Frequency of gamma oscillations in humans is modulated by velocity of visual motion

Journal of Neurophysiology

Volumn 114, Issue 1, 2015, Pages 244-255

  Orekhova, Elena V ^a   Butorina, Anna V ^a   Sysoeva, Olga V ^a   Prokofyev, Andrey O ^a   Nikolaeva, Anastasia Yu ^a   Stroganova, Tatiana A ^a  

^a MOSCOW STATE UNIVERSITY OF PSYCHOLOGY AND EDUCATION   (Russian Federation)

Author keywords

Electroencephalography; Frequency of gamma oscillations; Magnetoencephalography; Spatial suppression; Visual cortex

Indexed keywords

PARVALBUMIN;

ADOLESCENT; ARTICLE; CHILD; ELECTRIC POTENTIAL; ELECTROENCEPHALOGRAM; ELECTROOCULOGRAM; EXCITABILITY; FREQUENCY MODULATION; GAMMA OSCILLATION; GRATING; HUMAN; HUMAN EXPERIMENT; MALE; NONHUMAN; NORMAL HUMAN; OSCILLATION; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; REACTION TIME; VELOCITY; AGING; BRAIN; ELECTROENCEPHALOGRAPHY; GAMMA RHYTHM; GROWTH, DEVELOPMENT AND AGING; MAGNETOENCEPHALOGRAPHY; MOVEMENT PERCEPTION; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; PSYCHOPHYSICS; REGRESSION ANALYSIS;

ADOLESCENT; AGING; BRAIN; CHILD; ELECTROENCEPHALOGRAPHY; GAMMA RHYTHM; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; MOTION PERCEPTION; PHOTIC STIMULATION; PSYCHOPHYSICS; REGRESSION ANALYSIS;

EID: 84938886485     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00232.2015     Document Type: Article

References (84)

