Deciphering elapsed time and predicting action timing from neuronal population signals

Frontiers in Computational Neuroscience

Volumn 5, Issue , 2011, Pages

  Shinomoto, Shigeru ^a   Omi, Takahiro ^a   Mita, Akihisa ^b   Mushiake, Hajime ^b   Shima, Keisetsu ^b   Matsuzaka, Yoshiya ^b   Tanji, Jun ^c  

^a KYOTO UNIVERSITY   (Japan)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

Bayesian analysis; Pre supplementary motor area; Prefrontal cortex; Principal component analysis; State space; Timing of action

Indexed keywords

ACTIVATION ANALYSIS; BRAIN; DECODING; PRINCIPAL COMPONENT ANALYSIS; STATE SPACE METHODS;

BAYESIAN ALGORITHMS; BAYESIAN ANALYSIS; NEURONAL POPULATIONS; POPULATION ANALYSIS; PREFRONTAL CORTEX; SUPPLEMENTARY MOTOR AREAS; TEMPORAL INFORMATION; TIMING OF ACTION;

NEURONS;

ANIMAL EXPERIMENT; BRAIN FUNCTION; FIRING RATE; HAPLORHINI; NERVE CELL; NONHUMAN; POPULATION MODEL; SUPPLEMENTARY MOTOR AREA;

EID: 84959471585     PISSN: None     EISSN: 16625188     Source Type: Journal    
DOI: 10.3389/fncom.2011.00029     Document Type: Article

References (55)

