Repetition priming effects dissociate between miniature eye movements and induced gamma-band responses in the human electroencephalogram

European Journal of Neuroscience

Volumn 38, Issue 3, 2013, Pages 2425-2433

  Hassler, Uwe ^a   Friese, Uwe ^b   Martens, Ulla ^a   Trujillo Barreto, Nelson ^c   Gruber, Thomas ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c CUBAN NEUROSCIENCE CENTER   (Cuba)

Author keywords

Gamma band activity; Miniature saccades; Spike potential; Variable resolution electromagnetic tomography

Indexed keywords

AGED; ARTICLE; ARTIFACT; BRAIN FUNCTION; CONTROLLED STUDY; ELECTRODE; ELECTROENCEPHALOGRAPH; EYE MOVEMENT; EYE TRACKING; FEMALE; FUNCTIONAL DISSOCIATION; GAMMA RHYTHM; HUMAN; HUMAN EXPERIMENT; MAGNETOENCEPHALOGRAPHY; MALE; NEUROIMAGING; NORMAL HUMAN; OCCIPITAL CORTEX; PRIORITY JOURNAL; REACTION TIME; REPETITION PRIMING; RIGHT HANDEDNESS; SACCADIC EYE MOVEMENT; STIMULUS RESPONSE; TEMPORAL CORTEX; VISION; WAVEFORM;

EID: 84881312895     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12244     Document Type: Article

References (46)

1. Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. Ser. B, 57, 289-300.
2. Benjamini, Y. & Yekutieli, D. (2001) The control of the false dicovery rate in multiple testing under depency. Ann. Stat., 29, 1165-1188.
3. Bertrand, O. & Pantev, C. (1994). Stimulus frequency dependence of transient oscillatory evoked response (40 Hz) studied by electric and magnetic recordings in humans. In Pantev, C., Elbert, T. & Lütkenhöner, B. (Eds), Oscilatory Event-Related Brain Dynamics. Plenum Press, New York, pp. 231-242.
4. Binder, J.R., Desai, R.H., Graves, W.W. & Conant, L.L. (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex, 19, 2767-2796.
5. Bisley, J.W. (2011) The neural basis of visual attention. J. Physiol., 589, 49-57.
6. Bosch-Bayard, J., Valdes-Sosa, P., Virues-Alba, T., Aubert-Vazquez, E., John, E.R., Harmony, T., Riera-Diaz, J. & Trujillo-Baretto, N. (2001) 3D statistical parametric mapping of EEG source spectra by means of Variable Resolution Electromagnetic Tomography (VARETA). Clin. Electroencephal., 32, 47-61.
7. Busch, N.A., Herrmann, C.S., Mueller, M.M., Lenz, D. & Gruber, T. (2006) A cross-laboratory study of event-related gamma activity in a standard object recognition paradigm. NeuroImage, 33, 1169-1177.
8. Carl, C., Açik, A., König, P., Engel, A.K. & Hipp, J.F. (2012) The saccadic spike artifact in MEG. NeuroImage, 59, 1657-1667.
9. Delorme, A. & Makeig, S. (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Meth., 134, 9-21.
10. Dimigen, O., Valsecchi, M., Sommer, W. & Kliegl, R. (2009) Human microsaccade-related visual brain responses. J. Neurosci., 29, 12321-12331.
11. Engbert, R. & Kliegl, R. (2003) Microsaccades uncover the orientation of covert attention. Vision Res., 43, 1035-1045.
12. Engbert, R. & Mergenthaler, K. (2006) Microsaccades are triggered by low retinal image slip. Proc. Natl. Acad. Sci. USA, 103, 7192-7197.
13. Engbert, R., Mergenthaler, K., Sinn, P. & Pikovsky, A. (2011) An integrated model of fixational eye movements and microsaccades. Proc. Natl. Acad. Sci. USA, 108, E765-E770.
14. Fiebach, C.J., Gruber, T. & Supp, G.G. (2005) Neuronal mechanisms of repetition priming in occipitotemporal cortex: spatiotemporal evidence from functional magnetic resonance imaging and electroencephalography. J. Neurosci., 25, 3414-3422.
15. Friese, U., Rahm, B., Hassler, U., Kaiser, J. & Gruber, T. (2012a) Repetition suppression and effects of familiarity on BOLD signal and gammaband activity. NeuroReport, 23, 757-761.
16. Friese, U., Supp, G.G., Hipp, J.F., Engel, A.K. & Gruber, T. (2012b) Oscillatory MEG gamma band activity dissociates perceptual and conceptual aspects of visual object processing: a combined repetition/conceptual priming study. NeuroImage, 59, 861-871.
17. Grill-Spector, K. (2003) The neural basis of object perception. Curr. Opin. Neurobiol., 13, 159-166.
18. Grill-Spector, K., Henson, R. & Martin, A. (2006) Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn. Sci., 10, 14-23.
19. Gruber, T. & Mueller, M.M. (2005) Oscillatory brain activity dissociates between associative stimulus content in a repetition priming task in the human EEG. Cereb. Cortex, 15, 109-116.
20. Gruber, T., Trujillo-Barreto, N.J., Giabbiconi, C.-M., Valdés-Sosa, P.A. & Mueller, M.M. (2006) Brain electrical tomography (BET) analysis of induced gamma band responses during a simple object recognition task. NeuroImage, 29, 888-900.
21. Gruber, T., Maess, B., Trujillo-Barreto, N.J. & Mueller, M.M. (2008) Sources of synchronized induced Gamma-Band responses during a simple object recognition task: a replication study in human MEG. Brain Res., 1196, 74-84.
22. Hafed, Z.M. (2011) Mechanisms for generating and compensating for the smallest possible saccades. Eur. J. Neurosci., 33, 2101-2113.
23. Hassler, U., Trujillo-Barreto, N. & Gruber, T. (2011) Induced gamma band responses in human EEG after the control of miniature saccadic artifacts. NeuroImage, 57, 1411-1421.
24. Hemera Technologies. (1997) Photo Objects, vol. 1. Hemera Technologies, Catineau, Canada.
25. Henson, R.N. (2003) Neuroimaging studies of priming. Prog. Neurobiol., 70, 53-81.
26. Henson, R.N., Shallice, T. & Dolan, R. (2000) Neuroimaging evidence for dissociable forms of repetition priming. Science, 287, 1269-1272.
27. Junghöfer, M., Elbert, T., Tucker, D.M. & Rockstroh, B. (2000) Statistical control of artifacts in dense array EEG/MEG studies. Psychophysiology, 37, 523-532.
28. Kaspar, K., Hassler, U., Martens, U., Trujillo-Barreto, N. & Gruber, T. (2010) Steady-state visually evoked potential correlates of object recognition. Brain Res., 1343, 112-121.
29. Keren, A.S., Yuval-Greenberg, S. & Deouell, L.Y. (2010) Saccadic spike potentials in gamma-band EEG: characterization, detection and suppression. NeuroImage, 49, 2248-2263.
30. Makin, A.D.J., Ackerley, R., Wild, K., Poliakoff, E., Gowen, E. & El-Deredy, W. (2011) Coherent illusory contours reduce microsaccade frequency. Neuropsychologia, 49, 2798-2801.
31. Martens, U. & Gruber, T. (2012) Sharpening and formation: two distinct neuronal mechanisms of repetition priming. Eur. J. Neurosci., 36, 2989-2995.
32. McDonald, C.R., Thesen, T., Carlson, C., Blumberg, M., Girard, H.M., Trongnetrpunya, A., Sherfey, J.S., Devinsky, O., Kuzniecky, R., Dolye, W.K., Cash, S.S., Leonard, M.K., Hagler, D.J., Dale, A.M. & Halgren, E. (2010) Multimodal imaging of repetition priming: using fMRI, MEG, and intracranial EEG to reveal spatiotemporal profiles of word processing. NeuroImage, 53, 707-717.
33. Robertson, L.C. (2003) Binding, spatial attention and perceptual awareness. Nat. Rev. Neurosci., 4, 93-102.
34. Schacter, D.L. & Buckner, R.L. (1998) Priming and the brain. Neuron, 20, 185-195.
35. Schacter, D.L., Wig, G.S. & Stevens, W.D. (2007) Reductions in cortical activity during priming. Curr. Opin. Neurobiol., 17, 171-176.
36. Simons, J.S., Graham, K.S., Owen, A.M., Patterson, K. & Hodges, J.R. (2001) Perceptual and semantic components of memory for objects and faces: a pet study. J. Cognitive Neurosci., 13, 430-443.
37. Supp, G.G., Schlögl, A., Trujillo-Barreto, N., Müller, M.M. & Gruber, T. (2007) Directed cortical information flow during human object recognition: analyzing induced EEG gamma-band responses in brain's source space. PLoS ONE, 2, e684.
38. Tallon-Baudry, C. (2009) The roles of gamma-band oscillatory synchrony in human visual cognition. Front. Biosci., 14, 321-332.
39. Tallon-Baudry, C. & Bertrand, O. (1999) Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci., 3, 151-162.
40. Tanaka, K. (1997) Mechanisms of visual object recognition: monkey and human studies. Curr. Opin. Neurobiol., 7, 523-529.
41. Thoma, V. & Henson, R.N. (2011) Object representations in ventral and dorsal visual streams: fMRI repetition effects depend on attention and part-whole configuration. NeuroImage, 57, 513-525.
42. Visser, M., Jefferies, E. & Lambon Ralph, M.A. (2010) Semantic processing in the anterior temporal lobes: a meta-analysis of the functional neuroimaging literature. J. Cognitive Neurosci., 22, 1083-1094.
43. Wiggs, C.L. & Martin, A. (1998) Properties and mechanisms of perceptual priming. Curr. Opin. Neurobiol., 8, 227-233.
44. Worsley, K.J., Marrett, S., Neelin, P., Vandal, A.C., Friston, K.J. & Evans, A.C. (1996) A unified statistical approach for determining significant signals in images of cerebral activation. Hum. Brain Mapp., 4, 58-73.
45. Yuval-Greenberg, S., Tomer, O., Keren, A.S., Nelken, I. & Deouell, L.Y. (2008) Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron, 58, 429-441.
46. Zuber, B., Stark, L. & Cook, G. (1965) Microsaccades and the velocity-amplitude relationship for saccadic eye movements. Science, 150, 1459-1460.