1. Anver H, Ward PD, Magony A, Vreugdenhil M. NMDA receptor hypofunction phase couples independent gamma-oscillations in the rat visual cortex. Neuropsychopharmacology 36: 519-528, 2011.
2. Atallah BV, Scanziani M. Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62: 566-577, 2009.
3. Benedek K, Janaky M, Braunitzer G, Rokszin A, Keri S, Benedek G. Parallel development of contour integration and visual contrast sensitivity at low spatial frequencies. Neurosci Lett 472: 175-178, 2010.
4. Betts LR, Sekuler AB, Bennett PJ. Spatial characteristics of center-surround antagonism in younger and older adults. J Vis 9: 25.1-25.15, 2009.
5. Betts LR, Taylor CP, Sekuler AB, Bennett PJ. Aging reduces centersurround antagonism in visual motion processing. Neuron 45: 361-366, 2005.
6. Brainard DH. The Psychophysics Toolbox. Spat Vis 10: 433-436, 1997.
7. Braunitzer G, Rokszin A, Kobor J, Nagy A, Sztriha L, Benedek G. Development of visual contour integration in children with migraine without aura. Cephalalgia 31: 1048-1056, 2011.
8. Brunet N, Vinck M, Bosman CA, Singer W, Fries P. Gamma or no gamma, that is the question. Trends Cogn Sci 18: 507-509, 2014.
9. Campbell AE, Sumner P, Singh KD, Muthukumaraswamy SD. Acute effects of alcohol on stimulus-induced gamma oscillations in human primary visual and motor cortices. Neuropsychopharmacol 39: 2104-2113, 2014.
10. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-667, 2009.
11. Carlen M, Meletis K, Siegle JH, Cardin JA, Futai K, Vierling-Claassen D, Ruhlmann C, Jones SR, Deisseroth K, Sheng M, Moore CI, Tsai LH. A critical role for NMDA receptors in parvalbumin interneurons for gamma rhythm induction and behavior. Mol Psychiatry 17: 537-548, 2012.
12. Carmignoto G, Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258: 1007-1011, 1992.
13. Cho RY, Walker CP, Polizzotto NR, Wozny TA, Fissell C, Chen CM, Lewis DA. Development of sensory gamma oscillations and cross-frequency coupling from childhood to early adulthood. Cereb Cortex 25: 1509-1518, 2015.
14. Cousijn H, Haegens S, Wallis G, Near J, Stokes MG, Harrison PJ, Nobre AC. Resting GABA and glutamate concentrations do not predict visual gamma frequency or amplitude. Proc Natl Acad Sci USA 111: 9301-9306, 2014.
15. Edden RA, Muthukumaraswamy SD, Freeman TC, Singh KD. Orientation discrimination performance is predicted by GABA concentration and gamma oscillation frequency in human primary visual cortex. J Neurosci 29: 15721-15726, 2009.
16. Ferando I, Mody I. In vitro gamma oscillations following partial and complete ablation of delta subunit-containing GABAA receptors from parvalbumin interneurons. Neuropharmacology 88: 91-98, 2015.
17. Foss-Feig JH, Tadin D, Schauder KB, Cascio CJ. A substantial and unexpected enhancement of motion perception in autism. J Neurosci 33: 8243-8249, 2013.
18. Fries P. A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9: 474-480, 2005.
19. Gaetz W, Roberts TP, Singh KD, Muthukumaraswamy SD. Functional and structural correlates of the aging brain: relating visual cortex (V1) gamma band responses to age-related structural change. Hum Brain Mapp 33: 2035-2046, 2012.
20. Gieselmann MA, Thiele A. Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1. Eur J Neurosci 28: 447-459, 2008.
21. Golomb JD, McDavitt JR, Ruf BM, Chen JI, Saricicek A, Maloney KH, Hu J, Chun MM, Bhagwagar Z. Enhanced visual motion perception in major depressive disorder. J Neurosci 29: 9072-9077, 2009.
22. Gonzalez-Burgos G, Lewis DA. NMDA receptor hypofunction, parvalbuminpositive neurons, and cortical gamma oscillations in schizophrenia. Schizophrenia Bull 38: 950-957, 2012.
23. González-Burgos I, Alejandre-Gómez M. Cerebellar granule cell and Bergmann glial cell maturation in the rat is disrupted by pre- and postnatal exposure to moderate levels of ethanol. Int J Dev Neurosci 23: 383-388, 2005.
24. Gray C, DiPrisco G. Stimulus-dependent neuronal oscillations and local synchronization in striate cortex of the alert cat. J Neurosci 17: 3239-3253, 1997.
25. Gulyas AI, Szabo GG, Ulbert I, Holderith N, Monyer H, Erdelyi F, Szabo G, Freund TF, Hajos N. Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J Neurosci 30: 15134-15145, 2010.
26. Hadjipapas A, Lowet E, Roberts M, Peter A, De Weerd P. Parametric variation of gamma frequency and power with luminance contrast: A comparative study of human MEG and monkey LFP and spike responses. Neuroimage 112: 327-340, 2015.
27. Hashimoto T, Nguyen QL, Rotaru D, Keenan T, Arion D, Beneyto M, Gonzalez-Burgos G, Lewis DA. Protracted developmental trajectories of GABAA receptor alpha1 and alpha2 subunit expression in primate prefrontal cortex. Biol Psychiatry 65: 1015-1023, 2009.
