Dynamic causal modelling of eye movements during pursuit: Confirming precision-encoding in V1 using MEG

NeuroImage

Volumn 132, Issue , 2016, Pages 175-189

  Adams, Rick A ^a   Bauer, Markus ^a,b   Pinotsis, Dimitris ^a   Friston, Karl J ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Active inference; Dynamic causal modelling; Magnetoencephalography; Oculomotor control; Precision; Smooth pursuit; Visual occlusion

Indexed keywords

VOLTAGE GATED POTASSIUM CHANNEL;

ADULT; AMPLITUDE MODULATION; ARTICLE; ARTIFACT; BAYES THEOREM; CONNECTOME; CONTROLLED STUDY; CUNEUS; EYE MOVEMENT; FEMALE; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE PROCESSING; LEFT HEMISPHERE; MAGNETOENCEPHALOGRAPHY; MALE; MEASUREMENT PRECISION; NOISE; NORMAL HUMAN; PERCEPTION; POTASSIUM CURRENT; PREDICTION; PRIORITY JOURNAL; PROBABILITY; PROPRIOCEPTION; PYRAMIDAL NERVE CELL; RECEPTIVE FIELD; STRIATE CORTEX; SYSTEMATIC ERROR; VISCOSITY; VISUAL EVOKED POTENTIAL; VISUAL STIMULATION; ADOLESCENT; BIOLOGICAL MODEL; BRAIN MAPPING; MOVEMENT PERCEPTION; OCULOGRAPHY; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; PSYCHOMOTOR PERFORMANCE; SIGNAL PROCESSING; SMOOTH PURSUIT EYE MOVEMENT; SYSTEM ANALYSIS; VISUAL CORTEX; YOUNG ADULT;

ADOLESCENT; ADULT; BAYES THEOREM; BRAIN MAPPING; EYE MOVEMENT MEASUREMENTS; FEMALE; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; MODELS, NEUROLOGICAL; MOTION PERCEPTION; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; PURSUIT, SMOOTH; SIGNAL PROCESSING, COMPUTER-ASSISTED; SYSTEMS ANALYSIS; VISUAL CORTEX; YOUNG ADULT;

EID: 84962356458     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2016.02.055     Document Type: Article

References (64)

