Repeated stimuli elicit diminished high-gamma electrocorticographic responses

NeuroImage

Volumn 85, Issue , 2014, Pages 844-852

  Rodriguez Merzagora, Anna ^a   Coffey, Thomas J ^a   Sperling, Michael R ^b   Sharan, Ashwini ^b   Litt, Brian ^c   Baltuch, Gordon ^c   Jacobs, Joshua ^a  

^a DREXEL UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Electrocorticography; Gamma band; Repetition suppression

Indexed keywords

ARTICLE; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTROCORTICOGRAPHY; EVENT RELATED POTENTIAL; GAMMA RHYTHM; HUMAN; LATENT PERIOD; MENTAL TASK; NERVOUS SYSTEM FUNCTION; PRIORITY JOURNAL; REPETITION SUPPRESSION; RESPONSE TIME; TASK PERFORMANCE; WORKING MEMORY;

ELECTROCORTICOGRAPHY; GAMMA BAND; REPETITION SUPPRESSION;

BRAIN WAVES; ELECTROENCEPHALOGRAPHY; HUMANS; MEMORY, SHORT-TERM; OCCIPITAL LOBE; PHOTIC STIMULATION; REPETITION PRIMING; TEMPORAL LOBE;

EID: 84889672748     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2013.07.006     Document Type: Article

References (65)

