Considerations for resting state functional MRI and functional connectivity studies in rodents

Resting state functional MRI (rs-fMRI) and functional connectivity mapping have become widely used tools in the human neuroimaging community and their use is rapidly spreading into the realm of rodent research as well. One of the many attractive features of rs-fMRI is that it is readily translatable from humans to animals and back again. Changes in functional connectivity observed in human studies can be followed by more invasive animal experiments to determine the neurophysiological basis for the alterations, while exploratory work in animal models can identify possible biomarkers for further investigation in human studies. These types of interwoven human and animal experiments have a potentially large impact on neuroscience and clinical practice. However, impediments exist to the optimal application of rs-fMRI in small animals, some similar to those encountered in humans and some quite different. In this review we identify the most prominent of these barriers, discuss differences between rs-fMRI in rodents and in humans, highlight best practices for animal studies, and review selected applications of rs-fMRI in rodents. Our goal is to facilitate the integration of human and animal work to the benefit of both fields.

[1]  Kevin Murphy,et al.  Resting-state fMRI confounds and cleanup , 2013, NeuroImage.

[2]  M. Ingvar,et al.  Functional MRI at 4.7 Tesla of the Rat Brain during Electric Stimulation of Forepaw, Hindpaw, or Tail in Single- and Multislice Experiments , 2000, Experimental Neurology.

[3]  Ceon Ramon,et al.  Noninvasive Localization of Epileptic Sites from Stable Phase Synchronization Patterns on Different Days Derived from Short Duration Interictal Scalp dEEG , 2012, Brain Topography.

[4]  Andreas A Ioannides,et al.  Dynamic functional connectivity , 2007, Current Opinion in Neurobiology.

[5]  Angelo Bifone,et al.  Voxel Scale Complex Networks of Functional Connectivity in the Rat Brain: Neurochemical State Dependence of Global and Local Topological Properties , 2012, Comput. Math. Methods Medicine.

[6]  Kris Thielemans,et al.  Characterization of CD8+ T-Cell Responses in the Peripheral Blood and Skin Injection Sites of Melanoma Patients Treated with mRNA Electroporated Autologous Dendritic Cells (TriMixDC-MEL) , 2013, BioMed research international.

[7]  R. Cameron Craddock,et al.  Clinical applications of the functional connectome , 2013, NeuroImage.

[8]  Seong-Gi Kim,et al.  Effects of the α2‐adrenergic receptor agonist dexmedetomidine on neural, vascular and BOLD fMRI responses in the somatosensory cortex , 2013, The European journal of neuroscience.

[9]  B. Biswal Resting-State Functional Connectivity , 2015 .

[10]  Paul M. Matthews,et al.  Confounding effects of anesthesia on functional activation in rodent brain: a study of halothane and α-chloralose anesthesia , 2005, NeuroImage.

[11]  Leah Krubitzer,et al.  The Magnificent Compromise: Cortical Field Evolution in Mammals , 2007, Neuron.

[12]  Angelo Bifone,et al.  A stereotaxic MRI template set for the rat brain with tissue class distribution maps and co-registered anatomical atlas: Application to pharmacological MRI , 2006, NeuroImage.

[13]  Xiangyu Long,et al.  Functional segmentation of the brain cortex using high model order group PICA , 2009, Human brain mapping.

[14]  Yihong Yang,et al.  Registering and analyzing rat fMRI data in the stereotaxic framework by exploiting intrinsic anatomical features. , 2010, Magnetic resonance imaging.

[15]  Michael Brainin,et al.  Role of repetitive transcranial magnetic stimulation in stroke rehabilitation. , 2013, Frontiers of neurology and neuroscience.

[16]  M. Nelson,et al.  Physiological roles and properties of potassium channels in arterial smooth muscle. , 1995, The American journal of physiology.

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

[18]  V. Calhoun,et al.  Temporal lobe and “default” hemodynamic brain modes discriminate between schizophrenia and bipolar disorder , 2008, Human brain mapping.