28. Hermes D, Miller KJ, Wandell BA, Winawer J. Stimulus dependence of gamma oscillations in human visual cortex. Cereb Cortex. First published May 22, 2014; doi:10.1093/cercor/bhu091.
29. Holland PW, Welsch RE. Robust regression using iteratively re-weighted leastsquares. Commun Stat Theory Methods 6: 813-827, 1977.
30. Hoogenboom N, Schoffelen JM, Oostenveld R, Parkes LM, Fries P. Localizing human visual gamma-band activity in frequency, time and space. Neuroimage 29: 764-773, 2006.
31. Hudspeth WJ, Pribram KH. Psychophysiological indices of cerebral maturation. Int J Psychophysiol 12: 19-29, 1992.
32. Hughes SW, Crunelli V. Just a phase they're going through: the complex interaction of intrinsic high-threshold bursting and gap junctions in the generation of thalamic alpha and theta rhythms. Int J Psychophysiol 64: 3-17, 2007.
33. Jia XX, Xing DJ, Kohn A. No consistent relationship between gamma power and peak frequency in macaque primary visual cortex. J Neurosci 33: 17-25, 2013.
34. Kang K, Shelley M, Henrie JA, Shapley R. LFP spectral peaks in V1 cortex: network resonance and cortico-cortical feedback. J Comput Neurosci 29: 495-507, 2010.
35. Kiorpes L, Bassin SA. Development of contour integration in macaque monkeys. Vis Neurosci 20: 567-575, 2003.
36. Kirli KK, Ermentrout GB, Cho RY. Computational study of NMDA conductance and cortical oscillations in schizophrenia. Front Comput Neurosci 8: 133, 2014.
37. Koelewijn L, Rich AN, Muthukumaraswamy SD, Singh KD. Spatial attention increases high-frequency gamma synchronisation in human medial visual cortex. Neuroimage 79: 295-303, 2013.
38. Lawrence YA, Kemper TL, Bauman ML, Blatt GJ. Parvalbumin-, calbindin-, and calretinin-immunoreactive hippocampal interneuron density in autism. Acta Neurol Scand 121: 99-108, 2010.
39. Le Magueresse C, Monyer H. GABAergic interneurons shape the functional maturation of the cortex. Neuron 77: 388-405, 2013.
40. Lewis DA. Inhibitory neurons in human cortical circuits: substrate for cognitive dysfunction in schizophrenia. Curr Opin Neurobiol 26: 22-26, 2014.
41. Lima B, Singer W, Chen NH, Neuenschwander S. Synchronization dynamics in response to plaid stimuli in monkey V1. Cereb Cortex 20: 1556-1573, 2010.
42. 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: 852961, 2011.
43. Lozano-Soldevilla D, ter Huurne N, Cools R, Jensen O. GABAergic modulation of visual gamma and alpha oscillations and its consequences for working memory performance. Curr Biol 24: 2878-2887, 2014.
44. Mann EO, Mody I. Control of hippocampal gamma oscillation frequency by tonic inhibition and excitation of interneurons. Nat Neurosci 13: 205-212, 2010.
45. Miller R. Cortico-Hippocampal Interplay and the Representation of Contexts in the Brain. Berlin and New York: Springer-Verlag, 1991.
46. Muthukumaraswamy SD, Myers JF, Wilson SJ, Nutt DJ, Hamandi K, Lingford-Hughes A, Singh KD. Elevating endogenous GABA levels with GAT-1 blockade modulates evoked but not induced responses in human visual cortex. Neuropsychopharmacol 38: 1105-1112, 2013.
47. Muthukumaraswamy SD, Singh KD. Visual gamma oscillations: the effects of stimulus type, visual field coverage and stimulus motion on MEG and EEG recordings. Neuroimage 69: 223-230, 2013.
48. Muthukumaraswamy SD, Singh KD, Swettenham JB, Jones DK. Visual gamma oscillations and evoked responses: variability, repeatability and structural MRI correlates. Neuroimage 49: 3349-3357, 2010.
49. Naue N, Strüber D, Fründ I, Schadow J, Lenz D, Rach S, Körner U, Herrmann CS. Gamma in motion: pattern reversal elicits stronger gammaband responses than motion. Neuroimage 55: 808-817, 2011.
50. Nunez PL. Toward a quantitative description of large-scale neocortical dynamic function and EEG. Behav Brain Sci 23: 371-398; discussion 399- 437, 2000.
51. Oke OO, Magony A, Anver H, Ward PD, Jiruska P, Jefferys JG, Vreugdenhil M. High-frequency gamma oscillations coexist with lowfrequency gamma oscillations in the rat visual cortex in vitro. Eur J Neurosci 31: 1435-1445, 2010.
52. Orekhova EV, Stroganova TA, Posikera IN, Elam M. EEG theta rhythm in infants and preschool children. Clin Neurophysiol 117: 1047-1062, 2006.
53. Paffen CL, van der Smagt MJ, te Pas SF, Verstraten FA. Center-surround inhibition and facilitation as a function of size and contrast at multiple levels of visual motion processing. J Vis 5: 571-578, 2005.
54. Palomares M, Englund JA, Ahlers S. Patterns and trajectories in Williams Syndrome: the case of visual orientation discrimination. Res Dev Disabil 32: 1021-1029, 2011.
55. Paoletti P, Bellone C, Zhou Q. NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci 14: 383-400, 2013.
56. Paus T, Collins DL, Evans AC, Leonard G, Pike B, Zijdenbos A. Maturation of white matter in the human brain: a review of magnetic resonance studies. Brain Res Bull 54: 255-266, 2001.
