Multiscale Functional Imaging in V1 and Cortical Correlates of Apparent Motion

  • Yves FregnacEmail author
  • Pierre Baudot
  • Fréderic Chavane
  • Jean Lorenceau
  • Olivier Marre
  • Cyril Monier
  • Marc Pananceau
  • Pedro V. Carelli
  • Gerard Sadoc


In vivo intracellular electrophysiology offers the unique possibility of listening to the “synaptic rumor” of the cortical network captured by the recording electrode in a single V1 cell. The analysis of synaptic echoes evoked during sensory processing is used to reconstruct the distribution of input sources in visual space and time. It allows us to infer, in the cortical space, the dynamics of the effective input network afferent to the recorded cell. We have applied this method to demonstrate the propagation of visually evoked activity through lateral (and possibly feedback) connectivity in the primary cortex of higher mammals. This approach, based on functional synaptic imaging, is compared here with a real-time functional network imaging technique, based on the use of voltage-sensitive fluorescent dyes. The former method gives access to microscopic convergence processes during synaptic integration in a single neuron, while the latter describes the macroscopic divergence process at the neuronal map level. The joint application of the two techniques, which address two different scales of integration, is used to elucidate the cortical origin of low-level (non-attentive) binding processes participating in the emergence of illusory motion percepts predicted by the psychological Gestalt theory.


Receptive Field Apparent Motion Lateral Geniculate Nucleus Primary Visual Cortex Synaptic Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by the CNRS, and grants from ANR (NATSTATS) and the European integrated project FACETS (FET- Bio-I3: 015879). This long-lasting line of research has benefited in its realization of the experimental participation of Dr Sebastien Georges in psychophysics, of Dr. Peggy Séries in modeling, and of Julien Fournier, Nazyed Huguet and Drs Alice René, Lyle Graham and Manuel Levy in electrophysiology at UNIC. It has also benefited in the recent years of the scientific collaborations with the laboratory of Pr. Amiram Grinvald (Weizmann Institute, Rehovot, Israel) and the CNRS DyVA team (INCM, Marseille). We thank Drs Andrew Davison and Guillaume Masson for helpful comments.