[19]  O. H. Lowry,et al.  REGIONAL ENERGY RESERVES IN MOUSE BRAIN AND CHANGES WITH ISCHAEMIA AND ANAESTHESIA * , 1966, Journal of neurochemistry.

[20]  F. Hyder,et al.  Activation of single whisker barrel in rat brain localized by functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Hiroki Iida,et al.  Isoflurane and Sevoflurane Induce Vasodilation of Cerebral Vessels via ATP‐sensitive K+ Channel Activation , 1998, Anesthesiology.

[22]  Pierre J. Magistretti,et al.  Brain energy metabolism , 2013 .

[23]  Natalia Gulyaeva,et al.  Rodent Models of Depression: Neurotrophic and Neuroinflammatory Biomarkers , 2014, BioMed research international.

[24]  Ramachandran Ramani,et al.  Understanding anesthesia through functional imaging , 2008, Current opinion in anaesthesiology.

[25]  Pierre J Magistretti,et al.  Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. , 2011, Cell metabolism.

[26]  W. Weber,et al.  Anesthesia and other considerations for in vivo imaging of small animals. , 2008, ILAR journal.

[27]  S. Keilholz,et al.  Functional connectivity in blood oxygenation level‐dependent and cerebral blood volume‐weighted resting state functional magnetic resonance imaging in the rat brain , 2010, Journal of magnetic resonance imaging : JMRI.

[28]  Afonso C. Silva,et al.  Laminar specificity of functional MRI onset times during somatosensory stimulation in rat , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Stephen D. Mayhew,et al.  Investigating intrinsic connectivity networks using simultaneous BOLD and CBF measurements , 2014, NeuroImage.

[30]  S. Keilholz,et al.  Time‐dependent effects of isoflurane and dexmedetomidine on functional connectivity, spectral characteristics, and spatial distribution of spontaneous BOLD fluctuations , 2014, NMR in biomedicine.

[31]  Zhifeng Liang,et al.  Neuroplasticity to a single-episode traumatic stress revealed by resting-state fMRI in awake rats , 2014, NeuroImage.

[32]  JR Cormack,et al.  The role of α2-agonists in neurosurgery , 2005, Journal of Clinical Neuroscience.

[33]  Waqas Majeed,et al.  Spatiotemporal dynamics of low frequency fluctuations in BOLD fMRI of the rat , 2009, Journal of magnetic resonance imaging : JMRI.

[34]  Hillary D. Schwarb,et al.  Short‐time windows of correlation between large‐scale functional brain networks predict vigilance intraindividually and interindividually , 2013, Human brain mapping.

[35]  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.

[36]  F. Gyulai,et al.  Anesthetics and cerebral metabolism , 2004, Current opinion in anaesthesiology.

[37]  G. Goelman,et al.  Functional connectivity in prenatally stressed rats with and without maternal treatment with ladostigil, a brain‐selective monoamine oxidase inhibitor , 2014, The European journal of neuroscience.

[38]  Jesper L. R. Andersson,et al.  A template for spatial normalisation of MR images of the rat brain , 2003, Journal of Neuroscience Methods.

[39]  J. Snow,et al.  PHARMACOKINETICS OF HALOTHANE AND ETHER , 1964, British journal of anaesthesia.

[40]  G. Orban,et al.  Default Mode of Brain Function in Monkeys , 2011, The Journal of Neuroscience.

[41]  Jun Lu,et al.  The &agr;2-Adrenoceptor Agonist Dexmedetomidine Converges on an Endogenous Sleep-promoting Pathway to Exert Its Sedative Effects , 2003, Anesthesiology.

[42]  D. Leopold,et al.  Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest , 2008, Human brain mapping.

[43]  Kai-Hsiang Chuang,et al.  Pharmacological insight into neurotransmission origins of resting-state functional connectivity: α2-adrenergic agonist vs antagonist , 2014, NeuroImage.

[44]  Rupeng Li,et al.  Functional Connectivity in Rat Brain at 200 μm Resolution , 2014, Brain Connect..

[45]  Brian D. Mills,et al.  Large-scale topology and the default mode network in the mouse connectome , 2014, Proceedings of the National Academy of Sciences.

