age individuals , 2013, Neurobiology of Aging.

[5]  H. Heinze,et al.  Mesolimbic Functional Magnetic Resonance Imaging Activations during Reward Anticipation Correlate with Reward-Related Ventral Striatal Dopamine Release , 2008, The Journal of Neuroscience.

[6]  Karl Friston.  Neurophysiology: The Brain at Work , 2008, Current Biology.

[7]  S. H. Koenig,et al.  Sources of the increased longitudinal relaxation rates observed in melanotic melanoma. An in vitro study of synthetic melanins. , 1989, Investigative radiology.

[8]  B. Forstmann,et al.  Direct visualization of the subthalamic nucleus and its iron distribution using high‐resolution susceptibility mapping , 2012, Human brain mapping.

[9]  S Robinson,et al.  Optimized 3 T EPI of the amygdalae , 2004, NeuroImage.

[10]  Scott D. Brown,et al.  Cortico-striatal connections predict control over speed and accuracy in perceptual decision making , 2010, Proceedings of the National Academy of Sciences.

[11]  W. Nauta,et al.  Efferent connections of the substantia nigra and ventral tegmental area in the rat , 1979, Brain Research.

[12]  G. Aston-Jones,et al.  Locus coeruleus neurons in monkey are selectively activated by attended cues in a vigilance task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  N. Pelc,et al.  Brain motion: measurement with phase-contrast MR imaging. , 1992, Radiology.

[14]  Myung-Ho In,et al.  Highly accelerated PSF-mapping for EPI distortion correction with improved fidelity , 2012, Magnetic Resonance Materials in Physics, Biology and Medicine.

[15]  Michael J. Bannon,et al.  Age‐related and regional differences in dopamine transporter mRNA expression in human midbrain , 1997, Neurology.

[16]  M. Ungless,et al.  Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli , 2009, Proceedings of the National Academy of Sciences.

[17]  Oliver Speck,et al.  Magnetic resonance imaging of freely moving objects: prospective real-time motion correction using an external optical motion tracking system , 2006, NeuroImage.

[18]  Ruth M. Krebs,et al.  Novelty increases the mesolimbic functional connectivity of the substantia nigra/ventral tegmental area (SN/VTA) during reward anticipation: Evidence from high-resolution fMRI , 2011, NeuroImage.

[19]  Jens Frahm,et al.  COMMENTS AND CONTROVERSIES Functional MRI of the Human Amygdala , 2001 .

[20]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

[21]  D. Joel,et al.  The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum , 2000, Neuroscience.

[22]  E. Szabadi,et al.  Functional Neuroanatomy of the Noradrenergic Locus Coeruleus: Its Roles in the Regulation of Arousal and Autonomic Function Part I: Principles of Functional Organisation , 2008, Current neuropharmacology.

[23]  B. Moghaddam,et al.  Target‐Specific Glutamatergic Regulation of Dopamine Neurons in the Ventral Tegmental Area , 2000, Journal of neurochemistry.

[24]  G. Aston-Jones,et al.  Conditioned responses of monkey locus coeruleus neurons anticipate acquisition of discriminative behavior in a vigilance task , 1997, Neuroscience.

[25]  J. Bolam,et al.  Activity of Neurochemically Heterogeneous Dopaminergic Neurons in the Substantia Nigra during Spontaneous and Driven Changes in Brain State , 2009, The Journal of Neuroscience.

[26]  Raymond J. Dolan,et al.  Anticipation of novelty recruits reward system and hippocampus while promoting recollection , 2007, NeuroImage.

[27]  Samuel M. McClure,et al.  BOLD Responses Reflecting Dopaminergic Signals in the Human Ventral Tegmental Area , 2008, Science.

[28]  L. Swanson.  The locus coeruleus: A cytoarchitectonic, golgi and immunohistochemical study in the albino rat , 1976, Brain Research.

[29]  Peter Boesiger,et al.  Assessment of human brain motion using CSPAMM , 2007, Journal of magnetic resonance imaging : JMRI.

[30]  Afonso C. Silva,et al.  Elevated endogenous GABA level correlates with decreased fMRI signals in the rat brain during acute inhibition of GABA transaminase , 2005, Journal of neuroscience research.

[31]  Yoshiharu Tamakawa,et al.  The substantia nigra in Parkinson disease: proton density-weighted spin-echo and fast short inversion time inversion-recovery MR findings. , 2002, AJNR. American journal of neuroradiology.

[32]  S. Sara,et al.  Reward expectation, orientation of attention and locus coeruleus‐medial frontal cortex interplay during learning , 2004, The European journal of neuroscience.

