Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning

Access to three-dimensional structures in the brain is fundamental to probe signal processing at multiple levels, from integration of synaptic inputs to network activity mapping. Here, we present an optical method for independent three-dimensional photoactivation and imaging by combination of digital holography with remote-focusing. We experimentally demonstrate compensation of spherical aberration for out-of-focus imaging in a range of at least 300 μm, as well as scanless imaging along oblique planes. We apply this method to perform functional imaging along tilted dendrites of hippocampal pyramidal neurons in brain slices, after photostimulation by multiple spots glutamate uncaging. By bringing extended portions of tilted dendrites simultaneously in-focus, we monitor the spatial extent of dendritic calcium signals, showing a shift from a widespread to a spatially confined response upon blockage of voltage-gated Na+ channels.

[1]  N. Spruston,et al.  Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. , 1995, Science.

[2]  Nace L. Golding,et al.  Dendritic Sodium Spikes Are Variable Triggers of Axonal Action Potentials in Hippocampal CA1 Pyramidal Neurons , 1998, Neuron.

[3]  J. Magee,et al.  Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. , 1999, Journal of neurophysiology.

[4]  Dan Cojoc,et al.  Wave front engineering for microscopy of living cells. , 2005, Optics express.

[5]  M. London,et al.  Dendritic computation. , 2005, Annual review of neuroscience.

[6]  Mathieu Cohen,et al.  Wave-front reconstruction from multidirectional phase derivatives generated by multilateral shearing interferometers. , 2005, Optics letters.

[7]  J. Magee,et al.  Integrative Properties of Radial Oblique Dendrites in Hippocampal CA1 Pyramidal Neurons , 2006, Neuron.

[8]  Dejan Zecevic,et al.  Dendritic signals from rat hippocampal CA1 pyramidal neurons during coincident pre‐ and post‐synaptic activity: a combined voltage‐ and calcium‐imaging study , 2007, The Journal of physiology.

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

[10]  Tony Wilson,et al.  Aberration-free optical refocusing in high numerical aperture microscopy. , 2007, Optics letters.

[11]  T. Sejnowski,et al.  A Compact Multiphoton 3D Imaging System for Recording Fast Neuronal Activity , 2007, PloS one.

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

[13]  Valentina Emiliani,et al.  Patterned two-photon illumination by spatiotemporal shaping of ultrashort pulses. , 2008, Optics express.

[14]  Brendon O. Watson,et al.  SLM Microscopy: Scanless Two-Photon Imaging and Photostimulation with Spatial Light Modulators , 2008, Frontiers in neural circuits.

[15]  C Dunsby,et al.  Optically sectioned imaging by oblique plane microscopy. , 2008, Optics express.

[16]  T. Wilson,et al.  An optical technique for remote focusing in microscopy , 2008 .

[17]  Keith J. Kelleher,et al.  Three-dimensional random access multiphoton microscopy for functional imaging of neuronal activity , 2008, Nature Neuroscience.

[18]  Christoph Lutz,et al.  Holographic photolysis of caged neurotransmitters , 2008, Nature Methods.

[19]  David Ogden,et al.  Laser photolysis of caged compounds at 405nm: Photochemical advantages, localisation, phototoxicity and methods for calibration , 2009, Journal of Neuroscience Methods.

[20]  Michael D. Ehlers,et al.  Molecular genetics and imaging technologies for circuit-based neuroanatomy , 2009, Nature.

[21]  Valentina Emiliani,et al.  Temporal focusing with spatially modulated excitation. , 2009, Optics express.

[22]  D. McCormick,et al.  Rapid Neocortical Dynamics: Cellular and Network Mechanisms , 2009, Neuron.

[23]  Dirk Trauner,et al.  New photochemical tools for controlling neuronal activity , 2009, Current Opinion in Neurobiology.

[24]  T Wilson,et al.  Liquid crystal director dynamics imaged using two-photon fluorescence microscopy with remote focusing. , 2009, Physical review letters.

[25]  Christian Stricker,et al.  Arbitrary multisite two-photon excitation in four dimensions , 2009 .

[26]  Bradley J. Baker,et al.  Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[27]  R. Silver,et al.  A compact Acousto-Optic Lens for 2D and 3D femtosecond based 2-photon microscopy. , 2010, Optics express.

[28]  Valentina Emiliani,et al.  Holographic Photolysis for Multiple Cell Stimulation in Mouse Hippocampal Slices , 2010, PloS one.

[29]  Fabio Benfenati,et al.  Simultaneous two-photon imaging and photo-stimulation with structured light illumination. , 2010, Optics express.

[30]  Christopher Smith,et al.  Arbitrary-scan imaging for two-photon microscopy , 2010, BiOS.

[31]  Kraig E. Sheetz,et al.  Remote focusing for programmable multi-layer differential multiphoton microscopy , 2010, Biomedical optics express.

[32]  D A Agard,et al.  High‐resolution wide‐field microscopy with adaptive optics for spherical aberration correction and motionless focusing , 2010, Journal of microscopy.

[33]  K. Deisseroth,et al.  Molecular and Cellular Approaches for Diversifying and Extending Optogenetics , 2010, Cell.

[34]  Kishan Dholakia,et al.  Application of dynamic diffractive optics for enhanced femtosecond laser based cell transfection. , 2010, Journal of biophotonics.

[35]  B. Sabatini,et al.  Glutamate induces de novo growth of functional spines in developing cortex , 2011, Nature.

[36]  C. W. Smith,et al.  Resolution of oblique-plane images in sectioning microscopy. , 2011, Optics express.

[37]  Christopher Dunsby,et al.  Optically sectioned imaging by oblique plane microscopy , 2011, BiOS.

[38]  Tony Wilson,et al.  Agitation-free multiphoton microscopy of oblique planes. , 2011, Optics letters.

[39]  Valentina Emiliani,et al.  Three-dimensional holographic photostimulation of the dendritic arbor , 2011, Journal of neural engineering.

[40]  Rafael Yuste,et al.  Imaging Voltage in Neurons , 2011, Neuron.