[46]  Justin L. Vincent,et al.  Intrinsic functional architecture in the anaesthetized monkey brain , 2007, Nature.

[47]  Jeff H. Duyn,et al.  Mapping resting-state functional connectivity using perfusion MRI , 2008, NeuroImage.

[48]  Peter Herman,et al.  Quantitative basis for neuroimaging of cortical laminae with calibrated functional MRI , 2013, Proceedings of the National Academy of Sciences.

[49]  Ravi S. Menon,et al.  Resting‐state networks show dynamic functional connectivity in awake humans and anesthetized macaques , 2013, Human brain mapping.

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

[51]  Irene Tracey,et al.  Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal , 2004, NeuroImage.

[52]  Nathan S White,et al.  Impaired thalamocortical connectivity in humans during general-anesthetic-induced unconsciousness , 2003, NeuroImage.

[53]  P. Sebel,et al.  Functional connectivity changes with concentration of sevoflurane anesthesia , 2005, Neuroreport.

[54]  G. Vanhoutte,et al.  Changing body temperature affects the T  2* signal in the rat brain and reveals hypothalamic activity , 2006, Magnetic resonance in medicine.

[55]  J. Pillai Functional Connectivity. , 2017, Neuroimaging clinics of North America.

[56]  Vesa Kiviniemi,et al.  A Sliding Time-Window ICA Reveals Spatial Variability of the Default Mode Network in Time , 2011, Brain Connect..

[57]  Peter Herman,et al.  Energetics of neuronal signaling and fMRI activity , 2007, Proceedings of the National Academy of Sciences.

[58]  Mathias Hoehn,et al.  Reliability and spatial specificity of rat brain sensorimotor functional connectivity networks are superior under sedation compared with general anesthesia , 2013, NMR in biomedicine.

[59]  Dewen Hu,et al.  Hemodynamic and electrophysiological spontaneous low-frequency oscillations in the cortex: Directional influences revealed by Granger causality , 2014, NeuroImage.

[60]  Marcelo Febo,et al.  Technical and Conceptual Considerations for Performing and Interpreting Functional MRI Studies in Awake Rats , 2011, Front. Psychiatry.

[61]  Steven Laureys,et al.  The Effect of Clonidine Infusion on Distribution of Regional Cerebral Blood Flow in Volunteers , 2008, Anesthesia and Analgesia.

[62]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[63]  Jürgen Hennig,et al.  Tracking dynamic resting-state networks at higher frequencies using MR-encephalography , 2013, NeuroImage.

[64]  Jon H. Kaas,et al.  Reconstructing the Organization of Neocortex of the First Mammals and Subsequent Modifications , 2007 .

[65]  Kai-Hsiang Chuang,et al.  Neural correlate of resting-state functional connectivity under α2 adrenergic receptor agonist, medetomidine , 2014, NeuroImage.

[66]  Fahmeed Hyder,et al.  Increased resting functional connectivity in spike‐wave epilepsy in WAG/Rij rats , 2013, Epilepsia.

[67]  P N Ainslie,et al.  On the regulation of the blood supply to the brain: old age concepts and new age ideas. , 2010, Journal of applied physiology.

[68]  R. Lasek,et al.  Ontophyletics of the nervous system: development of the corpus callosum and evolution of axon tracts. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Vince D. Calhoun,et al.  Higher dimensional analysis shows reduced dynamism of time-varying network connectivity in schizophrenia patients , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[70]  Lei Wang,et al.  Aberrant resting-state functional connectivity in a genetic rat model of depression , 2014, Psychiatry Research: Neuroimaging.

[71]  Piyush M Patel,et al.  Effect of Dexmedetomidine on Cerebral Blood Flow Velocity, Cerebral Metabolic Rate, and Carbon Dioxide Response in Normal Humans , 2008, Anesthesiology.

[72]  S. Keilholz,et al.  Functional Connectivity Mapping in the Rat Brain using Spin-echo EPI , 2008 .

[73]  Daniel A. Handwerker,et al.  Periodic changes in fMRI connectivity , 2012, NeuroImage.