1. Achtman, N., Afshar, A., Santhanam, G., Yu, B. M., Ryu, S. I., and Shenoy, K. V. (2007). Free-paced high-performance brain-computer interfaces. J. Neural Eng. 4, 336-347.
2. Allan, L. G. (1979). The perception of time. Percept. Psychophys. 26, 340-354
3. Bak, M. J., and Schmidt, E. M. (1977). An improved time-amplitude window discriminator. IEEE Trans. Biomed. Eng. 24, 486-489.
4. Bansal, A. K., Vargas-Irwin, C. E., Truccolo, W., and Donoghue, J. P. (2011). Relationships among low-frequency local field potentials, spiking activity and 3-D reach and grasp kinematics in primary motor and ventral premotor cortices. J. Neurophysiol. 105, 1603-1619
5. Beck, J. M, Ma, W. J., Kiani, R., Hanks, T., Churchland, A. K., Roitman, J., Shadlen, M. N., Latham, P. E., and Pouget, A. (2008). Probabilistic population codes for Bayesian decision making. Neuron 60, 1142-1152.
6. Brody, C. D., Hernández, A., Zainos, A., and Romo, R. (2003). Timing and neural encoding of somatosensory parametric working memory in macaque prefrontal cortex. Cereb. Cortex 13, 1196-1207.
7. Brown, G. D. A., Neath, I., and Chater, N. (2007). A temporal ratio model of memory. Psychol. Rev. 114, 539-576
8. Buhusi, C. V., and Meck, W. H. (2005). What makes us tick? Functional and neural mechanisms of interval timing. Nat. Rev. Neurosci. 6, 755-765.
9. Buonomano, D. V., and Laje, R. (2010). Population clocks: motor timing with neural dynamics. Trends Cogn. Sci. (Regul. Ed.) 14, 520-527.
10. Carmena, J. M., Lebedev, M. A., Crist, R. E., O’Doherty, J. E., Santucci, D. M., Dimitrov, D. F., Patil, P. G., Henriquez, C. S., and Nicolelis, M. A. L. (2003). Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol. 1, e42. doi: 10.1371/journal.pbio.0000042
11. Churchland, M. M., Yu, B. M., Cunningham, J. P., Sugrue, L. P., Cohen, M. R., Corrado, G. S., Newsome, W. T., Clark, A. M., Hosseini, P., Scott, B. B., Bradley, D. C., Smith, M. A., Kohn, A., Movshon, J. A., Armstrong, K. M., Moore, T., Chang, S. W., Snyder, L. H., Lisberger, S. G., Priebe, N. J., Finn, I. M., Ferster, D., Ryu, S. I., Santhanam, G., Sahani, M., and Shenoy, K. V. (2010). Stimulus onset quenches neural variability: a widespread cortical phenomenon. Nat. Neurosci. 13, 369-378.
12. Coull, J. T., Vidal, F., Nazarian, B., and Macar, F. (2004). Functional anatomy of the attentional modulation of time estimation. Science 303, 1506-1508.
13. Cunningham, J. P., Gilja, V., Ryu, S. I., and Shenoy, K. V. (2009). Methods for estimating neural firing rates, and their application to brainmachine interfaces. Neural Netw. 22, 1235-1246.
14. Durstewitz, D. (2003). Self-organizing neural integrator predicts interval times through climbing activity. J. Neurosci. 23, 5342-5353.
15. Durstewitz, D. (2004). Neural representation of interval time. Neuroreport 15, 745-749.
16. Evarts, E. V. (1968). A technique for recording activity of subcortical neurons in moving animals. Electroencephalogr. Clin. Neurophysiol. 24, 83-86.
17. Fiala, J. C., Grossberg, S., and Bullock, D. (1996). Metabotropic glutamate receptor activation in cerebellar Purkinje cells as substrate for adaptive timing of the classically conditioned eye-blink response. J. Neurosci. 16, 3760-3774.
18. Gavornik, J. P., and Shouval, H. Z. (2011). A network of spiking neurons that can represent interval timing: mean field analysis. J. Comput. Neurosci. 30, 501-513.
19. Hopfield, J. J., and Brody, C. D. (2001). What is a moment? Transient synchrony as a collective mechanism for spatiotemporal integration. Proc. Natl. Acad. Sci. U.S.A. 98, 1282-1287
20. Ivry, R. B. (1996). The representation of temporal information in perception and motor control. Curr. Opin. Neurobiol. 6, 851-857.
21. Jacobs, A. L., Fridman, G., Douglas, R. M., Alam, N. M., Latham, P. E., Prusky, G. T., and Nirenberg, S. (2009). Ruling out and ruling in neural codes. Proc. Natl. Acad. Sci. U.S.A. 106, 5936-5941
22. Jazayeri, M., and Shadlen, M. N. (2010). Temporal context calibrates interval timing. Nat. Neurosci. 13, 1020-1026
23. Jin, D. Z., Fujii, N., and Graybiel, A. M. (2009). Neural representation of time in cortic-basal ganglia circuits. Proc. Natl. Acad. Sci. U.S.A. 106, 19156-19161
24. Karmarkar, U. R., and Buonomano, D. V. (2007). Timing in the absence of clocks: encoding time in neural network states. Neuron 53, 427-438.
25. Kilavik, B. E., Confais, J., Ponce-Alvarez, A., Diesmann, M., and Riehle, A. (2010). Evoked potentials of motor cortical LFPs reflect task timing and behavioral performance. J. Neurophysiol. 104, 2338-2351.
26. Lebedev, M. A., and Nicolelis, M. A. L. (2006). Brain-machine interfaces: past, present and future. Trends Neurosci. 29, 536-546.
