Saccades during object viewing modulate oscillatory phase in the superior temporal sulcus

Journal of Neuroscience

Volumn 31, Issue 50, 2011, Pages 18423-18432

  Bartlett, Adrian M ^a   Ovaysikia, Shima ^a   Logothetis, Nikos K ^b,c   Hoffman, Kari L ^a  

^a YORK UNIVERSITY   (Canada)

^b MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; ELECTRIC POTENTIAL; EVOKED VISUAL RESPONSE; EYE FIXATION; MACACA MULATTA; MALE; NONHUMAN; OSCILLATION; PERCEPTION; PRIORITY JOURNAL; PROCESSING; RECORDING; SACCADIC EYE MOVEMENT; SUPERIOR TEMPORAL SULCUS; VISION; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; FIXATION, OCULAR; MACACA MULATTA; MALE; NEURONS; PHOTIC STIMULATION; REACTION TIME; SACCADES; TEMPORAL LOBE; VISUAL CORTEX; VISUAL PERCEPTION;

EID: 83455179130     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4102-11.2011     Document Type: Article

References (82)

1. Afraz SR, Kiani R, Esteky H (2006) Microstimulation of inferotemporal cortex influences face categorization. Nature 442:692-695.
2. Anastassiou CA, Montgomery SM, Barahona M, Buzsáki G, Koch C (2010) The effect of spatially inhomogeneous extracellular electric fields on neurons. J Neurosci 30:1925-1936.
3. Anastassiou CA, Perin R, Markram H, Koch C (2011) Ephaptic coupling of cortical neurons. Nat Neurosci 14:217-223.
4. Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19:2209-2223.
5. Baylis GC, Rolls ET, Leonard CM (1987) Functional subdivisions of the temporal lobe neocortex. J Neurosci 7:330-342.
6. Berens P (2009) CircStat: a MATLAB toolbox for circular statistics. J Stat Soft 31:1-21.
7. Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP (2010) Chronux: a platform for analyzing neural signals. J Neurosci Methods 192:146-151.
8. Bollimunta A, Chen Y, Schroeder CE, Ding M (2008) Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques. J Neurosci 28:9976-9988.
9. Bollimunta A, Mo J, Schroeder CE, Ding M (2011) Neuronal mechanisms and attentional modulation of corticothalamic alpha oscillations. J Neurosci 31:4935-4943.
10. Bosman CA, Womelsdorf T, Desimone R, Fries P (2009) A microsaccadic rhythm modulates gamma-band synchronization and behavior. J Neurosci 29:9471-9480.
11. Bremmer F, Kubischik M, Hoffmann KP, Krekelberg B (2009) Neural dynamics of saccadic suppression. J Neurosci 29:12374-12383.
12. Bruce C, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 46:369-384.
13. Buonomano DV, Maass W (2009) State-dependent computations: spatiotemporal processing in cortical networks. Nat Rev Neurosci 10:113-125.
14. Burr DC, Morrone MC, Ross J (1994) Selective suppression of the magnocellular visual pathway during saccadic eye movements. Nature 371:511-513.
15. Cloherty SL, Mustari MJ, Rosa MG, Ibbotson MR (2010) Effects of saccades on visual processing in primate MSTd. Vision Res 50:2683-2691.
16. Deco G, Buehlmann A, Masquelier T, Hugues E (2011) The role of rhythmic neural synchronization in rest and task conditions. Front Hum Neurosci 5:4.
17. Diamond MR (2002) The effect of saccades on visual sensitivity and time perception. PhD thesis, University of Western Australia, School of Psychology.
18. Fell J, Axmacher N (2011) The role of phase synchronization in memory processes. Nat Rev Neurosci 12:105-118.
19. Fröhlich F, McCormick DA (2010) Endogenous electric fields may guide neocortical network activity. Neuron 67:129-143.
20. Gallant JL, Connor CE, Van Essen DC (1998) Neural activity in areas V1, V2 and V4 during free viewing of natural scenes compared to controlled viewing. Neuroreport 9:1673-1678.
21. Gawne TJ, Woods JM (2003) The responses of visual cortical neurons encode differences across saccades. Neuroreport 14:105-109.
22. Gutkin BS, Laing CR, Colby CL, Chow CC, Ermentrout GB (2001) Turning on and off with excitation: the role of spike-timing asynchrony and synchrony in sustained neural activity. J Comput Neurosci 11:121-134.
23. Hansen T, Gegenfurtner KR (2009) Independence of color and luminance edges in natural scenes. Vis Neurosci 26:35-49.
24. Henderson JM, Williams CC, Falk RJ (2005) Eye movements are functional during face learning. Mem Cognit 33:98-106.
