Spike inference from calcium imaging using sequential Monte Carlo methods

Biophysical Journal

Volumn 97, Issue 2, 2009, Pages 636-655

  Vogelstein, Joshua T ^a   Watson, Brendon O ^b   Packer, Adam M ^b   Yuste, Rafael ^b,c   Jedynak, Bruno ^d   Paninskik, Liam ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION;

ACTION POTENTIAL; ANALYTICAL ERROR; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FLUORESCENCE; MOLECULAR DYNAMICS; MOLECULAR IMAGING; MONTE CARLO METHOD; MOUSE; NONHUMAN; SIGNAL NOISE RATIO;

EID: 68949128883     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2008.08.005     Document Type: Article

References (79)

1. Yuste, R., and A. Konnerth. 2006. Imaging in Neuroscience and Development, A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Tsien, R. Y. 1981. A non-disruptive technique for loading calcium buffers and indicators into cells. Nature. 290:527-528.
3. Yuste, R., and L. C. Katz. 1991. Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron. 6:333-344.
4. 2+ imaging. Pflugers Arch. 446:766-773.
5. Stosiek, C., O. Garaschuk, K. Holthoff, and A. Konnerth. 2003. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA. 100:7319-7324.
6. 2+ imaging of local neuronal circuits. Neuron. 53:789-803.
7. Nevian, T., and F. Helmchen. 2007. Calcium indicator loading of neurons using single-cell electroporation. Pflugers Arch. 454:675-688.
8. 2+ based on green fluorescent proteins and calmodulin. Nature. 388:882-887.
9. Griesbeck, O., G. S. Baird, R. E. Campbell, D. A. Zacharias, and R. Y. Tsien. 2001. Reducing the environmental sensitivity of yellow fluorescent protein. Mechanism and applications. J. Biol. Chem. 276:29188-29194.
10. 2+ probe composed of a single green fluorescent protein. Nat. Biotechnol. 19:137-141.
11. Denk, W., J. H. Strickler, and W. W. Webb. 1990. Two-photon laser scanning fluorescence microscopy. Science. 248:73-76.
12. Oheim, M., E. Beaurepaire, E. Chaigneau, J. Mertz, and S. Charpak. 2001. Two-photon microscopy in brain tissue: parameters influencing the imaging depth. J. Neurosci. Methods. 111:29-37.
13. 3 regenerative amplifier. Opt. Lett. 28:1022-1024.
14. Flusberg, B. A., E. D. Cocker, W. Piyawattanametha, J. C. Jung, E. L. M. Cheung, et al. 2005. Fiber-optic fluorescence imaging. Nat. Methods. 2:941-950.
15. 2+ responses. Nature. 354:73-76.
16. Yuste, R., and W. Denk. 1995. Dendritic spines as basic functional units of neuronal integration. Nature. 375:682-684.
17. Engert, F., and T. Bonhoeffer. 1999. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature. 399:66-70.
18. Nimchinsky, E. A., R. Yasuda, T. G. Oertner, and K. Svoboda. 2004. The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J. Neurosci. 24:2054-2064.
19. Majewska, A., G. Yiu, and R. Yuste. 2000. A custom-made two-photon microscope and deconvolution system. Pflugers Arch. 441:398-408.
20. 2+ extrusion. J. Neurosci. 26:8183-8194.
21. Sdrulla, A. D., and D. J. Linden. 2007. Double dissociation between long-term depression and dendritic spine morphology in cerebellar Purkinje cells. Nat. Neurosci. 10:546-548.
22. Majewska, A. K., J. R. Newton, and M. Sur. 2006. Remodeling of synaptic structure in sensory cortical areas in vivo. J. Neurosci. 26:3021-3029.
23. Brenowitz, S. D., and W. G. Regehr. 2007. Reliability and heterogeneity of calcium signaling at single presynaptic boutons of cerebellar granule cells. J. Neurosci. 27:7888-7898.
24. 2+ signaling in dendrites of pyramidal neurons. Biophys. J. 70:1069-1081.
25. Svoboda, K., D. W. Tank, and W. Denk. 1996. Direct measurement of coupling between dendritic spines and shafts. Science. 272:716-719.
26. Maravall, M., Z. F. Mainen, B. L. Sabatini, and K. Svoboda. 2000. Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys. J. 78:2655-2667.
27. O'Malley, D. M., Y. H. Kao, and J. R. Fetcho. 1996. Imaging the functional organization of zebrafish hindbrain segments during escape behaviors. Neuron. 17:1145-1155.