[33]  J. Gore,et al.  Using High-Resolution MR Imaging at 7T to Evaluate the Anatomy of the Midbrain Dopaminergic System , 2011, American Journal of Neuroradiology.

[34]  A. Grace,et al.  The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  O. Hikosaka,et al.  Lateral habenula as a source of negative reward signals in dopamine neurons , 2007, Nature.

[36]  Christophe Phillips,et al.  Response to Comment on “Homeostatic Sleep Pressure and Responses to Sustained Attention in the Suprachiasmatic Area” , 2010, Science.

[37]  Jonathan D. Cohen,et al.  Computational roles for dopamine in behavioural control , 2004, Nature.

[38]  C. Berridge,et al.  The locus coeruleus–noradrenergic system: modulation of behavioral state and state-dependent cognitive processes , 2003, Brain Research Reviews.

[39]  Andrew J. Watrous,et al.  Modafinil Shifts Human Locus Coeruleus to Low-Tonic, High-Phasic Activity During Functional MRI , 2008, Science.

[40]  A. Grace,et al.  Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission , 2003, Nature Neuroscience.

[41]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[42]  Karl J. Friston,et al.  Nonlinear Dynamic Causal Models for Fmri Nonlinear Dynamic Causal Models for Fmri Nonlinear Dynamic Causal Models for Fmri , 2022 .

[43]  F. Bloom,et al.  Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  S. Sara,et al.  Orienting and Reorienting: The Locus Coeruleus Mediates Cognition through Arousal , 2012, Neuron.

[45]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[46]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[47]  A. R. Cools,et al.  Bilateral nigral 6-hydroxydopamine lesions increase the amount of extracellular dopamine in the nucleus accumbens , 2005, Experimental Neurology.

[48]  M. Zaitsev,et al.  High resolution single-shot EPI at 7T , 2008, Magnetic Resonance Materials in Physics, Biology and Medicine.

[49]  Olaf Dössel,et al.  Optimized EPI for fMRI using a slice-dependent template-based gradient compensation method to recover local susceptibility-induced signal loss , 2010, Magnetic Resonance Materials in Physics, Biology and Medicine.

[50]  Xiaoping Hu,et al.  Simultaneous imaging of locus coeruleus and substantia nigra with a quantitative neuromelanin MRI approach. , 2014, Magnetic resonance imaging.

[51]  R Turner,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex , 2003, NeuroImage.

[52]  Nikolaus Weiskopf,et al.  Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: A whole-brain analysis at 3 T and 1.5 T , 2006, NeuroImage.

[53]  S. Sesack,et al.  Anatomical Substrates for Glutamate‐Dopamine Interactions , 2003 .

[54]  Berrin Maraşligil,et al.  İnsanlarda Yenilik N2 Yanıtı Hedef Uyaranların Zamansal Sınıflamasını Yansıtır , 2011 .

[55]  Zhiming Zhang,et al.  Assessing nigrostriatal dysfunctions by pharmacological MRI in parkinsonian rhesus macaques , 2006, NeuroImage.

[56]  S. Nieuwenhuis,et al.  The anatomical and functional relationship between the P3 and autonomic components of the orienting response. , 2011, Psychophysiology.

[57]  W. Pan,et al.  Pedunculopontine Tegmental Nucleus Controls Conditioned Responses of Midbrain Dopamine Neurons in Behaving Rats , 2005, The Journal of Neuroscience.

[58]  P. Dayan,et al.  Behavioral/systems/cognitive Action Dominates Valence in Anticipatory Representations in the Human Striatum and Dopaminergic Midbrain , 2010 .

[59]  P. Tobler,et al.  Functional imaging of the human dopaminergic midbrain , 2009, Trends in Neurosciences.

[60]  Joseph V. Hajnal,et al.  Identification and characterisation of midbrain nuclei using optimised functional magnetic resonance imaging , 2012, NeuroImage.

[61]  Elyssa B. Margolis,et al.  Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. , 2007, Annual review of neuroscience.

[62]  Steen Moeller,et al.  Multiband multislice GE‐EPI at 7 tesla, with 16‐fold acceleration using partial parallel imaging with application to high spatial and temporal whole‐brain fMRI , 2010, Magnetic resonance in medicine.

[63]  M. Hariz,et al.  Stereotactic localization of the human pedunculopontine nucleus: atlas-based coordinates and validation of a magnetic resonance imaging protocol for direct localization. , 2008, Brain : a journal of neurology.

[64]  C. Fiorillo.  Two Dimensions of Value: Dopamine Neurons Represent Reward But Not Aversiveness , 2013, Science.