25. Hoffman KL, Ghazanfar AA, Gauthier I, Logothetis NK (2007) Categoryspecific responses to faces and objects in primate auditory cortex. Front Syst Neurosci 1:2.
26. Horel JA (1993) Retrieval of a face discrimination during suppression of monkey temporal cortex with cold. Neuropsychologia 31:1067-1077.
27. Horel JA, Pytko-Joiner DE, Voytko ML, Salsbury K (1987) The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behav Brain Res 23:29-42.
28. Ibbotson M, Krekelberg B (2011) Visual perception and saccadic eye movements. Curr Opin Neurobiol 21:553-558.
29. Ibbotson MR, Cloherty SL (2009) Visual perception: saccadic omission- suppression or temporal masking? Curr Biol 19:R493-R496.
30. Ibbotson MR, Price NS, Crowder NA, Ono S, Mustari MJ (2007) Enhanced motion sensitivity follows saccadic suppression in the superior temporal sulcus of the macaque cortex. Cereb Cortex 17:1129-1138.
31. Ibbotson MR, Crowder NA, Cloherty SL, Price NS, Mustari MJ (2008) Saccadic modulation of neural responses: possible roles in saccadic suppression, enhancement, and time compression. J Neurosci 28:10952-10960.
32. Ito J, Maldonado P, Singer W, Grün S (2011) Saccade-related modulations of neuronal excitability support synchrony of visually elicited spikes. Cereb Cortex 21:2482-2497.
33. Kayser C, Montemurro MA, Logothetis NK, Panzeri S (2009) Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 61:597-608.
34. Kleiser R, Seitz RJ, Krekelberg B (2004) Neural correlates of saccadic suppression in humans. Curr Biol 14:386-390.
35. Krauzlis RJ, Miles FA (1996) Release of fixation for pursuit and saccades in humans: evidence for shared inputs acting on different neural substrates. J Neurophysiol 76:2822-2833.
36. Kupper R, Gewaltig M, Korner U, Korner E (2005) Spike-latency codes and the effect of saccades. Neurocomputing 65-66:189-194.
37. Lakatos P, O'Connell MN, Barczak A, Mills A, Javitt DC, Schroeder CE (2009) The leading sense: supramodal control of neurophysiological context by attention. Neuron 64:419-430.
38. Latour PL (1962) Visual threshold during eye movements. Vision Res 2:261.
39. Lee TS, Mumford D (2003) Hierarchical Bayesian inference in the visual cortex. J Opt Soc Am A Opt Image Sci Vis 20:1434-1448.
40. Lee TS, Stepleton T, Potetz B, Samonds J (2009) Neural encoding of scene statistics for surface and object inference. In: Object categorization: computer and human vision perspectives (Dickinson S, Leonardis A, Schiele B, Tarr M, eds), pp 451-474. New York: Cambridge UP.
41. Leopold DA, Logothetis NK (1998) Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Exp Brain Res 123:341-345.
42. Li N, DiCarlo JJ (2008) Unsupervised natural experience rapidly alters invariant object representation in visual cortex. Science 321:1502-1507.
43. Lubenov EV, Siapas AG (2008) Decoupling through synchrony in neuronal circuits with propagation delays. Neuron 58:118-131.
44. MacEvoy SP, Hanks TD, Paradiso MA (2008) Macaque V1 activity during natural vision: effects of natural scenes and saccades. J Neurophysiol 99:460-472.
45. Maldonado P, Babul C, Singer W, Rodriguez E, Berger D, Grün S (2008) Synchronization of neuronal responses in primary visual cortex of monkeys viewing natural images. J Neurophysiol 100:1523-1532.
46. Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164:177-190.
47. Maris E, Schoffelen JM, Fries P (2007) Nonparametric statistical testing of coherence differences. J Neurosci Methods 163:161-175.
48. Masquelier T, Hugues E, Deco G, Thorpe SJ (2009) Oscillations, phase-offiring coding, and spike timing-dependent plasticity: an efficient learning scheme. J Neurosci 29:13484-13493.
49. Masquelier T, Albantakis L, Deco G (2011) The timing of vision-how neural processing links to different temporal dynamics. Front Psychol 2:151.
50. McLelland D, Paulsen O (2009) Neuronal oscillations and the rate-to-phase transform: mechanism, model and mutual information. J Physiol 587:769-785.
51. Melcher D (2005) Spatiotopic transfer of visual-form adaptation across saccadic eye movements. Curr Biol 15:1745-1748.
52. Melloni L, Schwiedrzik CM, Rodriguez E, Singer W (2009) (Micro)Saccades, corollary activity and cortical oscillations. Trends Cogn Sci 13:239-245.
