Direct and fast detection of neuronal activation in the human brain with diffusion MRI.

Using MRI, we found that a slowly diffusing water pool was expanding (1.7 +/- 0.3%) upon activation on the human visual cortex at the detriment of a faster diffusing pool. The time course of this water phase transition preceded the activation-triggered vascular response detected by usual functional MRI by several seconds. The observed changes in water diffusion likely reflect early biophysical events that take place in the activated cells, such as cell swelling and membrane expansion. Although the exact mechanisms remain to clarify, access to such an early and direct physiological marker of cortical activation with MRI will provide opportunities for functional neuroimaging of the human brain.

[1]  Sabrina S Wilson Radiology , 1938, Glasgow Medical Journal.

[2]  R. Keynes,et al.  Light Scattering and Birefringence Changes during Nerve Activity , 1968, Nature.

[3]  I. Tasaki,et al.  Subaxolemmal filamentous network in the giant nerve fiber of the squid (Loligo pealei L.) and its possible role in excitability , 1978, The Journal of cell biology.

[4]  Irving J. Lowe,et al.  A modified pulsed gradient technique for measuring diffusion in the presence of large background gradients , 1980 .

[5]  K. Iwasa,et al.  Rapid pressure changes and surface displacements in the squid giant axon associated with production of action potentials. , 1982, The Japanese journal of physiology.

[6]  T Kobayashi,et al.  Subaxolemmal cytoskeleton in squid giant axon. II. Morphological identification of microtubule- and microfilament-associated domains of axolemma , 1986, The Journal of cell biology.

[7]  D. Le Bihan,et al.  Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. , 1988, Radiology.

[8]  I. Tasaki,et al.  Volume expansion of nonmyelinated nerve fibers during impulse conduction. , 1990, Biophysical journal.

[9]  I. Tasaki,et al.  Rapid structural changes in nerve fibers evoked by electric current pulses. , 1992, Biochemical and biophysical research communications.

[10]  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.

[11]  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.

[12]  B. MacVicar,et al.  Imaging cell volume changes and neuronal excitation in the hippocampal slice , 1994, Neuroscience.

[13]  C. Sotak,et al.  Spreading waves of decreased diffusion coefficient lifter cortical stimulation in the rat brain , 1994, Magnetic resonance in medicine.

[14]  J. Jefferys,et al.  Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. , 1995, Physiological reviews.

[15]  Colin Blakemore,et al.  Contrast dependence of motion-onset and pattern-reversal evoked potentials , 1995, Vision Research.

[16]  K. Holthoff,et al.  Intrinsic optical signals in rat neocortical slices measured with near- infrared dark-field microscopy reveal changes in extracellular space , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  L. Vargova,et al.  Dynamic changes in water ADC, energy metabolism, extracellular space volume, and tortuosity in neonatal rat brain during global ischemia , 1996, Magnetic resonance in medicine.

[18]  J. Garcìa,et al.  Severe transient hypoglycemia causes reversible change in the apparent diffusion coefficient of water. , 1996, Stroke.

[19]  D. Norris,et al.  Biexponential diffusion attenuation in various states of brain tissue: Implications for diffusion‐weighted imaging , 1996, Magnetic resonance in medicine.

[20]  J C Gore,et al.  Reversible, reproducible reduction of brain water apparent diffusion coefficient by cortical electroshocks , 1997, Magnetic resonance in medicine.

[21]  E. Yeung,et al.  Long-range electrostatic trapping of single-protein molecules at a liquid-solid interface. , 1998, Science.

[22]  R. Schwartz-Bloom,et al.  Activation of Excitatory Amino Acid Receptors in the Rat Hippocampal Slice Increases Intracellular Cl− and Cell Volume , 1998, Journal of neurochemistry.

[23]  R. Buxton,et al.  Dynamics of blood flow and oxygenation changes during brain activation: The balloon model , 1998, Magnetic resonance in medicine.

[24]  P. Schwartzkroin,et al.  Osmolarity, ionic flux, and changes in brain excitability , 1998, Epilepsy Research.

[25]  D. van Dusschoten,et al.  Modeling of self-diffusion and relaxation time NMR in multi-compartment systems. , 1998, Journal of magnetic resonance.