1. Adams, R.A., Perrinet, L.U., Friston, K., Smooth pursuit and visual occlusion: active inference and oculomotor control in schizophrenia. PLoS One, 7, 2012, e47502, 10.1371/journal.pone.0047502.
2. Adams, R.A., Shipp, S., Friston, K.J., Predictions not commands: active inference in the motor system. Brain Struct. Funct. 218 (2013), 611–643, 10.1007/s00429-012-0475-5.
3. Adams, R.A., Stephan, K.E., Brown, H.R., Frith, C.D., Friston, K.J., The computational anatomy of psychosis. Front. Psychiatry, 4, 2013, 47, 10.3389/fpsyt.2013.00047.
4. Adams, R.A., Aponte, E., Marshall, L., Friston, K.J., Active inference and oculomotor pursuit: The dynamic causal modelling of eye movements. J. Neurosci. Methods 242C (2015), 1–14, 10.1016/j.jneumeth.2015.01.003.
5. Ballard, D.H., Hinton, G.E., Sejnowski, T.J., Parallel visual computation. Nature 306 (1983), 21–26.
6. Barnes, G.R., Asselman, P.T., The mechanism of prediction in human smooth pursuit eye movements. J. Physiol. 439 (1991), 439–461.
7. Bastos, A.M., Usrey, W.M., Adams, R.A., Mangun, G.R., Fries, P., Friston, K.J., Canonical Microcircuits for Predictive Coding. Neuron 76 (2012), 695–711, 10.1016/j.neuron.2012.10.038.
8. Bastos, A.M., Litvak, V., Moran, R., Bosman, C.A., Fries, P., Friston, K.J., A DCM study of spectral asymmetries in feedforward and feedback connections between visual areas V1 and V4 in the monkey. NeuroImage 108 (2015), 460–475, 10.1016/j.neuroimage.2014.12.081.
9. Bauer, M., Barnes, G., Kluge, C., Driver, J., Eye-tracking with MEG. Front. Neurosci. Conference Abstract: Biomag. Presented at the 17th International Conference on Biomagnetism, Dubrovnik, Croatia, 2010, 10.3389/conf.fnins.2010.06.00438.
10. Bialek, W., Nemenman, I., Tishby, N., Predictability, complexity, and learning. Neural Comput. 13 (2001), 2409–2463, 10.1162/089976601753195969.
11. Bogadhi, A.R., Montagnini, A., Masson, G.S., Dynamic interaction between retinal and extraretinal signals in motion integration for smooth pursuit. J. Vis., 13, 2013, 5, 10.1167/13.13.5.
12. Boly, M., Garrido, M.I., Gosseries, O., Bruno, M.-A., Boveroux, P., Schnakers, C., Massimini, M., Litvak, V., Laureys, S., Friston, K., Preserved Feedforward But Impaired Top-Down Processes in the Vegetative State. Science 332 (2011), 858–862, 10.1126/science.1202043.
13. Brainard, D.H., Longère, P., Delahunt, P.B., Freeman, W.T., Kraft, J.M., Xiao, B., Bayesian model of human color constancy. J. Vis. 6 (2006), 1267–1281, 10.1167/6.11.10.
14. Brown, H.R., Friston, K.J., Dynamic causal modelling of precision and synaptic gain in visual perception - an EEG study. NeuroImage 63 (2012), 223–231, 10.1016/j.neuroimage.2012.06.044.
15. Brown, H.R., Friston, K.J., The functional anatomy of attention: a DCM study. Front. Hum. Neurosci., 7, 2013, 784, 10.3389/fnhum.2013.00784.
16. Cornelissen, F.W., Peters, E.M., Palmer, J., The Eyelink Toolbox: eye tracking with MATLAB and the Psychophysics Toolbox. Behav. Res. Methods Instrum. Comput. J. Psychon. Soc. Inc. 34 (2002), 613–617.
17. Daunizeau, J., den Ouden, H.E.M., Pessiglione, M., Kiebel, S.J., Stephan, K.E., Friston, K.J., Observing the observer (I): meta-bayesian models of learning and decision-making. PLoS One, 5, 2010, e15554, 10.1371/journal.pone.0015554.
18. David, O., Harrison, L., Friston, K.J., Modelling event-related responses in the brain. NeuroImage 25 (2005), 756–770, 10.1016/j.neuroimage.2004.12.030.
19. David, O., Kiebel, S.J., Harrison, L.M., Mattout, J., Kilner, J.M., Friston, K.J., Dynamic causal modeling of evoked responses in EEG and MEG. NeuroImage 30 (2006), 1255–1272, 10.1016/j.neuroimage.2005.10.045.
20. Dayan, P., Hinton, G.E., Neal, R.M., Zemel, R.S., The Helmholtz machine. Neural Comput. 7 (1995), 889–904.
21. Deserno, L., Sterzer, P., Wüstenberg, T., Heinz, A., Schlagenhauf, F., Reduced prefrontal-parietal effective connectivity and working memory deficits in schizophrenia. J. Neurosci. Off. J. Soc. Neurosci. 32 (2012), 12–20, 10.1523/JNEUROSCI.3405-11.2012.