[65]  Peter Riederer,et al.  The relevance of iron in the pathogenesis of Parkinson’s disease , 2011, Journal of neurochemistry.

[66]  Lawrence L. Wald,et al.  Comparison of physiological noise at 1.5 T, 3 T and 7 T and optimization of fMRI acquisition parameters , 2005, NeuroImage.

[67]  Hiroshi Kawahara,et al.  The locus coeruleus noradrenergic system in the rat brain studied by dual-probe microdialysis , 1997, Brain Research.

[68]  L. Zrinzo,et al.  Surgical anatomy of the pedunculopontine and peripeduncular nuclei , 2008, British journal of neurosurgery.

[69]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[70]  Hans-Jochen Heinze,et al.  Mesolimbic novelty processing in older adults. , 2007, Cerebral cortex.

[71]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[72]  R. Habib,et al.  Activation of midbrain structures by associative novelty and the formation of explicit memory in humans. , 2004, Learning & memory.

[73]  Stephen M. Smith,et al.  Multiplexed Echo Planar Imaging for Sub-Second Whole Brain FMRI and Fast Diffusion Imaging , 2010, PloS one.

[74]  H. Heinze,et al.  Laminar activity in the hippocampus and entorhinal cortex related to novelty and episodic encoding , 2014, Nature Communications.

[75]  Kawin Setsompop,et al.  Ultra-fast MRI of the human brain with simultaneous multi-slice imaging. , 2013, Journal of magnetic resonance.

[76]  Manuel Schabus,et al.  Homeostatic Sleep Pressure and Responses to Sustained Attention in the Suprachiasmatic Area , 2009, Science.

[77]  A. Grace,et al.  Regulation of firing of dopaminergic neurons and control of goal-directed behaviors , 2007, Trends in Neurosciences.

[78]  Wade K. Smith,et al.  The human locus coeruleus: computer reconstruction of cellular distribution , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  Robert Turner,et al.  Image Distortion Correction in fMRI: A Quantitative Evaluation , 2002, NeuroImage.

[80]  D. German,et al.  Locus coeruleus cell loss in the aging human brain: A non‐random process , 1995, The Journal of comparative neurology.

[81]  Jonathan D. Cohen,et al.  Adaptive gain and the role of the locus coeruleus–norepinephrine system in optimal performance , 2005, The Journal of comparative neurology.

[82]  Christian Schwarzbauer,et al.  Positive or negative blips? The effect of phase encoding scheme on susceptibility-induced signal losses in EPI , 2005, NeuroImage.

[83]  Yasuo Terayama,et al.  Neuromelanin magnetic resonance imaging of locus ceruleus and substantia nigra in Parkinson's disease , 2006, Neuroreport.

[84]  R. Deichmann,et al.  Optimized EPI for fMRI studies of the orbitofrontal cortex: compensation of susceptibility-induced gradients in the readout direction , 2007, Magnetic Resonance Materials in Physics, Biology and Medicine.

[85]  Richard S. Frackowiak,et al.  Improved segmentation of deep brain grey matter structures using magnetization transfer (MT) parameter maps , 2009, NeuroImage.

[86]  Nikos K Logothetis,et al.  Interpreting the BOLD signal. , 2004, Annual review of physiology.

[87]  Paul S. Morgan,et al.  In vivo mapping of the human locus coeruleus , 2009, NeuroImage.

[88]  H. Condé,et al.  The role of the pedunculopontine tegmental nucleus in relation to conditioned motor performance in the cat I. Context-dependent and reinforcement-related single unit activity , 1998, Experimental Brain Research.

[89]  Brian B. Avants,et al.  The optimal template effect in hippocampus studies of diseased populations , 2010, NeuroImage.

[90]  X Hu,et al.  Retrospective estimation and correction of physiological fluctuation in functional MRI , 1995, Magnetic resonance in medicine.

[91]  Yan Zhu,et al.  Numerous GABAergic Afferents to Locus Ceruleus in the Pericerulear Dendritic Zone: Possible Interneuronal Pool , 2004, The Journal of Neuroscience.

[92]  Alexander Hammers,et al.  Volumes, spatial extents and a probabilistic atlas of the human basal ganglia and thalamus , 2007, NeuroImage.

[93]  David N. Kennedy,et al.  Automated Brainstem Co-registration (ABC) for MRI , 2006, NeuroImage.

[94]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[95]  R. Deichmann,et al.  Compensation of Susceptibility-Induced BOLD Sensitivity Losses in Echo-Planar fMRI Imaging , 2001, NeuroImage.