  1. Ahmed B, Hanazawa A, Undeman C, Eriksson D, Valentiniene S, Roland PE (2008) Cortical dynamics subserving visual apparent motion. Cereb Cortex 18(12):2796–2810PubMedCrossRefGoogle Scholar
  2. Albus K (1975) A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. I. The precision of the topography. Exp Brain Res 24:159–179PubMedCrossRefGoogle Scholar
  3. Angelucci A, Levitte JB, Walton EJS, Hupé JM, Bullier J, Lund JS (2002) Circuits for local and global signal integration in primary visual cortex. J Neurosci 22:8633–8646PubMedGoogle Scholar
  4. Anstis SM, Verstraten FAJ, Mather G (1998) The motion aftereffect: a review. Trends Cogn Sci 2:111–117PubMedCrossRefGoogle Scholar
  5. Basole A, White LE, Fitzpatrcik D (2003) Mapping multiple features in the population response of visual cortex. Nature 423:986–990PubMedCrossRefGoogle Scholar
  6. Baudot P, Chavane F, Pananceau M, Edet V, Gutkin B, Lorenceau J, Grant K, Frégnac Y (2000) Cellular correlates of apparent motion in the association field of cat area 17 neurons. Abstr Soc Neurosci 26:446Google Scholar
  7. Benucci A, Frazor RA, Carandini M (2007) Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron 55(1):103–117PubMedCrossRefGoogle Scholar
  8. Binzegger T, Douglas RJ, Martin KA (2004) A quantitative map of the circuit of cat primary visual cortex. J Neurosci 24:8441–8453PubMedCrossRefGoogle Scholar
  9. Borg-Graham LJ, Monier C, Frégnac Y (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393:369–373PubMedCrossRefGoogle Scholar
  10. Bringuier V, Chavane F, Glaeser L, Frégnac Y (1999) Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283:695–699PubMedCrossRefGoogle Scholar
  11. Cannon MW, Fullenkamp SC (1993) Spatial interactions in apparent contrast: individual differences in enhancement and suppression effects. Vision Res 33:1685–1695PubMedCrossRefGoogle Scholar
  12. Carlson GC, Coulter DA (2008) In vitro functional imaging in brain slices using fast voltage-sensitive dye imaging combined with whole-cell patch recording. Nat Protoc 3(2):249–255PubMedCrossRefGoogle Scholar
  13. Cass J, Alais D (2006) The mechanisms of collinear integration. J Vis 6(9):915–922PubMedCrossRefGoogle Scholar
  14. Castet E, Lorenceau J, Shiffrar M, Bonnet C (1993) Perceived speed of moving lines depends on orientation, length, speed and luminance. Vision Res 33:1921–1936PubMedCrossRefGoogle Scholar
  15. Chavane F, Monier C, Bringuier V, Baudot P, Borg-Graham L, Lorenceau J, Frégnac Y (2000) The visual cortical association field: a Gestalt concept or a physiological entity? J Physiol Paris 94:333–342PubMedCrossRefGoogle Scholar
  16. Chavane F, Sharon D, Jancke D, Marre O, Frégnac Y, Grinvald A (in revision). Horizontal spread of orientation selectivity in V1 requires intracortical cooperativity. J. NeuroscienceGoogle Scholar
  17. Daugman J (1985) Uncertainty relation for resolution in space, spatial frequency, and orientation optimized two-dimensional visual cortical filters. J Opt Soc Am A2:1160–1168CrossRefGoogle Scholar
  18. Field DJ, Hayes A, Hess RF (1993) Contour integration by the human visual system: evidence for a local “association field”. Vision Res 33:173–193PubMedCrossRefGoogle Scholar
  19. Frégnac Y (2001) Le combat des hémisphères. Pour Sci 283:94–95Google Scholar
  20. Frégnac Y, Bringuier V (1996) Spatio-temporal dynamics of synaptic integration in cat visual cortical receptive fields. In: Aertsen A, Braitenberg V (eds) Brain theory: biological basis and computational theory of vision. Springer, Amsterdam, pp 143–199Google Scholar
  21. Georges S, Sèries P, Frégnac Y, Lorenceau J (2002) Orientation dependent modulation of apparent speed: psychophysical evidence. Vision Res 42:2757–2772PubMedCrossRefGoogle Scholar
  22. Grinvald A, Hildesheim R (2004) VSDI: a new era in functional imaging of cortical dynamics. Nat Rev Neurosci 5(11):874–885PubMedCrossRefGoogle Scholar
  23. Grinvald A, Lieke EE, Frostig RD, Hildesheim R (1994) Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J Neurosci 14:2545–2568PubMedGoogle Scholar
  24. Hartline HK (1938) The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. Am J Physiol 121:400–415Google Scholar
  25. Haynes JD, Rees G (2006) Decoding mental states from brain activity in humans. Nat Rev Neurosci 7:523–534PubMedCrossRefGoogle Scholar
  26. Hikosaka O, Miyauchi S, Shimojo S (1993) Focal visual attention produces illusory temporal order and motion sensation. Vision Res 33:1219–1240PubMedCrossRefGoogle Scholar
  27. Hirsch JA, Gilbert CD (1991) Synaptic physiology of horizontal connections in the cat’s visual cortex. J Neurosci 11:1800–1809PubMedGoogle Scholar
  28. Hoffman KP, Stone J (1971) Conduction velocity of afferents to cat visual cortex: a correlation with cortical receptive field properties. Brain Res 32:460–466PubMedCrossRefGoogle Scholar
  29. Jancke D, Chavane F, Naaman S, Grinvald A (2004) Imaging cortical correlates of illusion in early visual cortex. Nature 428:423–426PubMedCrossRefGoogle Scholar