22. Dima, D., Dietrich, D.E., Dillo, W., Emrich, H.M., Impaired top-down processes in schizophrenia: a DCM study of ERPs. NeuroImage 52 (2010), 824–832, 10.1016/j.neuroimage.2009.12.086.
23. Dunkley, B.T., Freeman, T.C.A., Muthukumaraswamy, S.D., Singh, K.D., Cortical oscillatory changes in human middle temporal cortex underlying smooth pursuit eye movements. Hum. Brain Mapp., 2011, 10.1002/hbm.21478.
24. Eickhoff, S.B., Stephan, K.E., Mohlberg, H., Grefkes, C., Fink, G.R., Amunts, K., Zilles, K., A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25 (2005), 1325–1335, 10.1016/j.neuroimage.2004.12.034.
25. Feldman, H., Friston, K.J., Attention, uncertainty, and free-energy. Front. Hum. Neurosci., 4, 2010, 215, 10.3389/fnhum.2010.00215.
26. Friston, K.J., A theory of cortical responses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360 (2005), 815–836, 10.1098/rstb.2005.1622.
27. Friston, K.J., Harrison, L., Penny, W., Dynamic causal modelling. NeuroImage 19 (2003), 1273–1302, 10.1016/S1053-8119(03)00202-7.
28. Friston, K.J., Kilner, J., Harrison, L., A free energy principle for the brain. J. Physiol. Paris 100 (2006), 70–87, 10.1016/j.jphysparis.2006.10.001.
29. Friston, K.J., Mattout, J., Trujillo-Barreto, N., Ashburner, J., Penny, W., Variational free energy and the Laplace approximation. NeuroImage 34 (2007), 220–234, 10.1016/j.neuroimage.2006.08.035.
30. Friston, K.J., Harrison, L., Daunizeau, J., Kiebel, S., Phillips, C., Trujillo-Barreto, N., Henson, R., Flandin, G., Mattout, J., Multiple sparse priors for the M/EEG inverse problem. NeuroImage 39 (2008), 1104–1120, 10.1016/j.neuroimage.2007.09.048.
31. Friston, K.J., Daunizeau, J., Kilner, J., Kiebel, S.J., Action and behavior: a free-energy formulation. Biol. Cybern. 102 (2010), 227–260, 10.1007/s00422-010-0364-z.
32. Friston, K., Zeidman, P., Litvak, V., Empirical Bayes for DCM: A Group Inversion Scheme. Front. Syst. Neurosci., 9, 2015, 164, 10.3389/fnsys.2015.00164.
33. Garrido, M.I., Kilner, J.M., Kiebel, S.J., Friston, K.J., Evoked brain responses are generated by feedback loops. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 20961–20966, 10.1073/pnas.0706274105.
34. Gregory, R.L., Perceptions as hypotheses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 290 (1980), 181–197.
35. Grossberg, S., Roberts, K., Aguilar, M., Bullock, D., A neural model of multimodal adaptive saccadic eye movement control by superior colliculus. J. Neurosci. Off. J. Soc. Neurosci. 17 (1997), 9706–9725.
36. Haeusler, S., Maass, W., A statistical analysis of information-processing properties of lamina-specific cortical microcircuit models. Cereb. Cortex 1991:17 (2007), 149–162, 10.1093/cercor/bhj132.
37. Hirano, Y., Oribe, N., Kanba, S., Onitsuka, T., Nestor, P.G., Spencer, K.M., Spontaneous Gamma Activity in Schizophrenia. JAMA Psychiatry 72 (2015), 813–821, 10.1001/jamapsychiatry.2014.2642.
38. Jansen, B.H., Rit, V.G., Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns. Biol. Cybern. 73 (1995), 357–366.
39. Kiebel, S.J., David, O., Friston, K.J., Dynamic causal modelling of evoked responses in EEG/MEG with lead field parameterization. NeuroImage 30 (2006), 1273–1284, 10.1016/j.neuroimage.2005.12.055.
40. Kiebel, S.J., Garrido, M.I., Moran, R., Chen, C.-C., Friston, K.J., Dynamic causal modeling for EEG and MEG. Hum. Brain Mapp. 30 (2009), 1866–1876, 10.1002/hbm.20775.
41. Knill, D.C., Pouget, A., The Bayesian brain: the role of uncertainty in neural coding and computation. Trends Neurosci. 27 (2004), 712–719, 10.1016/j.tins.2004.10.007.
42. Krauzlis, R.J., Lisberger, S.G., A Control Systems Model of Smooth Pursuit Eye Movements with Realistic Emergent Properties. Neural Comput. 1 (1989), 116–122, 10.1162/neco.1989.1.1.116.