[74]  F. Hyder,et al.  Total neuroenergetics support localized brain activity: Implications for the interpretation of fMRI , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Mervyn Maze,et al.  A Hypnotic Response to Dexmedetomidine, an α2 Agonist, Is Mediated in the Locus Coerüleus in Rats , 1992 .

[76]  Zhifeng Liang,et al.  Mapping resting-state brain networks in conscious animals , 2010, Journal of Neuroscience Methods.

[77]  Daniel P. Kennedy,et al.  The intrinsic functional organization of the brain is altered in autism , 2008, NeuroImage.

[78]  Yihong Yang,et al.  Abstinence from Cocaine and Sucrose Self-Administration Reveals Altered Mesocorticolimbic Circuit Connectivity by Resting State MRI , 2014, Brain Connect..

[79]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

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

[81]  Waqas Majeed,et al.  Broadband Local Field Potentials Correlate with Spontaneous Fluctuations in Functional Magnetic Resonance Imaging Signals in the Rat Somatosensory Cortex Under Isoflurane Anesthesia , 2011, Brain Connect..

[82]  L. Becerra,et al.  Robust Reproducible Resting State Networks in the Awake Rodent Brain , 2011, PloS one.

[83]  M.P.A. van Meer Brain reorganization after experimental stroke: functional and structural MRI correlates , 2008 .

[84]  Shella D. Keilholz,et al.  The Neural Basis of Time-Varying Resting-State Functional Connectivity , 2014, Brain Connect..

[85]  Younglim Lee,et al.  Default-Mode-Like Network Activation in Awake Rodents , 2011, PloS one.

[86]  M. Steriade Impact of network activities on neuronal properties in corticothalamic systems. , 2001, Journal of neurophysiology.

[87]  M. Maze,et al.  A hypnotic response to dexmedetomidine, an alpha 2 agonist, is mediated in the locus coeruleus in rats. , 1992, Anesthesiology.

[88]  J. Cormack,et al.  The role of alpha2-agonists in neurosurgery. , 2005, Journal of clinical neuroscience : official journal of the Neurosurgical Society of Australasia.

[89]  L. Krubitzer The organization of neocortex in mammals: are species differences really so different? , 1995, Trends in Neurosciences.

[90]  Biyu J. He,et al.  Electrophysiological correlates of the brain's intrinsic large-scale functional architecture , 2008, Proceedings of the National Academy of Sciences.

[91]  Jeff H. Duyn,et al.  Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal , 2007, NeuroImage.

[92]  Tao Li,et al.  Mapping thalamocortical networks in rat brain using resting-state functional connectivity , 2013, NeuroImage.

[93]  Justin L. Vincent,et al.  Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior , 2007, Neuron.

[94]  David A. Leopold,et al.  The contribution of electrophysiology to functional connectivity mapping , 2013, NeuroImage.

[95]  Wei Chen,et al.  The Change of Functional Connectivity Specificity in Rats Under Various Anesthesia Levels and its Neural Origin , 2012, Brain Topography.

[96]  Dirk Wiedermann,et al.  A fully noninvasive and robust experimental protocol for longitudinal fMRI studies in the rat , 2006, NeuroImage.

[97]  D. Javitt,et al.  Functional connectivity fMRI in mouse brain at 7T using isoflurane , 2013, Journal of Neuroscience Methods.

[98]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Santiago Canals,et al.  Functional MRI of long-term potentiation: imaging network plasticity , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[100]  Waqas Majeed,et al.  Spatiotemporal dynamics of low frequency BOLD fluctuations in rats and humans , 2011, NeuroImage.

[101]  David A. Leopold,et al.  Dynamic functional connectivity: Promise, issues, and interpretations , 2013, NeuroImage.

[102]  Aline Seuwen,et al.  Specificity of stimulus-evoked fMRI responses in the mouse: The influence of systemic physiological changes associated with innocuous stimulation under four different anesthetics , 2014, NeuroImage.