57. Perry G, Hamandi K, Brindley LM, Muthukumaraswamy SD, Singh KD. The properties of induced gamma oscillations in human visual cortex show individual variability in their dependence on stimulus size. Neuroimage 68: 83-92, 2013.
58. Pinto JG, Hornby KR, Jones DG, Murphy KM. Developmental changes in GABAergic mechanisms in human visual cortex across the lifespan. Front Cell Neurosci 4: 16, 2010.
59. Ray S, Maunsell JH. Differences in gamma frequencies across visual cortex restrict their possible use in computation. Neuron 67: 885-896, 2010.
60. Rice JK, Rorden C, Little JS, Parra LC. Subject position affects EEG magnitudes. Neuroimage 64: 476-484, 2013.
61. Roth MM, Helmchen F, Kampa BM. Distinct functional properties of primary and posteromedial visual area of mouse neocortex. J Neurosci 32: 9716-9726, 2012.
62. Saxena N, Muthukumaraswamy SD, Diukova A, Singh K, Hall J, Wise R. Enhanced stimulus-induced gamma activity in humans during propofolinduced sedation. PLoS One 8: e57685, 2013.
63. Schwarzkopf DS, Robertson DJ, Song C, Barnes GR, Rees G. The frequency of visually induced gamma-band oscillations depends on the size of early human visual cortex. J Neurosci 32: 1507-1512, 2012.
64. Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698- 702, 2009.
65. Stroganova TA, Orekhova EV, Posikera IN. EEG alpha rhythm in infants. Clin Neurophysiol 110: 997-1012, 1999.
66. Swettenham JB, Muthukumaraswamy SD, Singh KD. Spectral properties of induced and evoked gamma oscillations in human early visual cortex to moving and stationary stimuli. J Neurophysiol 102: 1241-1253, 2009.
67. Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM. Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011: 879716, 2011.
68. Tadin D, Kim J, Park S. Weakened center-surround interactions in visual motion processing in schizophrenia. Schizophrenia Bull 33: 545, 2007.
69. Tadin D, Lappin JS, Gilroy LA, Blake R. Perceptual consequences of centre-surround antagonism in visual motion processing. Nature 424: 312- 315, 2003.
70. Tadin D, Silvanto J, Pascual-Leone A, Battelli L. Improved motion perception and impaired spatial suppression following disruption of cortical area MT/V5. J Neurosci 31: 1279-1283, 2011.
71. Taulu S, Kajola M, Simola J. Suppression of interference and artifacts by the Signal Space Separation Method. Brain Topogr 16: 269-275, 2004.
72. Tesche CD, Uusitalo MA, Ilmoniemi RJ, Huotilainen M, Kajola M, Salonen O. Signal-space projections of MEG data characterize both distributed and well-localized neuronal sources. Electroencephalogr Clin Neurophysiol 95: 189-200, 1995.
73. Thomson DJ. Spectrum estimation and harmonic analysis. Proc IEEE 70: 1055-1096, 1982.
74. Uhlhaas PJ, Pipa G, Lima B, Melloni L, Neuenschwander S, Nikolic D, Singer W. Neural synchrony in cortical networks: history, concept and current status. Front Integr Neurosci 3: 17, 2009.
75. Uhlhaas PJ, Pipa G, Neuenschwander S, Wibral M, Singer W. A new look at gamma? High- (>60 Hz) γ-band activity in cortical networks: function, mechanisms and impairment. Prog Biophys Mol Biol 105: 14-28, 2011.
76. Uusitalo MA, Ilmoniemi RJ. Signal-space projection method for separating MEG or EEG into components. Med Biol Eng Comput 35: 135-140, 1997.
77. van Pelt S, Boomsma DI, Fries P. Magnetoencephalography in twins reveals a strong genetic determination of the peak frequency of visually induced γ-band synchronization. J Neurosci 32: 3388-3392, 2012.
78. van Pelt S, Fries P. Visual stimulus eccentricity affects human gamma peak frequency. Neuroimage 78: 439-447, 2013.
79. Volman V, Behrens MM, Sejnowski TJ. Downregulation of parvalbumin at cortical GABA synapses reduces network gamma oscillatory activity. J Neurosci 31: 18137-18148, 2011.
80. Wang HX, Gao WJ. Cell type-specific development of NMDA receptors in the interneurons of rat prefrontal cortex. Neuropsychopharmacol 34: 2028- 2040, 2009.
81. Wang HX, Gao WJ. Development of calcium-permeable AMPA receptors and their correlation with NMDA receptors in fast-spiking interneurons of rat prefrontal cortex. J Physiol 588: 2823-2838, 2010.
82. Yang Y, Zhang J, Liang Z, Li GX, Wang YC, Ma YY, Zhou YF, Leventhal AG. Aging affects the neural representation of speed in Macaque area MT. Cereb Cortex 19: 1957-1967, 2009.
83. Zilles K, Palomero-Gallagher N, Grefkes C, Scheperjans F, Boy C, Amunts K, Schleicher A. Architectonics of the human cerebral cortex and transmitter receptor fingerprints: reconciling functional neuroanatomy and neurochemistry. Eur Neuropsychopharmacol 12: 587-599, 2002.
84. Zuiderbaan W, Harvey BM, Dumoulin SO. Modeling center-surround configurations in population receptive fields using fMRI. J Vis 12: 10, 2012.