Holographically patterned activation using photo-absorber induced neural–thermal stimulation

Objective. Patterned photo-stimulation offers a promising path towards the effective control of distributed neuronal circuits. Here, we demonstrate the feasibility and governing principles of spatiotemporally patterned microscopic photo-absorber induced neural–thermal stimulation (PAINTS) based on light absorption by exogenous extracellular photo-absorbers. Approach. We projected holographic light patterns from a green continuous-wave (CW) or an IR femtosecond laser onto exogenous photo-absorbing particles dispersed in the vicinity of cultured rat cortical cells. Experimental results are compared to predictions of a temperature-rate model (where membrane currents follow I ∝ dT/dt). Main results. The induced microscopic photo-thermal transients have sub-millisecond thermal relaxation times and stimulate adjacent cells. PAINTS activation thresholds for different laser pulse durations (0.02 to 1 ms) follow the Lapicque strength-duration formula, but with different chronaxies and minimal threshold energy levels for the two excitation lasers (an order of magnitude lower for the IR system <50 nJ). Moreover, the empirical thresholds for the CW system are found to be in good agreement with detailed simulations of the temperature-rate model, but are generally lower for the IR system, suggesting an auxiliary excitation mechanism. Significance. Holographically patterned PAINTS could potentially provide a means for minimally intrusive control over neuronal dynamics with a high level of spatial and temporal selectivity.

[1]  William J Tyler,et al.  A quantitative overview of biophysical forces impinging on neural function , 2013, Physical biology.

[2]  Inbar Brosh,et al.  Holographic optogenetic stimulation of patterned neuronal activity for vision restoration , 2013, Nature Communications.

[3]  Rafael Yuste,et al.  Two-photon optogenetics of dendritic spines and neural circuits in 3D , 2012, Nature Methods.

[4]  Igor L. Medintz,et al.  Nanoparticle targeting to neurons in a rat hippocampal slice culture model , 2012, ASN neuro.

[5]  Benjamin Migliori,et al.  Photoactivation of neurons by laser-generated local heating. , 2012, AIP advances.

[6]  Valentina Emiliani,et al.  Reshaping the optical dimension in optogenetics , 2012, Current Opinion in Neurobiology.

[7]  S. Shoham,et al.  Photo-Thermal Neural Excitation by Extrinsic and Intrinsic Absorbers: A Temperature-Rate Model , 2012, 1201.4617.

[8]  Earl J. Bergey,et al.  Organically Modified Silica Nanoparticles Are Biocompatible and Can Be Targeted to Neurons In Vivo , 2012, PloS one.

[9]  Mikhail G. Shapiro,et al.  Infrared light excites cells by changing their electrical capacitance , 2012, Nature Communications.

[10]  Karl Deisseroth,et al.  Optogenetics in Neural Systems , 2011, Neuron.

[11]  Jonathan M. Cayce,et al.  Pulsed infrared light alters neural activity in rat somatosensory cortex in vivo , 2011, NeuroImage.

[12]  Claus-Peter Richter,et al.  Infrared photostimulation of the crista ampullaris , 2011, The Journal of physiology.

[13]  Claus-Peter Richter,et al.  Neural stimulation with optical radiation , 2011, Laser & photonics reviews.

[14]  E. Isacoff,et al.  Scanless two-photon excitation of channelrhodopsin-2 , 2010, Nature Methods.

[15]  Heng Huang,et al.  Remote control of ion channels and neurons through magnetic-field heating of nanoparticles. , 2010, Nature nanotechnology.

[16]  W. N. Ross,et al.  Na+ imaging reveals little difference in action potential–evoked Na+ influx between axon and soma , 2010, Nature Neuroscience.

[17]  Daniel Weinreich,et al.  Excitation of primary afferent neurons by near-infrared light in vitro , 2010, Neuroreport.

[18]  Eduardo Fernández,et al.  Erratum: Toward the development of a cortically based visual neuroprosthesis (Journal of Neural Engineering (2009) 6 (035001)) , 2009 .

[19]  N Farah,et al.  Design and characteristics of holographic neural photo-stimulation systems , 2009, Journal of neural engineering.

[20]  Eduardo Fernandez,et al.  Toward the development of a cortically based visual neuroprosthesis , 2009, Journal of neural engineering.

[21]  James O. Phillips,et al.  Optical nerve stimulation for a vestibular prosthesis , 2009, BiOS.

[22]  Yusuf Tufail,et al.  Remote Excitation of Neuronal Circuits Using Low-Intensity, Low-Frequency Ultrasound , 2008, PloS one.

[23]  Vladimir P Zharov,et al.  Quantum dots as multimodal photoacoustic and photothermal contrast agents. , 2008, Nano letters.

[24]  Anita Mahadevan-Jansen,et al.  Biophysical mechanisms of transient optical stimulation of peripheral nerve. , 2007, Biophysical journal.

[25]  Claus-Peter Richter,et al.  Optical Stimulation of the Facial Nerve: A New Monitoring Technique? , 2007, The Laryngoscope.

[26]  Anita Mahadevan-Jansen,et al.  Pulsed laser versus electrical energy for peripheral nerve stimulation , 2007, Journal of Neuroscience Methods.

[27]  R Clay Reid,et al.  Demonstration of artificial visual percepts generated through thalamic microstimulation , 2007, Proceedings of the National Academy of Sciences.

[28]  Giancarlo Ruocco,et al.  Computer generation of optimal holograms for optical trap arrays. , 2007, Optics express.

[29]  Claus-Peter Richter,et al.  Laser stimulation of the auditory nerve , 2006, Lasers in surgery and medicine.

[30]  Anita Mahadevan-Jansen,et al.  Application of infrared light for in vivo neural stimulation. , 2005, Journal of biomedical optics.

[31]  Yuji Ikegaya,et al.  Large-scale imaging of cortical network activity with calcium indicators , 2005, Neuroscience Research.

[32]  P. Konrad,et al.  Optical stimulation of neural tissue in vivo. , 2005, Optics letters.

[33]  C. Veraart,et al.  Creating a meaningful visual perception in blind volunteers by optic nerve stimulation , 2005, Journal of neural engineering.

[34]  Ralf Brinkmann,et al.  RPE damage thresholds and mechanisms for laser exposure in the microsecond-to-millisecond time regimen. , 2005, Investigative ophthalmology & visual science.

[35]  W. Schrof,et al.  Three-dimensional thermal imaging using two-photon microscopy , 2004 .

[36]  R. Costalat,et al.  A Few Comments on Electrostatic Interactions in Cell Physiology , 2000, Acta biotheoretica.

[37]  Paiboon Tangyunyong,et al.  Fluorescent microthermal imaging—theory and methodology for achieving high thermal resolution images , 1995 .

[38]  Richard J. Watts,et al.  Temperature dependence of the photophysical and photochemical properties of the tris(2,2'-bipyridyl)ruthenium(II) ion in aqueous solution , 1976 .

[39]  D. Grahame The electrical double layer and the theory of electrocapillarity. , 1947, Chemical reviews.

[40]  P. Romano Association for Research in Vision and Ophthalmology. , 2000, Binocular vision & strabismus quarterly.

[41]  B. Hooper Optical-thermal response of laser-irradiated tissue , 1996 .

[42]  Ashleyj . Welch,et al.  Optical-Thermal Response of Laser-Irradiated Tissue , 1995 .

[43]  F. Barnes Cell membrane temperature rate sensitivity predicted from the Nernst equation. , 1984, Bioelectromagnetics.