1. Anderson B., Mruczek R., Kawasaki K., Sheinberg D. Effects of familiarity on neural activity in monkey inferior temporal lobe. Cereb. Cortex 2008, 18(11):2540-2552.
2. Azizian A., Polich J. Evidence for attentional gradient in the serial position memory curve from event-related potentials. J. Cogn. Neurosci. 2007, 19(12):2071-2081.
3. Blakely T., Miller K., Rao R., Holmes M., Ojemann J. Localization and classification of phonemes using high spatial resolution electrocorticography (ecog) grids. Engineering in Medicine and Biology Society, 2008. EMBS 2008. 30th Annual International Conference of the IEEE 2008, 4964-4967.
4. Bruns A. Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches?. J. Neurosci. Methods 2004, 137:321-332.
5. Buckner R.L., Koutstaal W., Schacter D.L., Wagner A.D., Rosen B.R. Functional-anatomic study of episodic retrieval using fMRI. I. Retrieval effort versus retrieval success. NeuroImage 1998, 7(3):151-162. (Apr). 10.1006/nimg.1998.0327.
6. Conrad N., Giabbiconi C.-M., Muller M.M., Gruber T. Neuronal correlates of repetition priming of frequently presented objects: insights from induced gamma band responses. Neurosci. Lett. 2007, 429(2-3):126-130. (Dec). 10.1016/j.neulet.2007.09.065.
7. Crone N.E., Miglioretti D.L., Gordon B., Lesser R.P. Functional mapping of human sen- sorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 1998, 121(12):2301.
8. Dale A.M., Liu A.K., Fischl B.R., Buckner R.L., Belliveau J.W., Lewine J.D., Halgren E. Dynamic statistical parametric mapping: combining fMRI and MEG for high-resolution imaging of cortical activity. Neuron 2000, 26(1):55-67. (Apr).
9. De Baene W., Vogels R. Effects of adaptation on the stimulus selectivity of macaque inferior temporal spiking activity and local field potentials. Cereb. Cortex 2010, 20(9):2145-2165. (Sep). 10.1093/cercor/bhp277.
10. Ekstrom A. How and when the fMRI bold signal relates to underlying neural activity: the danger in dissociation. Brain Res. Rev. 2010, 62(2):233-244.
11. Engel A.K., Moll C.K.E., Fried I., Ojemann G.A. Invasive recordings from the human brain-clinical insights and beyond. Nat. Rev. Neurosci. 2005, 6:35-47.
12. Epstein R., Parker W., Feiler A. Two kinds of fMRI repetition suppression? Evidence for dissociable neural mechanisms. J. Neurophysiol. 2008, 99(6):2877.
13. Fell J., Dietl T., Grunwald T., Kurthen M., Klaver P., Truatner P., Fernandez G. Neural bases of cognitive ERPs: more than phase reset. J. Cogn. Neurosci. 2004, 16:1595-1604.
14. Freeman W. Hilbert transform for brain waves. Scholarpedia 2007, 2(1):1338.
15. Friese U., Rahm B., Hassler U., Kaiser J., Gruber T. Repetition suppression and effects of familiarity on blood oxygenation level dependent signal and gamma-band activity. Neuroreport 2012, 23(13):757-761. (Sep). 10.1097/WNR.0b013e328356b173.
16. Gilbert J., Gotts S., Carver F., Martin A. Object repetition leads to local increases in the temporal coordination of neural responses. Front. Hum. Neurosci. 2010, 4.
17. Gonsalves B.D., Kahn I., Curran T., Norman K.A., Wagner A.D. Memory strength and repetition suppression: multimodal imaging of medial temporal cortical contributions to recognition. Neuron 2005, 47(5):751-761. (Sep). 10.1016/j.neuron.2005.07.013.
18. Gotts S., Chow C., Martin A. Repetition priming and repetition suppression: a case for enhanced efficiency through neural synchronization. Cogn. Neurosci. 2012, 3(3-4):227-237.
19. Grill-Spector K., Malach R. fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychol. (Amst) 2001, 107(1-3):293-321. (Apr).
20. Grill-Spector K., Sayres R., Ress D. High-resolution imaging reveals highly selective nonface clusters in the fusiform face area. Nat. Neurosci. 2006, 9(9):1177.
21. Gruber T., Matthias M. Oscillatory brain activity dissociates between associative stimulus content in a repetition priming task in the human EEG. Cereb. Cortex 2005, 15:109-116.
22. Gruber T., Giabbiconi C.-M., Trujillo-Barreto N.J., Muller M.M. Repetition suppression of induced gamma band responses is eliminated by task switching. Eur. J. Neurosci. 2006, 24(9):2654-2660. (Nov). 10.1111/j.1460-9568.2006.05130.x.
23. Hanslmayr S., Klimesch W., Sauseng P., Gruber W., Doppelmayr M., Freunberger R., Birbaumer N. Alpha phase reset contributes to the generation of erps. Cereb. Cortex 2007, 17(1):1-8.
24. Harris A., Aguirre G.K. Neural tuning for face wholes and part in human fusiform gyrus revealed by fMRI adaptation. J. Neurophysiol. 2010, 104(1):336-345.
25. Henson R., Rugg M.D. Neural response suppression, haemodynamic repetition effects, and behavioural priming. Neuropsychologia 2003, 41(3):263-270.
26. Henson R., Rugg M.D., Shallice T., Dolan R.J. Confidence in recognition memory for words: dissociating right prefrontal roles in episodic retrieval. J. Cogn. Neurosci. 2000, 12(6):913-923.
27. Henson R., Shallice T., Dolan R. Neuroimaging evidence for dissociable forms of repetition priming. Science 2000, 287(5456):1269.
28. Henson R., Rylands A., Ross E., Vuilleumeir P., Rugg M.D. The effect of repetition lag on electrophysiological and haemodynamic correlates of visual object priming. NeuroImage 2004, 21(4):1674-1689. (Apr). 10.1016/j.neuroimage.2003.12.020.
29. Hermes D., Siero J., Aarnoutse E., Leijten F., Petridou N., Ramsey N. Dissociation between neuronal activity in sensorimotor cortex and hand movement revealed as a function of movement rate. J. Neurosci. 2012, 32(28):9736-9744.
30. Jacobs J., Kahana M.J. Neural representations of individual stimuli in humans revealed by gamma-band ECoG activity. J. Neurosci. 2009, 29(33):10203-10214.
31. Jacobs J., Kahana M.J. Direct brain recordings fuel advances in cognitive electrophysiology. Trends Cogn. Sci. 2010, 14(4):162-171.
32. Jacobs J., Hwang G., Curran T., Kahana M.J. EEG oscillations and recognition memory: Theta correlates of memory retrieval and decision making. NeuroImage 2006, 15(2):978-987.
33. James T.W., Gauthier I. Repetition-induced changes in bold response reflect accumulation of neural activity. Hum. Brain Mapp. 2006, 27(1):37-46. (Jan). 10.1002/hbm.20165.