[103]  L. Boorman,et al.  The resting‐state neurovascular coupling relationship: rapid changes in spontaneous neural activity in the somatosensory cortex are associated with haemodynamic fluctuations that resemble stimulus‐evoked haemodynamics , 2013, The European journal of neuroscience.

[104]  Dieter Jaeger,et al.  Infraslow LFP correlates to resting-state fMRI BOLD signals , 2013, NeuroImage.

[105]  Catie Chang,et al.  Time–frequency dynamics of resting-state brain connectivity measured with fMRI , 2010, NeuroImage.

[106]  Valerio Zerbi,et al.  Resting-State Functional Connectivity Changes in Aging apoE4 and apoE-KO Mice , 2014, The Journal of Neuroscience.

[107]  V. Calhoun,et al.  Dynamic connectivity states estimated from resting fMRI Identify differences among Schizophrenia, bipolar disorder, and healthy control subjects , 2014, Front. Hum. Neurosci..

[108]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[109]  Shella D. Keilholz,et al.  Dynamic Properties of Functional Connectivity in the Rodent , 2013, Brain Connect..

[110]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[111]  E. Jones,et al.  Interhemispheric pathways in the absence of a corpus callosum. An experimental study of commissural connexions in the marsupial phalanger. , 1971, Journal of anatomy.

[112]  C. Sherrington,et al.  On the Regulation of the Blood‐supply of the Brain , 1890, The Journal of physiology.

[113]  Guillén Fernández,et al.  Stress-induced alterations in large-scale functional networks of the rodent brain , 2015, NeuroImage.

[114]  Patrick W Wright,et al.  Mapping Functional Connectivity Using Cerebral Blood Flow in the Mouse Brain , 2015, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[115]  M Steriade,et al.  Sleep oscillations and their blockage by activating systems. , 1994, Journal of psychiatry & neuroscience : JPN.

[116]  M. Viergever,et al.  Recovery of Sensorimotor Function after Experimental Stroke Correlates with Restoration of Resting-State Interhemispheric Functional Connectivity , 2010, The Journal of Neuroscience.

[117]  J. Lurito,et al.  Multiple sclerosis: low-frequency temporal blood oxygen level-dependent fluctuations indicate reduced functional connectivity initial results. , 2002, Radiology.

[118]  Bharat B. Biswal,et al.  Interhemispheric neuroplasticity following limb deafferentation detected by resting-state functional connectivity magnetic resonance imaging (fcMRI) and functional magnetic resonance imaging (fMRI) , 2010, NeuroImage.

[119]  H. Lu,et al.  Resting-State Functional Connectivity in Rat Brain , 2005 .

[120]  M. Schölvinck,et al.  Neural basis of global resting-state fMRI activity , 2010, Proceedings of the National Academy of Sciences.

[121]  O. Tervonen,et al.  Neuroglial Plasticity at Striatal Glutamatergic Synapses in Parkinson's Disease , 2011, Front. Syst. Neurosci..

[122]  Shella D. Keilholz,et al.  Evaluation of data-driven network analysis approaches for functional connectivity MRI , 2010, Brain Structure and Function.

[123]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[124]  Andreas Meyer-Lindenberg,et al.  Haloperidol modulates midbrain-prefrontal functional connectivity in the rat brain , 2013, European Neuropsychopharmacology.

[125]  S. Everling,et al.  Monkey in the middle: why non-human primates are needed to bridge the gap in resting-state investigations , 2012, Front. Neuroanat..

[126]  Trygve B. Leergaard,et al.  Waxholm Space atlas of the Sprague Dawley rat brain , 2014, NeuroImage.

[127]  Leanne Groban,et al.  Dexmedetomidine-Induced Sedation in Volunteers Decreases Regional and Global Cerebral Blood Flow , 2002, Anesthesia and analgesia.

[128]  Chunshui Yu,et al.  Contribution of the Resting-State Functional Connectivity of the Contralesional Primary Sensorimotor Cortex to Motor Recovery after Subcortical Stroke , 2014, PloS one.

[129]  M. Fox,et al.  The global signal and observed anticorrelated resting state brain networks. , 2009, Journal of neurophysiology.

