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Stimulus Localization by Neuronal Populations in Early Visual Cortex: Linking Functional Architecture to Perception

Chapter

Abstract

In primary visual areas any local input is initially transmitted via horizontal connections giving rise to a transient peak of activity with spreading surround. How does this scenario change when the stimulus starts to move? Psychophysical experiments indicate that localization is different for stationary flashed and moving objects depending on the stimulus history. We here demonstrate how successively presented stimuli alter cortical activation dynamics. By a combination of electrophysiological and optical recordings using voltage-sensitive dye we arrive at the conclusion that sub-threshold propagating activity pre-activates cortical regions far ahead of thalamic input. Such an anticipatory mechanism may contribute in shifts of the perceived position as observed for the flash-lag effect and line-motion illusion in human psychophysics.

Keywords

Receptive Field Primary Visual Cortex Stimulus Position Supplementary Movie Receptive Field Size 
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.

Notes

Acknowledgments

D.J. supported by Minerva Foundation, BMBF, Deutsche Forschungsge­meinschaft (Scho 336/4-2 and Di 334/5-1,3). F.C. supported by Marie Curie EU fellowship. A.G. supported by the Grodetsky Center, Goldsmith, Korber & ISF Foundations, BMBF/MOS, and NIH 1R01-EB00790-01 grants.