53. Montemurro MA, Rasch MJ, Murayama Y, Logothetis NK, Panzeri S (2008) Phase-of-firing coding of natural visual stimuli in primary visual cortex. Curr Biol 18:375-380.
54. Nadasdy Z (2009) Information encoding and reconstruction from the phase of action potentials. Front Syst Neurosci 3:6.
55. Nadasdy Z (2010) Binding by asynchrony: the neuronal phase code. Front Neurosci 15:4.
56. Ozen S, Sirota A, Belluscio MA, Anastassiou CA, Stark E, Koch C, Buzsáki G (2010) Transcranial electric stimulation entrains cortical neuronal populations in rats. J Neurosci 30:11476-11485.
57. Perrett DI, Hietanen JK, Oram MW, Benson PJ (1992) Organization and functions of cells responsive to faces in the temporal cortex. Philos Trans R Soc Lond B Biol Sci 335:23-30.
58. Purpura KP, Kalik SF, Schiff ND (2003) Analysis of perisaccadic field potentials in the occipitotemporal pathway during active vision. J Neurophysiol 90:3455-3478.
59. Rajkai C, Lakatos P, Chen CM, Pincze Z, Karmos G, Schroeder CE (2008) Transient cortical excitation at the onset of visual fixation. Cereb Cortex 18:200-209.
60. Rao RP, Ballard DH (1999) Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 2:79-87.
61. Reppas JB, Usrey WM, Reid RC (2002) Saccadic eye movements modulate visual responses in the lateral geniculate nucleus. Neuron 35:961-974.
62. Ringo JL, Sobotka S, Diltz MD, Bunce CM (1994) Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons. J Neurophysiol 71:1285-1288.
63. Rolls ET, Aggelopoulos NC, Zheng F (2003) The receptive fields of inferior temporal cortex neurons in natural scenes. J Neurosci 23:339-348.
64. Rucci M, Desbordes G (2003) Contributions of fixational eye movements to the discrimination of briefly presented stimuli. J Vis 3:852-864.
65. Samengo I, Montemurro MA (2010) Conversion of phase information into a spike-count code by bursting neurons. PLoS One 5:e9669.
66. Scalaidhe SP, Albright TD, Rodman HR, Gross CG (1995) Effects of superior temporal polysensory area lesions on eye movements in the macaque monkey. J Neurophysiol 73:1-19.
67. Scalaidhe SP, Rodman HR, Albright TD, Gross CG (1997) The effects of combined superior temporal polysensory area and frontal eye field lesions on eye movements in the macaque monkey. Behav Brain Res 84:31-46.
68. Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32:9-18.
69. Schroeder CE, Wilson DA, Radman T, Scharfman H, Lakatos P (2010) Dynamics of active sensing and perceptual selection. Curr Opin Neurobiol 20:172-176.
70. Seltzer B, Pandya DN (1989) Frontal lobe connections of the superior temporal sulcus in the rhesus monkey. J Comp Neurol 281:97-113.
71. Seltzer B, Pandya DN (1994) Parietal, temporal, and occipital projections to cortex of the superior temporal sulcus in the rhesus monkey: a retrograde tracer study. J Comp Neurol 343:445-463.
72. Siapas AG, Lubenov EV, Wilson MA (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46:141-151.
73. Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193-1216.
74. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60:683-697.
75. Sobotka S, Nowicka A, Ringo JL (1997) Activity linked to externally cued saccades in single units recorded from hippocampal, parahippocampal, and inferotemporal areas of macaques. J Neurophysiol 78:2156-2163.
76. Sobotka S, Zuo W, Ringo JL (2002) Is the functional connectivity within temporal lobe influenced by saccadic eye movements? J Neurophysiol 88:1675-1684.
77. Thiele A, Henning P, Kubischik M, Hoffmann KP (2002) Neural mechanisms of saccadic suppression. Science 295:2460-2462.
78. Vinje WE, Gallant JL (2000) Sparse coding and decorrelation in primary visual cortex during natural vision. Science 287:1273-1276.
79. Vinje WE, Gallant JL (2002) Natural stimulation of the nonclassical receptive field increases information transmission efficiency in V1. J Neurosci 22:2904-2915.
80. Womelsdorf T, Fries P, Mitra PP, Desimone R (2006) Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 439:733-736.
81. Yeterian EH, Pandya DN (1989) Thalamic connections of the cortex of the superior temporal sulcus in the rhesus monkey. J Comp Neurol 282:80-97.
82. Zipser K, Lamme VA, Schiller PH (1996) Contextual modulation in primary visual cortex. J Neurosci 16:7376-7389.