MR imaging in the non-human primate: studies of function and of dynamic connectivity

Since its early development in the late 1940s, nuclear magnetic resonance has become a powerful tool for applications ranging from chemical analysis or the study of the structure of solids to biomedical investigations. In the early 1990s the potential of this technique for functional brain mapping was demonstrated, causing unprecedented excitement in both basic and clinical neuroscience. It was shown that by using the appropriate pulse sequences the so-called functional magnetic resonance imaging (fMRI) technique can be made sensitive to local magnetic susceptibility alterations produced by changes in the concentration of deoxyhemoglobin in venous blood vessels. This blood-oxygenation-level-dependent (BOLD) contrast mechanism was successfully implemented in awake human subjects, in small animals, and recently in the non-human primate--the experimental animal of choice for the study of cognitive behavior. Simultaneous imaging and electrode recordings promise new insights into the mechanisms by which large-scale networks in the brain contribute to the local neural activity recorded at a given cortical site. Moreover, the use of MRI-visible tracers and of electrical microstimulation applied during imaging proves to be ideal for the study of connectivity in the living animal.

[1]  N. Logothetis,et al.  Ultra High-Resolution fMRI in Monkeys with Implanted RF Coils , 2002, Neuron.

[2]  P. Magistretti,et al.  Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[3]  B. Gustafsson,et al.  Afterpotentials and transduction properties in different types of central neurones. , 1984, Archives italiennes de biologie.

[4]  D Purves,et al.  Specialized vascularization of the primate visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  W. H. Vance,et al.  Effects of antidromic stimulation of the ventral root on glucose utilization in the ventral horn of the spinal cord in the rat. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[6]  B. Horwitz,et al.  Integrating electrophysiological and anatomical experimental data to create a large-scale model that simulates a delayed match-to-sample human brain imaging study. , 1998, Cerebral cortex.

[7]  M. Young,et al.  Neuronal population activity and functional imaging , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  Ravi S. Menon,et al.  Field Strength Dependence of Functional MRI Signals , 2000 .

[9]  G. Buzsáki,et al.  Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: Activity‐dependent phase‐precession of action potentials , 1998, Hippocampus.

[10]  N. Logothetis.  The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[11]  Nikos K. Logothetis,et al.  Three-Dimensional Shape Representation in Monkey Cortex , 2002, Neuron.

[12]  N. Logothetis,et al.  Magnetic Resonance Imaging of Neuronal Connections in the Macaque Monkey , 2001, Neuron.

[13]  R. Desimone,et al.  Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. , 1987, Journal of neurophysiology.

[14]  J. Allman,et al.  Mapping human visual cortex with positron emission tomography , 1986, Nature.

[15]  P. Lennie.  The Cost of Cortical Computation , 2003, Current Biology.

[16]  M. Raichle.  A Brief History of Human Functional Brain Mapping , 2000 .

[17]  Adelbert Ames,et al.  CNS energy metabolism as related to function , 2000, Brain Research Reviews.

[18]  L. Sokoloff.  Function-related changes in energy metabolism in the nervous system: localization and mechanisms. , 1993, The Keio journal of medicine.

[19]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[20]  N. Logothetis,et al.  Functional imaging of the monkey brain , 1999, Nature Neuroscience.

[21]  G. Orban,et al.  Extracting 3D from Motion: Differences in Human and Monkey Intraparietal Cortex , 2002, Science.

[22]  L. Sokoloff,et al.  Role of sodium and potassium ions in regulation of glucose metabolism in cultured astroglia. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Miriam Scadeng,et al.  Direct comparison of visual cortex activation in human and non-human primates using functional magnetic resonance imaging , 2001, Journal of Neuroscience Methods.

[24]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[25]  A. Crane,et al.  Differential effects of electrical stimulation of sciatic nerve on metabolic activity in spinal cord and dorsal root ganglion in the rat. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Tank,et al.  4 Tesla gradient recalled echo characteristics of photic stimulation‐induced signal changes in the human primary visual cortex , 1993 .

[27]  N. Logothetis,et al.  Visual Areas in Macaque Cortex Measured Using Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[28]  S. Ogawa.  Brain magnetic resonance imaging with contrast-dependent oxygenation , 1990 .

[29]  J. Reichenbach,et al.  Quantitative differentiation between BOLD models in fMRI , 2001, Magnetic resonance in medicine.

[30]  R. Nudo,et al.  Stimulation‐induced [14C]2‐deoxyglucose labeling of synaptic activity in the central auditory system , 1986, The Journal of comparative neurology.

[31]  A. Toga,et al.  5 – Optical Imaging Based on Intrinsic Signals , 2002 .

[32]  H. Duvernoy,et al.  Cortical blood vessels of the human brain , 1981, Brain Research Bulletin.

[33]  B. Rosen,et al.  Microscopic susceptibility variation and transverse relaxation: Theory and experiment , 1994, Magnetic resonance in medicine.

[34]  M. Jüptner,et al.  Review: Does Measurement of Regional Cerebral Blood Flow Reflect Synaptic Activity?—Implications for PET and fMRI , 1995, NeuroImage.

[35]  N. Logothetis.  The Underpinnings of the BOLD Functional Magnetic Resonance Imaging Signal , 2003, The Journal of Neuroscience.

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

[37]  S. Okada,et al.  Manganese Transport in the Neural Circuit of Rat CNS , 1998, Brain Research Bulletin.

[38]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[39]  U. Mitzdorf.  Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. , 1987, The International journal of neuroscience.

[40]  J. Csicsvari,et al.  Intracellular features predicted by extracellular recordings in the hippocampus in vivo. , 2000, Journal of neurophysiology.