[130]  Nikolaus Kriegeskorte,et al.  How does an fMRI voxel sample the neuronal activity pattern: Compact-kernel or complex spatiotemporal filter? , 2010, NeuroImage.

[131]  Jeff H. Duyn,et al.  Temporal dynamics of the BOLD fMRI impulse response , 2005, NeuroImage.

[132]  Francesco Sforazzini,et al.  Distributed BOLD and CBV-weighted resting-state networks in the mouse brain , 2014, NeuroImage.

[133]  K Shmueli,et al.  Low-Frequency Fluctuations in the Cardiac Rate Contribute to Variance in the Resting-State fMRI BOLD Signal , 2007 .

[134]  Zhe‐Xi Luo,et al.  Transformation and diversification in early mammal evolution , 2007, Nature.

[135]  Xiaoping P. Hu,et al.  Comparison of alpha-chloralose, medetomidine and isoflurane anesthesia for functional connectivity mapping in the rat. , 2010, Magnetic resonance imaging.

[136]  Andrea L. Cirranello,et al.  The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals , 2013, Science.

[137]  Dieter Jaeger,et al.  Quasi-periodic patterns (QPP): Large-scale dynamics in resting state fMRI that correlate with local infraslow electrical activity , 2014, NeuroImage.

[138]  M. Verhoye,et al.  Functional Connectivity fMRI of the Rodent Brain: Comparison of Functional Connectivity Networks in Rat and Mouse , 2011, PloS one.

[139]  R T Constable,et al.  Resting functional connectivity between the hemispheres in childhood absence epilepsy , 2011, Neurology.

[140]  A Villringer,et al.  Characterization of CBF response to somatosensory stimulation: model and influence of anesthetics. , 1993, The American journal of physiology.

[141]  John E. W. Mayhew,et al.  Investigating neural–hemodynamic coupling and the hemodynamic response function in the awake rat , 2006, NeuroImage.

[142]  J. Mayhew,et al.  Fine detail of neurovascular coupling revealed by spatiotemporal analysis of the hemodynamic response to single whisker stimulation in rat barrel cortex. , 2008, Journal of neurophysiology.

[143]  John E. W. Mayhew,et al.  Neurovascular coupling is brain region-dependent , 2012, NeuroImage.

[144]  M. Ueki,et al.  Effect of alpha‐chloralose, halothane, pentobarbital and nitrous oxide anesthesia on metabolic coupling in somatosensory cortex of rat , 1992, Acta anaesthesiologica Scandinavica.

[145]  Rafael Delgado y Palacios,et al.  Different anesthesia regimes modulate the functional connectivity outcome in mice , 2014, Magnetic resonance in medicine.

[146]  Matthew N. DeSalvo,et al.  Where fMRI and Electrophysiology Agree to Disagree: Corticothalamic and Striatal Activity Patterns in the WAG/Rij Rat , 2011, The Journal of Neuroscience.

[147]  Craig K. Jones,et al.  Functional networks in the anesthetized rat brain revealed by independent component analysis of resting-state FMRI. , 2010, Journal of neurophysiology.

[148]  Edward T. Bullmore,et al.  Fledgling pathoconnectomics of psychiatric disorders , 2013, Trends in Cognitive Sciences.

[149]  Remco J. Renken,et al.  Automated correction of spin-history related motion artefacts in fMRI: Simulated and phantom data , 2005, IEEE Transactions on Biomedical Engineering.

[150]  Clara A. Scholl,et al.  Synchronized delta oscillations correlate with the resting-state functional MRI signal , 2007, Proceedings of the National Academy of Sciences.

[151]  B. Biswal,et al.  Functional connectivity in the motor cortex of resting human brain using echo‐planar mri , 1995, Magnetic resonance in medicine.

[152]  I. Rozet,et al.  Anesthesia for functional neurosurgery: the role of dexmedetomidine , 2008, Current opinion in anaesthesiology.

[153]  Dajiang Zhu,et al.  Dynamic functional connectomics signatures for characterization and differentiation of PTSD patients , 2014, Human brain mapping.