28. Smetters, D., A. Majewska, and R. Yuste. 1999. Detecting action potentials in neuronal populations with calcium-imaging. Methods. 18:215-221.
29. Ikegaya, Y., G. Aaron, R. Cossart, D. Aronov, I. Lampl, et al. 2004. Synfire chains and cortical songs: temporal modules of cortical activity. Science. 304:559-564.
30. Niell, C. M., and S. J. Smith. 2005. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron. 45:941-951.
31. Ohki, K., S. Chung, Y. H. Ch'ng, P. Kara, and R. C. Reid. 2005. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature. 433:597-603.
32. Ohki, K., S. Chung, P. Kara, M. Hbener, T. Bonhoeffer, et al. 2006. Highly ordered arrangement of single neurons in orientation pinwheels. Nature. 442:925-928.
33. Yaksi, E., B. Judkewitz, and R. W. Friedrich. 2007. Topological Reorganization of Odor Representations in the Olfactory Bulb. PLoS Biol. 5:e178.
34. Sato, T. R., N. W. Gray, Z. F. Mainen, and K. Svoboda. 2007. The functional microarchitecture of the mouse barrel cortex. PLoS Biol. 5:e189.
35. Root, C. M., J. L. Semmelhack, A. M. Wong, J. Flores, and J. W. Wang. 2007. Propagation of olfactory information in Drosophila. Proc. Natl. Acad. Sci. USA. 104:11826-11831.
36. Sjulson, L., and G. Miesenböck. 2007. Optical recording of action potentials and other discrete physiological events: a perspective from signal detection theory. Physiology (Bethesda). 22:47-55.
37. Fan, G. Y., H. Fujisaki, A. Miyawaki, R. K. Tsay, R. Y. Tsien, et al. 1999. Video-rate scanning two-photon excitation fluorescence microscopy and ratio imaging with cameleons. Biophys. J. 76:2412-2420.
38. 2+ imaging. Cell Calcium. 30:383-393.
39. Iyer, V., T. M. Hoogland, and P. Saggau. 2006. Fast functional imaging of single neurons using random-access multiphoton (RAMP) microscopy. J. Neurophysiol. 95:535-545.
40. 2+ indicators. J. Neurosci. 24:9572-9579.
41. 2+ sensor. Biophys J. 93:4031-4040.
42. Yasuda, R., E. A. Nimchinsky, V. Scheuss, T. A. Pologruto, T. G. Oertner, et al. 2004. Imaging calcium concentration dynamics in small neuronal compartments. Sci. STKE. 219:l5.
43. Reiff, D. F., A. Ihring, G. Guerrero, E. Y. Isacoff, M. Joesch, et al. 2005. In vivo performance of genetically encoded indicators of neural activity in flies. J. Neurosci. 25:4766-4778.
44. 2+ imaging. Nat. Methods. 3:377-383.
45. Borst, A., and H. D. I. Abarbanel. 2007. Relating a calcium indicator signal to the unperturbed calcium concentration time-course. Theor. Biol. Med. Model. 4:7.
46. Kerr, J. N. D., D. Greenberg, and F. Helmchen. 2005. Imaging input and output of neocortical networks in vivo. Proc. Natl. Acad. Sci. USA. 102:14063-14068.
47. Greenberg, D. S., A. R. Houweling, and J. N. D. Kerr. 2008. Population imaging of ongoing neuronal activity in the visual cortex of awake rats. Nat. Neurosci. 11:749-751.
48. Holekamp, T. F., D. Turaga, and T. E. Holy. 2008. Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron. 57:661-672.
49. Sasaki, T., N. Takahashi, N. Matsuki, and Y. Ikegaya. 2008. Fast and accurate detection of action potentials from somatic calcium fluctuations. J. Neurophysiol. 100:1668.
50. Sabatini, B. L., and W. G. Regehr. 1998. Optical measurement of presynaptic calcium currents. Biophys. J. 74:1549-1563.
51. Cornelisse, L. N., R. A. J. van Elburg, R. M. Meredith, R. Yuste, and H. D. Mansvelder. 2007. High speed two-photon imaging of calcium dynamics in dendritic spines: consequences for spine calcium kinetics and buffer capacity. PLoS ONE. 2:e1073.
52. Regehr, W. G., and P. P. Atluri. 1995. Calcium transients in cerebellar granule cell presynaptic terminals. Biophys. J. 68:2156-2170.
53. Smith, A., A. Doucet, N. de Freitas, and N. Gordon. 2001. Sequential Monte Carlo Methods in Practice. Springer, New York.
