Restoring Susceptibility Induced MRI Signal Loss in Rat Brain at 9.4 T: A Step towards Whole Brain Functional Connectivity Imaging

The aural cavity magnetic susceptibility artifact leads to significant echo planar imaging (EPI) signal dropout in rat deep brain that limits acquisition of functional connectivity fcMRI data. In this study, we provide a method that recovers much of the EPI signal in deep brain. Needle puncture introduction of a liquid-phase fluorocarbon into the middle ear allows acquisition of rat fcMRI data without signal dropout. We demonstrate that with seeds chosen from previously unavailable areas, including the amygdala and the insular cortex, we are able to acquire large scale networks, including the limbic system. This tool allows EPI-based neuroscience and pharmaceutical research in rat brain using fcMRI that was previously not feasible.

[1]  B. Rosen,et al.  Cocaine Activation Discriminates Dopaminergic Projections by Temporal Response: An fMRI Study in Rat , 2000, NeuroImage.

[2]  O. Sporns,et al.  Network centrality in the human functional connectome. , 2012, Cerebral cortex.

[3]  R. Maddock.  The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain , 1999, Trends in Neurosciences.

[4]  B. Rosen,et al.  Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation , 1998, Magnetic resonance in medicine.

[5]  R. J. Dolan,et al.  Parallel Neural Responses in Amygdala Subregions and Sensory Cortex during Implicit Fear Conditioning , 2001, NeuroImage.

[6]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  Christoph Juchem,et al.  Magnetic field modeling with a set of individual localized coils. , 2010, Journal of magnetic resonance.

[8]  D. Cechetto,et al.  Autonomic responses and efferent pathways from the insular cortex in the rat , 1991, The Journal of comparative neurology.

[9]  David C. Van Essen,et al.  The future of the human connectome , 2012, NeuroImage.

[10]  J. Voogd,et al.  The human central nervous system , 1978 .

[11]  R. Dolan,et al.  Distinct spatial frequency sensitivities for processing faces and emotional expressions , 2003, Nature Neuroscience.

[12]  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.

[13]  Tao Jin,et al.  Brain switch for reflex micturition control detected by FMRI in rats. , 2009, Journal of neurophysiology.

[14]  C Büchel,et al.  Painful stimuli evoke different stimulus-response functions in the amygdala, prefrontal, insula and somatosensory cortex: a single-trial fMRI study. , 2002, Brain : a journal of neurology.

[15]  Terence W Nixon,et al.  Dynamic shim updating (DSU) for multislice signal acquisition , 2003, Magnetic resonance in medicine.

[16]  R W Cox,et al.  Software tools for analysis and visualization of fMRI data , 1997, NMR in biomedicine.

[17]  Mathias Hoehn,et al.  High field BOLD response to forepaw stimulation in the mouse , 2010, NeuroImage.

[18]  Paul J. Laurienti,et al.  Consistency of Network Modules in Resting-State fMRI Connectome Data , 2012, PloS one.

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

[20]  J. Voogd,et al.  The Human Central Nervous System , 1978, Springer Berlin Heidelberg.

[21]  J. A. Ricardo,et al.  Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat , 1978, Brain Research.

[22]  Christopher P. Pawela,et al.  Long-term vascular access ports as a means of sedative administration in a rodent fMRI survival model , 2011, Journal of Neuroscience Methods.

[23]  P. Fox,et al.  In vivo fMRI demonstration of hypothalamic function following intraperitoneal glucose administration in a rat model , 2000, Magnetic resonance in medicine.

[24]  J. O'Doherty,et al.  Encoding Predictive Reward Value in Human Amygdala and Orbitofrontal Cortex , 2003, Science.

[25]  Larry W. Swanson,et al.  Combining collation and annotation efforts toward completion of the rat and mouse connectomes in BAMS , 2012, Front. Neuroinform..

[26]  Ji-Kyung Choi,et al.  Exogenous contrast agent improves sensitivity of gradient‐echo functional magnetic resonance imaging at 9.4 T , 2004, Magnetic resonance in medicine.

[27]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  S. Matsuura,et al.  Human brain region response to distention or cold stimulation of the bladder: a positron emission tomography study. , 2002, The Journal of urology.

[29]  Jochen Ditterich,et al.  Splash: A Software Tool for Stereotactic Planning of Recording Chamber Placement and Electrode Trajectories , 2011, Front. Neuroinform..

[30]  Alexander Huk,et al.  PLDAPS: A Hardware Architecture and Software Toolbox for Neurophysiology Requiring Complex Visual Stimuli and Online Behavioral Control , 2012, Front. Neuroinform..

[31]  Ian Marshall,et al.  Imaging Conditioned Fear Circuitry Using Awake Rodent fMRI , 2013, PloS one.

[32]  J. Detre,et al.  Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Jing Li,et al.  Partial Fourier transform reconstruction for single‐shot MRI with linear frequency‐swept excitation , 2013, Magnetic resonance in medicine.

[34]  Christoph Juchem,et al.  Multi-coil magnetic field modeling. , 2013, Journal of magnetic resonance.

[35]  A. Meyer-Lindenberg,et al.  5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression , 2005, Nature Neuroscience.

[36]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[37]  C. Saper,et al.  Convergence of autonomic and limbic connections in the insular cortex of the rat , 1982, The Journal of comparative neurology.

[38]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[39]  P. Basser,et al.  Observation of microscopic diffusion anisotropy in the spinal cord using double‐pulsed gradient spin echo MRI , 2008, Magnetic resonance in medicine.

[40]  A. Rubens.  Caloric stimulation and unilateral visual neglect , 1985, Neurology.

[41]  The Human Central Nervous System, 4th ed. , 2008, American Journal of Neuroradiology.

[42]  Christian Windischberger,et al.  Toward discovery science of human brain function , 2010, Proceedings of the National Academy of Sciences.

[43]  J. Bootman,et al.  Safety evaluation of perfluoropolyethers, liquid polymers used in barrier creams and other skin-care products. , 1996, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

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

[45]  Daniel P. Kennedy,et al.  Intact Bilateral Resting-State Networks in the Absence of the Corpus Callosum , 2011, The Journal of Neuroscience.

[46]  Abraham Z. Snyder,et al.  Function in the human connectome: Task-fMRI and individual differences in behavior , 2013, NeuroImage.

[47]  Allan R. Jones,et al.  A mesoscale connectome of the mouse brain , 2014, Nature.

[48]  Jennifer H. Pfeifer,et al.  Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders , 2006, Nature Neuroscience.

[49]  J. Hyde,et al.  Multishot partial‐k‐space EPI for high‐resolution fMRI demonstrated in a rat whisker barrel stimulation model at 3t , 2003, Magnetic resonance in medicine.

[50]  Joseph E LeDoux,et al.  Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[52]  Jonathan C. W. Brooks,et al.  Somatotopic organisation of the human insula to painful heat studied with high resolution functional imaging , 2005, NeuroImage.

[53]  C. Rampon,et al.  Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods , 1997, Neuroscience.

[54]  Menno Witter,et al.  The Retrosplenial Cortex: Intrinsic Connectivity and Connections with the (Para)Hippocampal Region in the Rat. An Interactive Connectome , 2011, Front. Neuroinform..

[55]  Joseph E LeDoux,et al.  The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  D. Paré,et al.  Stimulation of Medial Prefrontal Cortex Decreases the Responsiveness of Central Amygdala Output Neurons , 2003, The Journal of Neuroscience.