Targeted Path Scanning: An Emerging Method for Recording Fast Changing Network Dynamics across Large Distances

Attention is being increasingly focused on the dynamical behavior of large networks of neurons and astrocytes and the changes in these dynamics that occur during the progression of diseases like epilepsy. Recording from large numbers of identified cell types has been traditionally difficult, but the advent of fluorescent indicators capable of detecting changes in the internal calcium levels of cells has led to the ability to visually record the activity of large numbers of cells. However, for most imaging techniques the temporal resolution is sharply limited by the time it takes lasers to traverse the typical raster scan. As network dynamics can evolve quite rapidly, this is a serious limitation. The present paper describes the Targeted Path Scan technique, which dramatically increases the scanning frequency by allowing the user selection of trajectories through cells of interest. TPS is discussed in the context of a study of altered network dynamics in a common rat model of epilepsy. In this study, traveling waves of calcium transients that were frequently encountered in astrocytes imaged in brain slices obtained from control rats were dramatically reduced in astrocytes imaged in brain slices obtained from rats that had experienced status epilepticus. The speed of these traveling waves would have made them impossible to identify using traditional scanning techniques.

[1]  R. Yuste,et al.  Optical probing of neuronal circuits with calcium indicators. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[2]  S. Finkbeiner,et al.  Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. , 1990, Science.

[3]  A. Charles,et al.  Intercellular signaling in glial cells: Calcium waves and oscillations in response to mechanical stimulation and glutamate , 1991, Neuron.

[4]  C. Rose,et al.  Developmental profile and properties of sulforhodamine 101—Labeled glial cells in acute brain slices of rat hippocampus , 2008, Journal of Neuroscience Methods.

[5]  J. White,et al.  Two-photon imaging of spatially extended neuronal network dynamics with high temporal resolution , 2008, Journal of Neuroscience Methods.

[6]  R. Miles,et al.  Emergence of disinhibition‐induced synchrony in the CA3 region of the guinea pig hippocampus in vitro , 2006, The Journal of physiology.

[7]  R. Racine,et al.  Modification of seizure activity by electrical stimulation. 3. Mechanisms. , 1972, Electroencephalography and clinical neurophysiology.

[8]  P. Brown Oscillatory nature of human basal ganglia activity: Relationship to the pathophysiology of Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[9]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[10]  H. Bergman,et al.  Pathological synchronization in Parkinson's disease: networks, models and treatments , 2007, Trends in Neurosciences.

[11]  Rafael Yuste,et al.  Two-photon photostimulation and imaging of neural circuits , 2007, Nature Methods.

[12]  H. Kettenmann,et al.  Different Mechanisms Promote Astrocyte Ca2+ Waves and Spreading Depression in the Mouse Neocortex , 2003, The Journal of Neuroscience.

[13]  C. Giaume,et al.  Astrocyte calcium waves: What they are and what they do , 2006, Glia.

[14]  吴立文 Epilepsy as a Dynamic Disease , 2004 .

[15]  Yitzhak Schiller,et al.  Network Dynamics during Development of Pharmacologically Induced Epileptic Seizures in Rats In Vivo , 2010, The Journal of Neuroscience.

[16]  R. Racine,et al.  Modification of seizure activity by electrical stimulation. II. Motor seizure. , 1972, Electroencephalography and clinical neurophysiology.

[17]  Michael M. Halassa,et al.  Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. , 2010, Annual review of physiology.

[18]  A. Araque,et al.  Calcium Elevation in Astrocytes Causes an NMDA Receptor-Dependent Increase in the Frequency of Miniature Synaptic Currents in Cultured Hippocampal Neurons , 1998, The Journal of Neuroscience.

[19]  F. Helmchen,et al.  Imaging cellular network dynamics in three dimensions using fast 3D laser scanning , 2007, Nature Methods.

[20]  Baljit S Khakh,et al.  Bulk Loading of Calcium Indicator Dyes to Study Astrocyte Physiology: Key Limitations and Improvements Using Morphological Maps , 2011, The Journal of Neuroscience.

[21]  Liad Hollender,et al.  High-Resolution In Vivo Imaging of the Neurovascular Unit during Spreading Depression , 2007, The Journal of Neuroscience.

[22]  N. Matsuki,et al.  Large-Scale Calcium Waves Traveling through Astrocytic Networks In Vivo , 2011, The Journal of Neuroscience.

[23]  D. Small,et al.  Astrocytes in Alzheimer's disease: emerging roles in calcium dysregulation and synaptic plasticity. , 2010, Journal of Alzheimer's disease : JAD.

[24]  M. Belluscio,et al.  Brain Oscillations, Medium Spiny Neurons, and Dopamine , 2002, Cellular and Molecular Neurobiology.

[25]  K. Wilcox,et al.  Increased coupling and altered glutamate transport currents in astrocytes following kainic-acid-induced status epilepticus , 2010, Neurobiology of Disease.

[26]  T. Murphy,et al.  Rapid Astrocyte Calcium Signals Correlate with Neuronal Activity and Onset of the Hemodynamic Response In Vivo , 2007, The Journal of Neuroscience.

[27]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[28]  Ch. von der Malsburg,et al.  A neural cocktail-party processor , 1986, Biological Cybernetics.

[29]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[30]  S. Finkbeiner Calcium waves in astrocytes-filling in the gaps , 1992, Neuron.

[31]  E. Halgren,et al.  Single-neuron dynamics in human focal epilepsy , 2011, Nature Neuroscience.

[32]  L. V. Van Eldik,et al.  Glial Activation Links Early‐Life Seizures and Long‐Term Neurologic Dysfunction: Evidence Using a Small Molecule Inhibitor of Proinflammatory Cytokine Upregulation , 2007, Epilepsia.

[33]  Eduardo Soriano,et al.  Neuronal Activity Regulates Correlated Network Properties of Spontaneous Calcium Transients in Astrocytes In Situ , 2002, The Journal of Neuroscience.

[34]  S. Gobbo,et al.  Neuronal Synchrony Mediated by Astrocytic Glutamate through Activation of Extrasynaptic NMDA Receptors , 2004, Neuron.

[35]  T. Takano,et al.  An astrocytic basis of epilepsy , 2005, Nature Medicine.

[36]  R. McCarley,et al.  Neural synchrony indexes disordered perception and cognition in schizophrenia. , 2004, Proceedings of the National Academy of Sciences of the United States of America.