43. Lencer, R., Trillenberg, P., Neurophysiology and neuroanatomy of smooth pursuit in humans. Brain Cogn. 68 (2008), 219–228, 10.1016/j.bandc.2008.08.013.
44. Litvak, V., Mattout, J., Kiebel, S., Phillips, C., Henson, R., Kilner, J., Barnes, G., Oostenveld, R., Daunizeau, J., Flandin, G., Penny, W., Friston, K., EEG and MEG data analysis in SPM8. Comput. Intell. Neurosci., 2011, 2011, 852961, 10.1155/2011/852961.
45. Maloney, L.T., Zhang, H., Decision-theoretic models of visual perception and action. Vis. Res. 50 (2010), 2362–2374, 10.1016/j.visres.2010.09.031.
46. Mattout, J., Henson, R.N., Friston, K.J., Canonical source reconstruction for MEG. Comput. Intell. Neurosci., 67613, 2007, 10.1155/2007/67613.
47. Moran, R.J., Campo, P., Symmonds, M., Stephan, K.E., Dolan, R.J., Friston, K.J., Free energy, precision and learning: the role of cholinergic neuromodulation. J. Neurosci. Off. J. Soc. Neurosci. 33 (2013), 8227–8236, 10.1523/JNEUROSCI.4255-12.2013.
48. Mukherjee, T., Battifarano, M., Simoncini, C., Osborne, L.C., Shared sensory estimates for human motion perception and pursuit eye movements. J. Neurosci. Off. J. Soc. Neurosci. 35 (2015), 8515–8530, 10.1523/JNEUROSCI.4320-14.2015.
49. Mumford, D., On the computational architecture of the neocortex. II. The role of cortico-cortical loops. Biol. Cybern. 66 (1992), 241–251.
50. Olshausen, B.A., Field, D.J., Emergence of simple-cell receptive field properties by learning a sparse code for natural images. Nature 381 (1996), 607–609, 10.1038/381607a0.
51. Oostenveld, R., Fries, P., Maris, E., Schoffelen, J.-M., FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci., 2011, 2011, 156869, 10.1155/2011/156869.
52. Orban de Xivry, J.-J., Bennett, S.J., Lefèvre, P., Barnes, G.R., Evidence for Synergy Between Saccades and Smooth Pursuit During Transient Target Disappearance. J. Neurophysiol. 95 (2006), 418–427, 10.1152/jn.00596.2005.
53. Orban de Xivry, J.-J., Coppe, S., Blohm, G., Lefèvre, P., Kalman filtering naturally accounts for visually guided and predictive smooth pursuit dynamics. J. Neurosci. Off. J. Soc. Neurosci. 33 (2013), 17301–17313, 10.1523/JNEUROSCI.2321-13.2013.
54. Osborne, L.C., Lisberger, S.G., Bialek, W., A sensory source for motor variation. Nature 437 (2005), 412–416, 10.1038/nature03961.
55. Perrinet, L.U., Adams, R.A., Friston, K.J., Active inference, eye movements and oculomotor delays. Biol. Cybern., 2014, 10.1007/s00422-014-0620-8.
56. Rao, R.P., Ballard, D.H., Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat. Neurosci. 2 (1999), 79–87, 10.1038/4580.
57. Robinson, D.A., Gordon, J.L., Gordon, S.E., A model of the smooth pursuit eye movement system. Biol. Cybern. 55 (1986), 43–57.
58. Shergill, S.S., Samson, G., Bays, P.M., Frith, C.D., Wolpert, D.M., Evidence for sensory prediction deficits in schizophrenia. Am. J. Psychiatry 162 (2005), 2384–2386, 10.1176/appi.ajp.162.12.2384.
59. Shibata, T., Tabata, H., Schaal, S., Kawato, M., A model of smooth pursuit in primates based on learning the target dynamics. Neural Netw. Off. J. Int. Neural Netw. Soc. 18 (2005), 213–224, 10.1016/j.neunet.2005.01.001.
60. Tavassoli, A., Ringach, D.L., Dynamics of smooth pursuit maintenance. J. Neurophysiol. 102 (2009), 110–118, 10.1152/jn.91320.2008.
61. Thomson, A.M., West, D.C., Wang, Y., Bannister, A.P., Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2–5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb. Cortex 1991:12 (2002), 936–953.
62. Uusitalo, M.A., Ilmoniemi, R.J., Signal-space projection method for separating MEG or EEG into components. Med. Biol. Eng. Comput. 35 (1997), 135–140.
63. Weiss, Y., Simoncelli, E.P., Adelson, E.H., Motion illusions as optimal percepts. Nat. Neurosci. 5 (2002), 598–604, 10.1038/nn858.
64. Yuille, A., Kersten, D., Vision as Bayesian inference: analysis by synthesis?. Trends Cogn. Sci. 10 (2006), 301–308, 10.1016/j.tics.2006.05.002.