[41]  L. Toth,et al.  How accurate is magnetic resonance imaging of brain function? , 2003, Trends in Neurosciences.

[42]  K. Uğurbil,et al.  Experimental determination of the BOLD field strength dependence in vessels and tissue , 1997, Magnetic resonance in medicine.

[43]  K. Uğurbil,et al.  Microvascular BOLD contribution at 4 and 7 T in the human brain: Gradient‐echo and spin‐echo fMRI with suppression of blood effects , 2003, Magnetic resonance in medicine.

[44]  L. Sokoloff,et al.  RELATION BETWEEN PHYSIOLOGICAL FUNCTION AND ENERGY METABOLISM IN THE CENTRAL NERVOUS SYSTEM , 1977, Journal of neurochemistry.

[45]  J. R. Baker,et al.  The intravascular contribution to fmri signal change: monte carlo modeling and diffusion‐weighted studies in vivo , 1995, Magnetic resonance in medicine.

[46]  D. Attwell,et al.  The neural basis of functional brain imaging signals , 2002, Trends in Neurosciences.

[47]  G. Buzsáki,et al.  Nucleus basalis and thalamic control of neocortical activity in the freely moving rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[49]  M. Mintun,et al.  Nonoxidative glucose consumption during focal physiologic neural activity. , 1988, Science.

[50]  Leslie G. Ungerleider,et al.  Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido‐nigral complex in the monkey , 1990, The Journal of comparative neurology.

[51]  Martin Lauritzen,et al.  Brain Function and Neurophysiological Correlates of Signals Used in Functional Neuroimaging , 2003, The Journal of Neuroscience.

[52]  N. Logothetis,et al.  Integration of Local Features into Global Shapes Monkey and Human fMRI Studies , 2003, Neuron.

[53]  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.

[54]  R. Douglas,et al.  A functional microcircuit for cat visual cortex. , 1991, The Journal of physiology.

[55]  Zhang Kun,et al.  PROGRESS IN VISUAL CORTICAL RESEARCH USING OPTICAL IMAGING BASED ON INTRINSIC SIGNALS , 2000 .

[56]  J. Ford,et al.  Combined event‐related fMRI and EEG evidence for temporal—parietal cortex activation during target detection , 1997, Neuroreport.

[57]  Ravi S. Menon,et al.  Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. , 1993, Biophysical journal.

[58]  Y Harada,et al.  The calcium component of the action potential in spinal motoneurones of the rat. , 1983, The Journal of physiology.

[59]  Nikos K. Logothetis,et al.  Motion Processing in the Macaque: Revisited with Functional Magnetic Resonance Imaging , 2001, The Journal of Neuroscience.

[60]  W. Sloot,et al.  Axonal transport of manganese and its relevance to selective neurotoxicity in the rat basal ganglia , 1994, Brain Research.

[61]  J. Mazziotta,et al.  Brain Mapping: The Methods , 2002 .

[62]  H. Scheich,et al.  New Insights into the Hemodynamic Blood Oxygenation Level-Dependent Response through Combination of Functional Magnetic Resonance Imaging and Optical Recording in Gerbil Barrel Cortex , 2000, The Journal of Neuroscience.

[63]  M. Raichle,et al.  Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[64]  J. Frahm,et al.  Mapping of retinal projections in the living rat using high‐resolution 3D gradient‐echo MRI with Mn2+‐induced contrast , 2001, Magnetic resonance in medicine.

[65]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[66]  P. Magistretti,et al.  Cellular mechanisms of brain energy metabolism and their relevance to functional brain imaging. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[67]  Afonso C. Silva,et al.  In vivo neuronal tract tracing using manganese‐enhanced magnetic resonance imaging , 1998, Magnetic resonance in medicine.

[68]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[69]  B. Wandell.  Computational neuroimaging of human visual cortex. , 1999, Annual review of neuroscience.

[70]  R. S. Hinks,et al.  Time course EPI of human brain function during task activation , 1992, Magnetic resonance in medicine.

[71]  O Hidaka,et al.  Role of calcium conductances on spike afterpotentials in rat trigeminal motoneurons. , 1997, Journal of neurophysiology.

[72]  M. Corbetta,et al.  Top-down modulation of early sensory cortex. , 1997 .

[73]  S. Laughlin,et al.  An Energy Budget for Signaling in the Grey Matter of the Brain , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[74]  J. Hogg.  Magnetic resonance imaging. , 1994, Journal of the Royal Naval Medical Service.

[75]  J C Gore,et al.  Quantification of intravascular and extravascular contributions to BOLD effects induced by alteration in oxygenation or intravascular contrast agents , 1998, Magnetic resonance in medicine.

[76]  J. Hochmann,et al.  Proton NMR on deoxyhemoglobin: Use of a modified DEFT technique , 1980 .

[77]  Nikos K. Logothetis,et al.  The Effect of Image Scrambling on Visual Cortical BOLD Activity in the Anesthetized Monkey , 2002, NeuroImage.

[78]  E. Tanaka,et al.  Ionic mechanisms underlying the depolarizing and hyperpolarizing afterpotentials of single spike in guinea-pig cingulate cortical neurons , 1993, Neuroscience.

[79]  K. Jellinger.  The tripartite synapse Glia in Synaptic Transmission , 2003 .

[80]  G. Palm,et al.  Density of neurons and synapses in the cerebral cortex of the mouse , 1989, The Journal of comparative neurology.

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

[82]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[83]  M. Colonnier,et al.  A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys , 1982, The Journal of comparative neurology.