Action potential propagation imaged with high temporal resolution near-infrared video microscopy and polarized light

Department of Physics and Astronomy, Washington State University, Pullman, WA 99164-2814, USA.
NeuroImage (Impact Factor: 6.36). 05/2008; 40(3):1034-43. DOI: 10.1016/j.neuroimage.2007.12.055
Source: PubMed


To identify the neural constituents responsible for generating polarized light changes, we created spatially resolved movies of propagating action potentials from stimulated lobster leg nerves using both reflection and transmission imaging modalities. Changes in light polarization are associated with membrane depolarization and provide sub-millisecond temporal resolution. Typically, signals are detected using light transmitted through tissue; however, because we eventually would like to apply polarization techniques in-vivo, reflected light is required. In transmission mode, the optical signal was largest throughout the center of the nerve, suggesting that most of the optical signal arose from the inner nerve bundle. In reflection mode, polarization changes were largest near the edges, suggesting that most of the optical signal arose from the outer sheath. In support of these observations, an optical model of the tissue showed that the outer sheath is more reflective while the inner nerve bundle is more transmissive. In order to apply these techniques in-vivo, we must consider that brain tissue does not have a regular orientation of processes as in the lobster nerve. We tested the effect of randomizing cell orientation by tying the nerve in an overhand knot prior to imaging, producing polarization changes that can be imaged even without regular cell orientations.

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    • "A theoretical framework for interpreting the mechanism of the SPR-based neural activity recording should be established to gain deeper insight into the mechanism of SPR neural activity detection and to use this technique in different applications such as SPRbased in vivo neural recording [15] [16] [17] [18] and image acquisition of neural activity in cultured neural network [19] [20] [21] [22]. Several near field and light transport theories have been used to successfully explain the experimental results of biomedical optics [23] [24] [25] [26] [27] [28] [29] [30] [31] [32]; these physical theories thus may be able to explain the mechanism by which SPR detects neural activity. "
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    ABSTRACT: The mechanism of neural activity detection using the surface plasmon resonance (SPR) phenomenon was theoretically explored in this paper. Investigating the mechanism of SPR neural recordings has been difficult due to the complex relationship between different physiological and physical processes such as excitation of a nerve fiber and coherent charge fluctuations on the metal surface. This paper examines how these different processes may be connected by introducing a set of compartmental theoretical models that deal with the molecular scale phenomena; Poisson–Boltzmann (PB) equation, which was used to describe the ion concentration change under the time varying electrostatic potential, Drude–Lorentz electron model, which was used to describe electron dynamics under the time varying external forces, and a Fresnel's three-layered model, which expresses the reflectivity of the SPR system in terms of the dielectric constants. Each physical theoretical model was numerically analyzed using the finite element method (FEM) formulated for the PB equation and the Green's method formulated for the Drude–Lorentz electron equation. The model predicts that the ionic thermal force originating from the opening of the K+ ion channel is fundamental for modifying the dipole moment of the gold's free electron; thus, the reflectivity is changed in the SPR system. The discussion was done also on important attributes of the SPR signal such as biphasic fluctuation and the electrical noise-free characteristics.
    Optics & Laser Technology 07/2011; 43(5-43):938-948. DOI:10.1016/j.optlastec.2010.12.010 · 1.65 Impact Factor
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    • "IOSs associated with hemodynamic and metabolic changes [24, 25] can be used to infer the physiological well-being of the retina, but they are not direct measure of neural activities. On the other hand, it has been demonstrated that fast IOSs have the time courses that are comparable to that of the retinal electrophysiological kinetics, i.e., electroretinogram (ERG) responses [26, 27]. Imaging fast IOSs may thus provide a new method to directly evaluate the functional integrity of photoreceptors and inner retina neurons. "
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    ABSTRACT: High resolution monitoring of stimulus-evoked retinal neural activities is important for understanding retinal neural mechanisms, and can be a powerful tool for retinal disease diagnosis and treatment outcome evaluation. Fast intrinsic optical signals (IOSs), which have the time courses comparable to that of electrophysiological activities in the retina, hold the promise for high resolution imaging of retinal neural activities. However, application of fast IOS imaging has been hindered by the contamination of slow, high magnitude optical responses associated with transient hemodynamic and metabolic changes. In this paper we demonstrate the feasibility of separating fast retinal IOSs from slow optical responses by combining flicker stimulation and dynamic (temporal) differential image processing. A near infrared flood-illumination microscope equipped with a high-speed (1000 Hz) digital camera was used to conduct concurrent optical imaging and ERG measurement of isolated frog retinas. High spatiotemporal resolution imaging revealed that fast IOSs could follow flicker frequency up to at least 6 Hz. Comparable time courses of fast IOSs and ERG kinetics provide evidence that fast IOSs are originated from stimulus activated retinal neurons.
    Optics Express 03/2010; 18(7):7210-8. DOI:10.1364/OE.18.007210 · 3.49 Impact Factor
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    • "Once placed within the longitudinal groove, the nerve was immersed in crab Ringer's solution made of 525mM/l NaCl, 13.3mM/l KCl, 12.4mM/l CaCl 2 , 24.8mM/l MgCl 2 and 5mM/l Dextrose (Schei et al., 2008). The nerve was blotted using filter paper at the start of each 1 minute recording and then irrigated again as soon as it was completed. "
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    ABSTRACT: Electrical impedance tomography (EIT) is a recently developed medical imaging method which has the potential to produce images of fast neuronal depolarization in the brain. The principle is that current remains in the extracellular space at rest but passes into the intracellular space during depolarization through open ion channels. As current passes into the intracellular space across the capacitance of cell membranes at higher frequencies, applied current needs to be below 100 Hz. A method is presented for its measurement with subtraction of the contemporaneous evoked potentials which occur in the same frequency band. Neuronal activity is evoked by stimulation and resistance is recorded from the potentials resulting from injection of a constant current square wave at 1 Hz with amplitude less than 25% of the threshold for stimulating neuronal activity. Potentials due to the evoked activity and the injected square wave are removed by subtraction. The method was validated with compound action potentials in crab walking leg nerve. Resistance changes of -0.85+/-0.4% (mean+/-SD) occurred which decreased from -0.97+/-0.43% to -0.46+/-0.16% with spacing of impedance current application electrodes from 2 to 8 mm but did not vary significantly with applied currents of 1-10 microA. These tallied with biophysical modelling, and so were consistent with a genuine physiological origin. This method appears to provide a reproducible and artefact free means for recording resistance changes during neuronal activity which could lead to the long-term goal of imaging of fast neural activity in the brain.
    Journal of Neuroscience Methods 06/2009; 180(1):87-96. DOI:10.1016/j.jneumeth.2009.03.012 · 2.05 Impact Factor
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