34. Kaliukhovich D.A., Vogels R. Stimulus repetition probability does not affect repetition suppression in macaque inferior temporal cortex. Cereb. Cortex 2011, 21(7):1547-1558. (Jul). 10.1093/cercor/bhq207.
35. Larsson J., Smith A.T. fMRI repetition suppression: neuronal adaptation or stimulus expectation?. Cereb. Cortex 2012, 22(3):567-576. (Mar). 10.1093/cercor/bhr119.
36. Logothetis N., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
37. Maccotta L., Buckner R.L. Evidence for neural effects of repetition that directly correlate with behavioral priming. J. Cogn. Neurosci. 2004, 16(9):1625-1632. (Nov). 10.1162/0898929042568451.
38. Malach R. Targeting the functional properties of cortical neurons using fMR-adaptation. NeuroImage 2012, 62(2):1163-1169. (Aug). 10.1016/j.neuroimage.2012.01.002.
39. Manning J.R., Jacobs J., Fried I., Kahana M.J. Broadband shifts in LFP power spectra are correlated with single-neuron spiking in humans. J. Neurosci. 2009, 29(43):13613-13620.
40. McDonald C.R., Thesen T., Carlson C., Blumberg M., Girard H.M., Trongnetrpunya A., Halgren E. Multimodal imaging of repetition priming: using fMRI, MEG, and intracranial EEG to reveal spatiotemporal profiles of word processing. NeuroImage 2010, 53(2):707-717. (Nov). 10.1016/j.neuroimage.2010.06.069.
41. Miller E.K., Desimone R. Parallel neuronal mechanisms for short-term memory. Science 1994, 263(5146):520-522. (Jan).
42. Miller K., Leuthardt E.C., Schalk G., Rao R.P.N., Anderson N.R., Moran D.W., Ojemann J.G. Spectral changes in cortical surface potentials during motor movement. J. Neurosci. 2007, 27:2424-2432.
43. Miller K., Zanos S., Fetz E.E., den Nijs M., Ojemann J. Decoupling the cortical power spectrum reveals real-time representation of individual finger movements in humans. J. Neurosci. 2009, 29(10):3132-3137.
44. Miller K., Hermes D., Honey C., Hebb A., Ramsey N., Knight R., Fetz E. Human motor cortical activity is selectively phase-entrained on underlying rhythms. PLoS Comput. Biol. 2012, 8(9):e1002655.
45. Noguchi Y., Inui K., Kakigi R. Temporal dynamics of neural adaptation effect in the human visual ventral stream. J. Neurosci. 2004, 24(28):6283-6290. (Jul). 10.1523/JNEUROSCI.0655-04.2004.
46. Pasley B.N., David S.V., Mesgarani N., Flinker A., Shamma S.A., Crone N.E., Chang E.F. Reconstructing speech from human auditory cortex. PLoS Biol. 2012, 10(1):e1001251.
47. Pei X., Barbour D., Leuthardt E., Schalk G. Decoding vowels and consonants in spoken and imagined words using electrocorticographic signals in humans. J. Neural Eng. 2011, 8(4):046028.
48. Puce A., Allison T., McCarthy G. Electrophysiological studies of human face perception. iii: effects of top-down processing on face-specific potentials. Cereb. Cortex 1999, 9(5):445-458.
49. Ray M.K., Mackay C.E., Harmer C.J., Crow T.J. Bilateral generic working memory circuit requires left-lateralized addition for verbal processing. Cereb. Cortex 2008, 18:1421-1428.
50. Sambeth A., Maes J.H.R., Quian Quiroga R., Coenen A.M.L. Effects of stimulus repetitions on the event-related potential of humans and rats. Int. J. Psychophysiol. 2004, 53(3):197-205. (Aug). 10.1016/j.ijpsycho.2004.04.004.
51. Sawamura H., Orban G., Vogels R. Selectivity of neuronal adaptation does not match response selectivity: a single-cell study of the fMRI adaptation paradigm. Neuron 2006, 49(2):307-318.
52. Sayres R., Grill-Spector K. Object-selective cortex exhibits performance-independent repetition suppression. J. Neurophysiol. 2006, 95(2):995-1007. (Feb). 10.1152/jn.00500.2005.
53. Sederberg P.B., Gauthier L.V., Terushkin V., Miller J.F., Barnathan J.A., Kahana M.J. Oscillatory correlates of the primacy effect in episodic memory. NeuroImage 2006, 32(3):1422-1431.
54. Serruya M.D., Sederberg P.B., Kahana M.J. Power shifts track serial position and modulate encoding in human episodic memory. Cereb. Cortex 2013, (in press).
55. Sobotka S., Ringo J.L. Mnemonic responses of single units recorded from monkey inferotemporal cortex, accessed via transcommissural versus direct pathways: a dissociation between unit activity and behavior. J. Neurosci. 1996, 16(13):4222-4230. (Jul).
56. Sternberg S. High-speed scanning in human memory. Science 1966, 153:652-654.
57. Swick D., Knight R. Event-related potentials differentiate the effects of aging on word and non-word repetition inexplicit and implicit memory tasks. J. Exp. Psychol. Learn. Mem. Cogn. 1997, 23(1):123.
58. Tootell R.B.H., Hadjikhani N.K., Vanduffel W., Liu A.K., Mendola J.D., Sereno M.I., Dale A.M. Functional analysis of primary visual cortex (v1) in humans. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(3):811-817. (Retrieved from http://www.pnas.org/content/95/3/811.abstract).
59. van Gerven M., Maris E., Sperling M., Sharan A., Litt B., Anderson C., Jacobs J. Multivariate encoding of letter representations from ECoG signals. NeuroImage 2013, 70:223-232. (April). 10.1016/j.neuroimage.2012.12.059.
60. Van Strien J.W., Verkoeijen P.P.J.L., Van der Meer N., Franken I.H.A. Electrophysiological correlates of word repetition spacing: ERP and induced band power old/new effects with massed and spaced repetitions. Int. J. Psychophysiol. 2007, 66(3):205-214. (Dec). 10.1016/j.ijpsycho.2007.07.003.
61. Vidyasagar R., Stancak A., Parkes L.M. A multimodal brain imaging study of repetition suppression in the human visual cortex. NeuroImage 2010, 49(2):1612-1621. (Jan). 10.1016/j.neuroimage.2009.10.020.
62. Weiner K., Grill-Spector K. Synchrony upon repetition: one or multiple neural mechanisms?. Cogn. Neurosci. 2012, 3(3-4):243-244.
63. Wiggs C.L., Martin A. Properties and mechanisms of perceptual priming. Curr. Opin. Neurobiol. 1998, 8(2):227-233. (Apr).
64. Yacoub E., Harel N., Ugurbil K. High-field fMRI unveils orientation columns in humans. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(30):10607-10612.
65. Yeung N., Bogacz R., Holroyd C.B., Cohen J.D. Detection of synchronized oscillations in the encephalogram: an evaluation of methods. Psychophysiology 2004, 41(6):822-832.