Suppressive Traveling Waves Shape Representations of Illusory Motion in Primary Visual Cortex of Awake Primate

被引:35
作者
Chemla, Sandrine [1 ,2 ]
Reynaud, Alexandre [1 ,2 ,5 ]
di Volo, Matteo [3 ,6 ]
Zerlaut, Yann [3 ,7 ]
Perrinet, Laurent [1 ,2 ]
Destexhe, Alain [3 ,4 ,6 ]
Chavane, Frederic [1 ,2 ]
机构
[1] Inst Neurosci Timone, CNRS, Unite Mixte Rech 7289, F-13385 Marseille 05, France
[2] Aix Marseille Univ, F-13385 Marseille 05, France
[3] CNRS, Unite Neurosci Informat & Complexite, F-91198 Gif Sur Yvette, France
[4] European Inst Theoret Neurosci, F-75012 Paris, France
[5] McGill Univ, McGill Vis Res, Dept Ophthalmol, Montreal, PQ, Canada
[6] Paris Saclay Inst Neurosci NeuroPSI, Gif Sur Yvette, France
[7] Ist Italian Tecnol, Ctr Neurosci & Cognit Syst, Neural Coding Lab, Corso Bettini 31, I-38068 Rovereto, Italy
基金
欧盟地平线“2020”;
关键词
apparent motion; awake monkey; intracortical interactions; nonlinear processing; traveling waves; voltage-sensitive dye imaging; CORTICAL DYNAMICS; LOW-LEVEL; COMPUTATIONAL ARCHITECTURE; VISUOTOPIC ORGANIZATION; STRIATE CORTEX; MACAQUE MONKEY; FIELD; RANGE; INTEGRATION; MODEL;
D O I
10.1523/JNEUROSCI.2792-18.2019
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
How does the brain link visual stimuli across space and time? Visual illusions provide an experimental paradigm to study these processes. When two stationary dots are flashed in close spatial and temporal succession, human observers experience a percept of apparent motion. Large spatiotemporal separation challenges the visual system to keep track of object identity along the apparent motion path, the so-called "correspondence problem." Here, we use voltage-sensitive dye imaging in primary visual cortex (V1) of awake monkeys to show that intracortical connections within V1 can solve this issue by shaping cortical dynamics to represent the illusory motion. We find that the appearance of the second stimulus in V1 creates a systematic suppressive wave traveling toward the retinotopic representation of the first. Using a computational model, we show that the suppressive wave is the emergent property of a recurrent gain control fed by the intracortical network. This suppressive wave acts to explain away ambiguous correspondence problems and contributes to precisely encode the expected motion velocity at the surface of V1. Together, these results demonstrate that the nonlinear dynamics within retinotopic maps can shape cortical representations of illusory motion. Understanding these dynamics will shed light on how the brain links sensory stimuli across space and time, by preformatting population responses for a straightforward read-out by downstream areas.
引用
收藏
页码:4282 / 4298
页数:17
相关论文
共 77 条
[1]   SPATIOTEMPORAL ENERGY MODELS FOR THE PERCEPTION OF MOTION [J].
ADELSON, EH ;
BERGEN, JR .
JOURNAL OF THE OPTICAL SOCIETY OF AMERICA A-OPTICS IMAGE SCIENCE AND VISION, 1985, 2 (02) :284-299
[2]   Cortical Dynamics Subserving Visual Apparent Motion [J].
Ahmed, Bashir ;
Hanazawa, Akitoshi ;
Undeman, Calle ;
Eriksson, David ;
Valentiniene, Sonata ;
Roland, Per E. .
CEREBRAL CORTEX, 2008, 18 (12) :2796-2810
[3]  
ALBRIGHT TD, 1987, EXP BRAIN RES, V65, P582
[4]  
Angelucci A, 2002, J NEUROSCI, V22, P8633
[5]  
BLAKEMORE C, 1972, EXP BRAIN RES, V15, P439
[6]   LOW-LEVEL AND HIGH-LEVEL PROCESSES IN APPARENT MOTION [J].
BRADDICK, OJ ;
RUDDOCK, KH ;
MORGAN, MJ ;
MARR, D .
PHILOSOPHICAL TRANSACTIONS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES, 1980, 290 (1038) :137-151
[7]   Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons [J].
Bringuier, V ;
Chavane, F ;
Glaeser, L ;
Frégnac, Y .
SCIENCE, 1999, 283 (5402) :695-699
[8]   Integrated model of visual processing [J].
Bullier, J .
BRAIN RESEARCH REVIEWS, 2001, 36 (2-3) :96-107
[9]   Motion psychophysics: 1985-2010 [J].
Burr, David ;
Thompson, Peter .
VISION RESEARCH, 2011, 51 (13) :1431-1456
[10]   Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps [J].
Buzás, P ;
Eysel, UT ;
Adorján, P ;
Kisvárday, ZF .
JOURNAL OF COMPARATIVE NEUROLOGY, 2001, 437 (03) :259-285