  30. Kalatsky VA, Stryker MP (2003) New paradigm for optical imaging: temporally encoded maps of intrinsic signal. Neuron 38(4):529–545PubMedCrossRefGoogle Scholar
  31. Karube F, Kisvarday ZF (2006). Bouton distribution of deep-layer spiny neurons on the functional maps in cat visual cortex. FENS Forum Abstr 3:179.14.Google Scholar
  32. Kay KN, Naseralis T, Prenger RJ, Gallant JL (2008) Identifying human natural images from brain activity. Nature 452:352–355PubMedCrossRefGoogle Scholar
  33. Knierim JJ, Van Essen DC (1992) Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J Neurophysiol 67:961–980PubMedGoogle Scholar
  34. Lee S, Blake R, Heeger DJ (2007) Hierarchy of cortical responses underlying binocular rivalry. Nature Neurosci 10(8):1048–1054PubMedCrossRefGoogle Scholar
  35. Levitt JB, Lund JS (1997) Contrast dependence of contextual effects in primate visual cortex. Nature 387:73–76PubMedCrossRefGoogle Scholar
  36. Mitchison G, Crick F (1982) Long axons within the striate cortex: their distribution, orientation, and patterns of connection. Proc Natl Acad Sci U S A 79:3661–3665PubMedCrossRefGoogle Scholar
  37. Monier C, Chavane F, Baudot P, Graham L, Frégnac Y (2003) Orientation and direction selectivity of excitatory and inhibitory inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37:663–680PubMedCrossRefGoogle Scholar
  38. Moore CI, Nelson SB (1998) Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J Neurophysiol 80:2882–2892PubMedGoogle Scholar
  39. Nauhaus I, Busse L, Carandini M, Ringach DL (2009) Stimulus contrast modulates functional connectivity in visual cortex. Nature Neurosci 12:70–76PubMedCrossRefGoogle Scholar
  40. Nowak LG, Bullier J (1997) The timing of information transfer in the visual system. In: Rockland KS, Kaas JH, Peters A (eds) Extrastriate visual cortex in primates. New York, Plenum, pp 205–241Google Scholar
  41. Polat U, Sagi D (1993) Lateral interactions between spatial channels: suppression and facilitation revealed by lateral masking experiments. Vision Res 33:993–999PubMedCrossRefGoogle Scholar
  42. Polat U, Mizobe K, Pettet MW, Kasamatsu T, Norcia AM (1998) Collinear stimuli regulate visual responses depending on cell’s contrast threshold. Nature 391:580–584PubMedCrossRefGoogle Scholar
  43. Roland PE (2002) Dynamic depolarisation fields in the cerebral cortex. Trends Neurosci 25:183–190PubMedCrossRefGoogle Scholar
  44. Roland PE, Hanazawa A, Undeman C, Eriksson D, Tompa T, Nakamura H, Valentiniene S, Ahmed B (2006) Cortical feedback depolarization waves: a mechanism of top-down influence on early visual areas. Proc Natl Acad Sci U S A 103(33):12586–12591PubMedCrossRefGoogle Scholar
  45. Séries P, Lorenceau J, Frégnac Y (2003) The silent surround of V1 receptive fields : theory and experiments. J Physiol Paris 97(4–6):453–474PubMedCrossRefGoogle Scholar
  46. Séries P, Georges S, Lorenceau J, Frégnac Y (2002) Orientation dependent modulation of apparent speed: a model based on the dynamics of feed-forward and horizontal connectivity in V1 cortex. Vision Res 42:2781–2797PubMedCrossRefGoogle Scholar
  47. Shoham D, Glaser DE, Arieli AI, Kenet T, Wijnbergen C, Toledo Y, Hildesheim R, Grinvald A (1999) Imaging cortical dynamics at high spatial and temporal resolution with novel blue voltage-sensitive dyes. Neuron 24(4):791–802PubMedCrossRefGoogle Scholar
  48. Tanifuji M, Sugiyama T, Murase K (1994) Horizontal propagation of excitation in rat visual cortical slices revealed by optical imaging. Science 266:1057–1059PubMedCrossRefGoogle Scholar
  49. Thirion B, Diuchesnay E, Hubbard EM, Dubois J, Poline J-B, LeBihan D, Deheane S (2006) Inverse retinotopy: inferring the visual content of images from brain activation patterns. Neuroimage 33:1104–1116PubMedCrossRefGoogle Scholar
  50. Tootell RB, Silverman MS, Switkes E, De Valois RL (1982) Deoxyglucose analysis of retinotopic organization in primate striate cortex. Science 218:902–904PubMedCrossRefGoogle Scholar
  51. Warnking J, Dojat M, Guerin-Dughe A, Delon-Martin C, Olympieff S, Richard N, Chehikian A, Segebarth C (2002) FMRI retinotopic mapping-step by step. Neuroimage 17:1665–1683PubMedCrossRefGoogle Scholar
  52. Wertheimer M (1912) Experimentelle Studien über das Sehen von Beuegung. Z Psychol Physiol Sinnesorg 61:161–265Google Scholar
  53. Williams MA, Baker C, Op De Beeck HP, Shim WM, Dang S, Triantafyllou C, Kanwisher N (2008) Feedback of visual object information to foveal retinotopic cortex. Nature Neurosci 11:1439–1445PubMedCrossRefGoogle Scholar
  54. Xu W, Huang X, Takagaki K, Wu JY (2007) Compression and reflection of visually evoked cortical waves. Neuron 55(1):119–129PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Yves Fregnac
    • 1
    Email author
  • Pierre Baudot
  • Fréderic Chavane
  • Jean Lorenceau
  • Olivier Marre
  • Cyril Monier
  • Marc Pananceau
  • Pedro V. Carelli
  • Gerard Sadoc
  1. 1.Unité de Neurosciences Intégratives et Computationnelles (UNIC), CNRS UPR 2191Gif-sur-YvetteFrance

Personalised recommendations