54. Dempster, A., N. Laird, D. Rubin, et al. 1977. Maximum likelihood from incomplete data vis the EM algorithm. J. Royal Stat. Soc. B. 39:1-38.
55. Gao, Y., M. Black, E. Bienenstock, S. Shoham, and J. Donoghue. 2002. Probabilistic inference of hand motion from neural activity in motor cortex. Adv. Neural Inf. Process. Syst. 14:213-220.
56. Brockwell, A. E., A. L. Rojas, and R. E. Kass. 2004. Recursive Bayesian decoding of motor cortical signals by particle filtering. J. Neurophysiol. 91:1899-1907.
57. Kelly, R., and T. Lee. 2004. Decoding V1 neuronal activity using particle filtering with Volterra kernels. Adv. Neural Inf. Process. Syst. 15:1359-1366.
58. Samejima, K., K. Doya, Y. Ueda, and M. Kimura. 2004. Estimating internal variables and parameters of a learning agent by a particle filter. Adv. Neural Inf. Process. Syst. 9:16.
59. Huys, Q., and L. Paninski. 2006. Smoothing of, and parameter estimation from, noisy biophysical recordings. PLoS Comput. Biol. 5:e1000379.
60. Sanger, T. D. 2007. Bayesian filtering of myoelectric signals. J. Neurophysiol. 97:1839-1845.
61. Ergün, A., R. Barbieri, U. T. Eden, M. A. Wilson, and E. N. Brown. 2007. Construction of point process adaptive filter algorithms for neural systems using sequential Monte Carlo methods. IEEE Trans. Biomed. Eng. 54:419-428.
62. Rabiner, L. R. 1989. A tutorial on Hidden Markov Models and selected applications in speech recognition. Proc. IEEE. 72:257-286.
63. Kalman, R. 1960. A new approach to linear filtering and prediction problems. Journal of Basic Engineering. 82:35-45.
64. Douc, R., O. Cappe, and E. Moulines. 2005. Comparison of resampling schemes for particle filtering. Proc. 4th International Symposium on Image and Signal Processing and Analysis. 64-69.
65. Wills, A., T. Schön, and B. Ninness. 2008. Parameter estimation for discrete-time nonlinear systems using EM. Proc. 17th IFAC World Congress.
66. MacLean, J. N., B. O. Watson, G. B. Aaron, and R. Yuste. 2005. Internal dynamics determine the cortical response to thalamic stimulation. Neuron. 48:811-823.
67. McCullagh, P., and J. Nelder. 1989. Chapman and Hall, Generalized Linear Models.
68. Paninski, L., J. Pillow, and J. Lewi. 2007. Statistical models for neural encoding, decoding, and optimal stimulus design. Prog. Brain Res. 165:493-507.
69. Reference deleted in proof.
70. Paninski, L. 2004. Maximum likelihood estimation of cascade point-process neural encoding models. Network: Computation in Neural Systems. 15:243-262.
71. Truccolo, W., U. T. Eden, M. R. Fellows, J. P. Donoghue, and E. N. Brown. 2005. A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. J. Neurophysiol. 93:1074-1089.
72. Paninski, L., J. W. Pillow, and E. P. Simoncelli. 2004. Maximum likelihood estimation of a stochastic integrate-and-fire neural encoding model. Neural Comput. 16:2533-2561.
73. Vogelstein, J., A. Packer, R. Yuste, and L. Paninski. 2009. Towards inferring neural circuits from population calcium imaging. Frontiers in Systems Neuroscience. Conference Abstract: Computational and systems neuroscience.
74. Göbel, W., and F. Helmchen. 2007. In vivo calcium imaging of neural network function. Physiology (Bethesda). 22:358-365.
75. Dombeck, D. A., A. N. Khabbaz, F. Collman, T. L. Adelman, and D. W. Tank. 2007. Imaging large-scale neural activity with cellular resolution in awake, mobile mice. Neuron. 56:43-57.
76. Tsien, R. W., and R. Y. Tsien. 1990. Calcium channels, stores, and oscillations. Annu. Rev. Cell Biol. 6:715-760.
77. Pillow, J., J. Shlens, L. Paninski, A. Sher, A. Litke, E. Chichilnisky, and E. Simoncelli. 2008. Spatiotemporal correlations and visual signaling in a complete neuronal population. Nature. 454:995-999.
78. Kass, R., and A. Raftery. 1995. Bayes factors. J. Am. Stat. Assoc. 90:773-795.
79. Shumway, R., and D. Stoffer. 2006. Time Series Analysis and Its Applications, 2nd edition. Springer, New York.