27. Lebedev, M. A., O’Doherty, J. E., and Nicolelis, M. A. L. (2008). Decoding of temporal intervals from cortical ensemble activity. J. Neurophysiol. 99, 166-186
28. Leon, M. I., and Shadlen, M. N. (2003). Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38, 317-327.
29. MacEvoy, S. P., and Epstein, R. A. (2009). Decoding the representation of multiple simultaneous objects in human occipitotemporal cortex. Curr. Biol. 19, 943-947.
30. MacKay, D. J. C. (2003). Information Theory, Inference and Learning Algorithms. Cambridge: Cambridge University Press.
31. Matell, M. S., and Meck, W. H. (2004). Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. Brain Res. Cogn. Brain Res. 21, 139-170.
32. Matell, M. S., Meck, W. H., and Nicolelis, M. A. L. (2003). Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons. Behav. Neurosci. 117, 760-773.
33. Mauk, M. D., and Buonomano, D. V. (2004). The neural basis of temporal processing. Annu. Rev. Neurosci. 27, 307-340.
34. Meck, W. H., Penney, T. B., and Pouthas, V. (2008). Cortico-striatal representation of time in animals and humans. Curr. Opin. Neurobiol. 18, 145-152.
35. Miall, C. (1989). The storage of time intervals using oscillating neurons. Neural. Comput. 1, 359-371.
36. Miall, R. C. (1993). Neural networks and the representation of time. Psychol. Belg. 33, 255-269.
37. Mita, A., Mushiake, H., Shima, K., Matsuzaka, Y., and Tanji, J. (2009). Interval time coding by neurons in the presupplementary and supplementary motor areas. Nat. Neurosci. 12, 502-507.
38. Mongillo, G., Barak, O., and Tsodyks, M. (2008). Synaptic theory of working memory. Science 319, 1543-1546
39. Nicolelis, M. A. L., Baccala, L. A., Lin, R. C. S., and Chapin, J. K. (1995). Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 268, 1353-1358.
40. Niki, H., and Watanabe, M. (1979). Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Res. 171, 213-224.
41. Pillow, J. W., Ahmadian, Y., and Paninski, L. (2011). Model-based decoding, information estimation, and changepoint detection techniques for multineuron spike trains. Neural. Comput. 23, 1-45.
42. Pillow, J. W., Shlens, J., Paninski, L., Sher, A., Litke, A. M., Chichilnisky, E. J., and Simoncelli, E. P. (2008). Spatiotemporal correlations and visual signalling in a complete neuronal population. Nature 454, 995-999
43. Quiroga, R. Q., and Panzeri, S. (2009). Extracting information from neuronal populations: information theory and decoding approaches. Nat. Rev. Neurosci. 10, 173-185.
44. Rao, S. M., Mayer, A. R., and Harrington, D. L. (2001). The evolution of brain activation during temporal processing. Nat. Neurosci. 4, 317-323.
45. Renoult, L., Roux, S., and Riehle, A. (2006). Time is a rubberband: neuronal activity in monkey motor cortex in relation to time estimation. Eur. J. Neurosci. 23, 3098-3108.
46. Reutimann, J., Yakovlev, V., Fusi, S., and Senn, W. (2004). Climbing neuronal activity as an event-based cortical representation of time. J. Neurosci. 24, 3295-3303.
47. Rickert, J., Riehle, A., Aertsen, A., Rotter, S., and Nawrot, M. P. (2009). Dynamic encoding of movement direction in motor cortical neurons. J. Neurosci. 29, 13870-13882.
48. Rieke, F., Warland, D., de Ruyter van Steveninck, R., and Bialek, W. (1997). Spikes: Exploring the Neural Code. Cambridge: MIT Press.
49. Santhanam, G., Ryu, S. I., Yu, B. M., Afshar, A., and Shenoy, K. V. (2006). A high-performance brain computer interface. Nature 442, 195-198.
50. Serruya, M. D., Hatsopoulos, N. G., Paninski, L., Fellows, M. R., and Donoghue, J. P. (2002). Instant neural control of a movement signal. Nature 416, 141-142.
51. Shimokawa, T., and Shinomoto, S. (2006). Inhibitory neurons can facilitate rhythmic activity in a neural network. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 73, 66221.
52. Shinomoto, S., Kim, H., Shimokawa, T., Matsuno, N., Funahashi, S., Shima, K., Fujita, I., Tamura, H., Doi, T., Kawano, K., Inaba, N., Fukushima, K., Kurkin, S., Kurata, K., Taira, M., Tsutsui, K.-I., Komatsu, H., Ogawa, T., Koida, K., Tanji, J., and Toyama, K. (2009). Relating neuronal firing patterns to functional differentiation of cerebral cortex. PLoS Comput. Biol. 5, e1000433. doi: 10.1371/journal.pcbi.1000433
53. Shinomoto, S., Shima, K., and Tanji, J. (2003). Differences in spiking pat-terns among cortical neurons. Neural. Comput. 15, 2823-2842.
54. Szátmary, B., and Izhikevich, E. M. (2009). Spike-timing theory of working memory. PLoS Comput. Biol. 6, e1000879. doi: 10.1371/journal.pcbi.1000879
55. Yu, B. M., Cunningham, J. P., Santhanam, G., Ryu, S. I., Shenoy, K. V., and Sahani, M. (2009). Gaussian-process factor analysis for low-dimensional singletrial analysis of neural population activity. J. Neurophysiol. 102, 614-635.