[26]  J. Gore,et al.  In vivo measurement of ADC change due to intravascular susceptibility variation , 1999, Magnetic resonance in medicine.

[27]  I. Tasaki,et al.  Rapid structural changes in nerve fibers and cells associated with their excitation processes. , 1999, The Japanese journal of physiology.

[28]  D L Buckley,et al.  The effect of ouabain on water diffusion in the rat hippocampal slice measured by high resolution NMR imaging , 1999, Magnetic resonance in medicine.

[29]  C. Nicholson,et al.  Changes in brain cell shape create residual extracellular space volume and explain tortuosity behavior during osmotic challenge. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J C Gore,et al.  Effects of cell volume fraction changes on apparent diffusion in human cells. , 2000, Magnetic resonance imaging.

[31]  A. R. Gardner-Medwin,et al.  Apparent diffusion coefficient and MR relaxation during osmotic manipulation in isolated turtle cerebellum , 2000, Magnetic resonance in medicine.

[32]  D. Le Bihan,et al.  Water diffusion compartmentation and anisotropy at high b values in the human brain , 2000, Magnetic resonance in medicine.

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

[34]  J B Poline,et al.  Transient decrease in water diffusion observed in human occipital cortex during visual stimulation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  S. Maier,et al.  Normal brain and brain tumor: multicomponent apparent diffusion coefficient line scan imaging. , 2001, Radiology.

[36]  Stéphane Lehéricy,et al.  Arteriovenous brain malformations: is functional MR imaging reliable for studying language reorganization in patients? Initial observations. , 2002, Radiology.

[37]  Frank J Vergeldt,et al.  Modelling of self-diffusion and relaxation time NMR in multicompartment systems with cylindrical geometry. , 2002, Journal of magnetic resonance.

[38]  J. Neil,et al.  Evidence that both fast and slow water ADC components arise from intracellular space , 2002, Magnetic resonance in medicine.

[39]  C. Braun,et al.  Effects of water on cortical excitability in humans , 2002, The European journal of neuroscience.

[40]  Angus M. Brown,et al.  Intrinsic optical signals in the rat optic nerve: Role for K+ uptake via NKCC1 and swelling of astrocytes , 2002, Glia.

[41]  Hiroshi Tsubokawa,et al.  GABAergic input contributes to activity-dependent change in cell volume in the hippocampal CA1 region , 2002, Neuroscience Research.

[42]  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.

[43]  F. Di Salle,et al.  Issues concerning the construction of a metabolic model for neuronal activation , 2003, Journal of neuroscience research.

[44]  G. L. Bretthorst,et al.  Statistical model for diffusion attenuated MR signal , 2003, Magnetic resonance in medicine.

[45]  Denis Le Bihan,et al.  Looking into the functional architecture of the brain with diffusion MRI , 2003, Nature Reviews Neuroscience.

[46]  V. Wedeen,et al.  Reduction of eddy‐current‐induced distortion in diffusion MRI using a twice‐refocused spin echo , 2003, Magnetic resonance in medicine.

[47]  Eva Syková,et al.  The relationship between changes in intrinsic optical signals and cell swelling in rat spinal cord slices , 2003, NeuroImage.

[48]  D. Yablonskiy,et al.  On the nature of the NAA diffusion attenuated MR signal in the central nervous system , 2004, Magnetic resonance in medicine.

[49]  V. Kiselev,et al.  Effect of magnetic field gradients induced by microvasculature on NMR measurements of molecular self-diffusion in biological tissues. , 2004, Journal of magnetic resonance.

[50]  A. Sukstanskii,et al.  Effects of permeable boundaries on the diffusion-attenuated MR signal: insights from a one-dimensional model. , 2004, Journal of magnetic resonance.

[51]  Jonathan Nissanov,et al.  Assessment of axonal fiber tract architecture in excised rat spinal cord by localized NMR q‐space imaging: Simulations and experimental studies , 2004, Magnetic resonance in medicine.

[52]  Y. Okada,et al.  Volume‐sensitive chloride channels in mouse cortical neurons: characterization and role in volume regulation , 2005, The European journal of neuroscience.