[96]  A. Carlsson,et al.  Network interactions in schizophrenia — therapeutic implications , 2000, Brain Research Reviews.

[97]  Karl J. Friston,et al.  Diffusion-based spatial priors for functional magnetic resonance images , 2008, NeuroImage.

[98]  Stephen D. Mayhew,et al.  Brainstem functional magnetic resonance imaging: Disentangling signal from physiological noise , 2008, Journal of magnetic resonance imaging : JMRI.

[99]  Marguerite Wieler,et al.  Midbrain iron content in early Parkinson disease , 2008, Neurology.

[100]  Mark G. Baxter,et al.  The Rostromedial Tegmental Nucleus (RMTg), a GABAergic Afferent to Midbrain Dopamine Neurons, Encodes Aversive Stimuli and Inhibits Motor Responses , 2009, Neuron.

[101]  N. Logothetis,et al.  Neurophysiology of the BOLD fMRI Signal in Awake Monkeys , 2008, Current Biology.

[102]  Chris Zarow,et al.  Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. , 2003, Archives of neurology.

[103]  W. Gibb,et al.  Melanin, tyrosine hydroxylase, calbindin and substance P in the human midbrain and substantia nigra in relation to nigrostriatal projections and differential neuronal susceptibility in Parkinson's disease , 1992, Brain Research.

[104]  A. Gonçalves-Ferreira,et al.  The human locus coeruleus 3-D stereotactic anatomy , 2012, Surgical and Radiologic Anatomy.

[105]  Richard G. Wise,et al.  Physiological noise modelling for spinal functional magnetic resonance imaging studies , 2008, NeuroImage.

[106]  Maurizio Corbetta,et al.  Comment on “Modafinil Shifts Human Locus Coeruleus to Low-Tonic, High-Phasic Activity During Functional MRI” and “Homeostatic Sleep Pressure and Responses to Sustained Attention in the Suprachiasmatic Area” , 2010, Science.

[107]  N. Bunzeck,et al.  Absolute Coding of Stimulus Novelty in the Human Substantia Nigra/VTA , 2006, Neuron.

[108]  S. Kollias,et al.  Duvernoy's Atlas of the Human Brain Stem and Cerebellum , 2009, American Journal of Neuroradiology.

[109]  W. Schultz,et al.  Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli , 1996, Nature.

[110]  R. Deichmann,et al.  Real-time functional magnetic resonance imaging: methods and applications. , 2007, Magnetic resonance imaging.

[111]  R. Pamphlett,et al.  Diagnostic evaluation of the substantia nigra , 1996, Neuropathology and applied neurobiology.

[112]  C. Nico Boehler,et al.  Mesolimbic interaction of emotional valence and reward improves memory formation , 2008, Neuropsychologia.

[113]  John R. C Christensen,et al.  Regional and temporal differences in real-time dopamine efflux in the nucleus accumbens during free-choice novelty , 1997, Brain Research.

[114]  Minryung R. Song,et al.  Diversity and Homogeneity in Responses of Midbrain Dopamine Neurons , 2013, The Journal of Neuroscience.

[115]  W. Schultz,et al.  Learning-Related Human Brain Activations Reflecting Individual Finances , 2007, Neuron.

[116]  Elyssa B. Margolis,et al.  Kappa opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[117]  Antoine Lutti,et al.  Multiparametric brainstem segmentation using a modified multivariate mixture of Gaussians☆ , 2013, NeuroImage: Clinical.

[118]  J. Connor,et al.  Iron, brain ageing and neurodegenerative disorders , 2004, Nature Reviews Neuroscience.

[119]  M M Mesulam,et al.  Human reticular formation: Cholinergic neurons of the pedunculopontine and laterodorsal tegmental nuclei and some cytochemical comparisons to forebrain cholinergic neurons , 1989, The Journal of comparative neurology.

[120]  Samuel M. McClure,et al.  Distinct Midbrain and Habenula Pathways Are Involved in Processing Aversive Events in Humans , 2015, The Journal of Neuroscience.

[121]  S. Sara.  The locus coeruleus and noradrenergic modulation of cognition , 2009, Nature Reviews Neuroscience.

[122]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[123]  Arno Klein,et al.  Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration , 2009, NeuroImage.

[124]  O. Hikosaka,et al.  Two types of dopamine neuron distinctly convey positive and negative motivational signals , 2009, Nature.

[125]  Raymond J. Dolan,et al.  Parcellation of the human substantia nigra based on anatomical connectivity to the striatum , 2013, NeuroImage.

[126]  S. Foote,et al.  Extrathalamic modulation of cortical function. , 1987, Annual review of neuroscience.