[154]  Xiping Liu,et al.  Dynamic Repertoire of Intrinsic Brain States Is Reduced in Propofol-Induced Unconsciousness , 2015, Brain Connect..

[155]  Wei Chen,et al.  Procedure for minimizing stress for fMRI studies in conscious rats , 2005, Journal of Neuroscience Methods.

[156]  D. Jaeger,et al.  Phase-amplitude coupling and infraslow (<1 Hz) frequencies in the rat brain: relationship to resting state fMRI , 2014, Front. Integr. Neurosci..

[157]  Aileen Schroeter,et al.  Optimization of anesthesia protocol for resting-state fMRI in mice based on differential effects of anesthetics on functional connectivity patterns , 2014, NeuroImage.

[158]  M. Raichle,et al.  Rat brains also have a default mode network , 2012, Proceedings of the National Academy of Sciences.

[159]  Lei Zhou,et al.  BOLD study of stimulation-induced neural activity and resting-state connectivity in medetomidine-sedated rat , 2008, NeuroImage.

[160]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.

[161]  P. Willner,et al.  Loss of social status: preliminary evaluation of a novel animal model of depression , 1995, Journal of psychopharmacology.

[162]  Pablo A Celnik,et al.  Understanding and enhancing motor recovery after stroke using transcranial magnetic stimulation. , 2011, Restorative neurology and neuroscience.

[163]  Stefan A. Carp,et al.  The effect of different anesthetics on neurovascular coupling , 2010, NeuroImage.

[164]  I. Fried,et al.  Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex , 2008, Nature Neuroscience.

[165]  K. Nagata [Brain energy metabolism]. , 1997, Nihon rinsho. Japanese journal of clinical medicine.

[166]  Bharat B. Biswal,et al.  A protocol for use of medetomidine anesthesia in rats for extended studies using task-induced BOLD contrast and resting-state functional connectivity , 2009, NeuroImage.

[167]  T. Butts,et al.  The evolution of the vertebrate cerebellum: absence of a proliferative external granule layer in a non‐teleost ray‐finned fish , 2014, Evolution & development.

[168]  J B Patlak,et al.  Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. , 1990, The American journal of physiology.

[169]  Mathias Hoehn,et al.  Functional connectivity in the rat at 11.7T: Impact of physiological noise in resting state fMRI , 2011, NeuroImage.

[170]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[171]  Seong-Gi Kim,et al.  Early Temporal Characteristics of Cerebral Blood Flow and Deoxyhemoglobin Changes during Somatosensory Stimulation , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[172]  M. Zornow,et al.  Dexmedetomidine, an α2‐Adrenergic Agonist, Decreases Cerebral Blood Flow in the Isoflurane‐Anesthetized Dog , 1990, Anesthesia and analgesia.

[173]  R. Turner,et al.  Characterization and Correction of Interpolation Effects in the Realignment of fMRI Time Series , 2000, NeuroImage.

[174]  R G Shulman,et al.  Dynamic mapping at the laminar level of odor-elicited responses in rat olfactory bulb by functional MRI. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[175]  Dieter Jaeger,et al.  Neural correlates of time-varying functional connectivity in the rat , 2013, NeuroImage.

[176]  M. Greicius,et al.  Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI , 2004, Proc. Natl. Acad. Sci. USA.

[177]  B. Morris,et al.  Advancing schizophrenia drug discovery: optimizing rodent models to bridge the translational gap , 2012, Nature Reviews Drug Discovery.

[178]  Janet Scheel,et al.  Spatiotemporal Dynamics , 2017, Encyclopedia of GIS.

[179]  Shella D. Keilholz,et al.  Effects of Severing the Corpus Callosum on Electrical and BOLD Functional Connectivity and Spontaneous Dynamic Activity in the Rat Brain , 2013, Brain Connect..

[180]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[181]  Takeshi Ogawa,et al.  An in vivo MRI Template Set for Morphometry, Tissue Segmentation, and fMRI Localization in Rats , 2011, Front. Neuroinform..