References

  1. 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
  2. Allman J, Miezin F, McGuiness E (1985) Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. Annu Rev Neurosci 8:407–430PubMedCrossRefGoogle Scholar
  3. Benucci A, Frazor RA, Carandini M (2007) Standing waves and traveling waves distinguish two circuits in visual cortex. Neuron 55:103–117PubMedCrossRefGoogle Scholar
  4. Berry MJ II, Brivanlou IH, Jordan TA, Meister M (1999) Anticipation of moving stimuli by the retina. Nature 398:334–338PubMedCrossRefGoogle Scholar
  5. Bishop PO, Coombs JS, Henry GH (1971) Responses to visual contours: Spatio-temporal aspects of excitation in the receptive fields of simple striate neurones. J Physiol (London) 219:625–657Google Scholar
  6. Bishop PO, Coombs JS, Henry GH (1973) Receptive fields of simple cells in the cat striate cortex. J Physiol (London) 231:31–60Google Scholar
  7. 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
  8. Cavanagh P, Arguin M, von Grünau M (1989) Interattribute apparent motion. Vision Res 29:1197–1204PubMedCrossRefGoogle Scholar
  9. Ceriatti C, Botelho EP, Soares JGM, Gattass R, Fiorani M (2007) Shorter latencies to moving stimuli in primate V1 single units. Soc Neurosci Abstracts 37:279.22Google Scholar
  10. Cohen LB, Salzberg BM, Grinvald A (1978) Optical methods for monitoring neuron activity. Annu Rev Neurosci 7:171–182CrossRefGoogle Scholar
  11. Dayan P, Abbott LF (2001) Theoretical neuroscience: computational and mathematical modeling of neural systems. Cambridge, MIT PressGoogle Scholar
  12. DeVries SH, Baylor DA (1997) Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J Neurophysiol 78:2048–2060PubMedGoogle Scholar
  13. Dinse HR, Jancke D (2001a) Time-variant processing in V1: From microscopic (single cell) to mesoscopic (population) levels. Trends Neurosci 24:203–205PubMedCrossRefGoogle Scholar
  14. Dinse HR, Jancke D (2001b) Comparative population analysis of cortical representations in parametric spaces of visual field and skin: a unifying role for nonlinear interactions as a basis for active information processing across modalities. Prog Brain Res 130:155–173PubMedCrossRefGoogle Scholar
  15. Dragoi V, Sharma J, Miller EK, Sur M (2002) Dynamics of neuronal sensitivity in visual cortex and local feature discrimination. Nat Neurosci 5:883–891PubMedCrossRefGoogle Scholar
  16. Dumoulin SO, Wandell BA (2008) Population receptive field estimates in human visual cortex. Neuroimage 39:647–660PubMedCrossRefGoogle Scholar
  17. Downing PE, Treisman AM (1997) The line-motion illusion: Attention or impletion? J Exp Psychol Hum Percept Perform 23:768–779PubMedCrossRefGoogle Scholar
  18. Duysens J, Orban GA, Verbeke O (1982) Velocity sensitivity mechanisms in cat visual cortex. Exp Brain Res 45:285–294PubMedCrossRefGoogle Scholar
  19. Eagleman DM, Sejnowski TJ (2000) Motion integration and postdiction in visual awareness. Science 287:2036–2038PubMedCrossRefGoogle Scholar
  20. Fitzpatrick D (2000) Seeing beyond the receptive field in primary visual cortex. Curr Opin Neurobiol 10:438–443PubMedCrossRefGoogle Scholar
  21. Freeman WJ (2000) Mesoscopic neurodynamics: from neuron to brain. J Physiol (Paris) 94:303–322CrossRefGoogle Scholar
  22. Fu YX, Shen Y, Gao H, Dan Y (2004) Asymmetry in visual cortical circuits underlying motion-induced perceptual mislocalization. J Neurosci 24:2165–2171PubMedCrossRefGoogle Scholar
  23. Gegenfurtner KR, Hawken MJ (1996) Interaction of motion and color in the visual pathways. Trends Neurosci 19:394–400PubMedCrossRefGoogle Scholar
  24. Grinvald A, Anglister L, Freeman JA, Hildesheim R, Manker A (1984) Real-time optical imaging of naturally evoked electrical activity in intact frog brain. Nature 308:848–850PubMedCrossRefGoogle Scholar
  25. Grinvald A, Lieke E, Frostig R, 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
  26. Grinvald A, Shoham D, Shmuel A, Glaser D, Vanzetta I, Shtoyerman E, Slovin H, Arieli A (1999) In vivo optical imaging of cortical architecture and dynamics. In: Wind-Horst U, Johansson H (eds) Modern techniques in neuroscience research. Springer, New York, pp 893–969Google Scholar
  27. Grinvald A, Hildesheim R (2004) VSDI: a new era in functional imaging of cortical dynamics. Nat Rev Neurosci 5:874–885PubMedCrossRefGoogle Scholar
  28. Hazelhoff FF, Wiersma H (1924) Die Wahrnehmungszeit [The sensation time]. Zeitschrift für Psychologie 96:171–188Google Scholar
  29. Hikosaka O, Miyauchi S (1993) Voluntary and stimulus induced attention detected as motion sensation. Perception 22:517–526PubMedCrossRefGoogle Scholar
  30. Hikosaka O, Miyauchi S, Shimojo S (1993) Focal visual attention produces illusory temporal order and motion sensation. Vision Res 33:1219–1240PubMedCrossRefGoogle Scholar
  31. Hughes A (1971) Topographical relationships between the anatomy and physiology of the rabbit visual system. Doc Ophthalmol 30:33–159PubMedCrossRefGoogle Scholar
  32. Jancke D, Erlhagen W, Dinse HR, Akhavan AC, Giese M, Steinhage A, Schöner G (1999) Parametric population representation of retinal location: neuronal interaction dynamics in cat primary visual cortex. J Neurosci 19:9016–9028PubMedGoogle Scholar
  33. Jancke D (2000). Orientation formed by a spot’s trajectory: a two-dimensional population approach in primary visual cortex. J Neurosci 20 RC86:1–6Google Scholar
  34. Jancke D, Chavane F, Naaman S, Grinvald A (2004a) Imaging correlates of visual illusion in early visual cortex. Nature 428:423–426PubMedCrossRefGoogle Scholar
  35. Jancke D, Erlhagen W, Schöner G, Dinse HR (2004b) Shorter latencies for motion trajectories than for flashes in population responses of primary visual cortex. J Physiol (London) 556:971–982CrossRefGoogle Scholar
  36. Jazayeri M, Movshon JA (2006) A new perceptual illusion reveals mechanisms of sensory decoding. Nat Neurosci 446:912–915Google Scholar
  37. Jensen HJ, Martin J (1980) On localization of moving objects in the visual system of cats. Biol Cybern 36:173–177PubMedCrossRefGoogle Scholar
  38. Kanizsa G (1951). Sulla polarizzazione del movimento gamma. Archiva Psicologica Neurologica Psichiatrica 3:224–267Google Scholar
  39. Kawahara J, Yokosawa K, Nishida S, Sato T (1996) Illusory line motion in visual search: attentional facilitation or apparent motion? Perception 25:901–920PubMedCrossRefGoogle Scholar
  40. Kenkel F (1913) Untersuchungen über den Zusammenhang zwischen Erscheinungsgröße und Erscheinungsbewegung bei einigen sogenannten optischen Täuschungen. Zeitschrift für Psychologie 67:358–449Google Scholar
  41. Kerzel D, Gegenfurtner KR (2003) Neuronal processing delays are compensated in the sensorimotor branch of the visual system. Curr Biol 13:1975–1978PubMedCrossRefGoogle Scholar
  42. Kirschfeld K, Kammer T (1999) The Fröhlich effect: a consequence of the interaction of visual focal attention and metacontrast. Vision Res 39:3702–3709PubMedCrossRefGoogle Scholar
  43. Krekelberg B, Lappe M (1999) Temporal recruitment along the trajectory of moving objects and the perception of position. Vision Res 39:2669–2679PubMedCrossRefGoogle Scholar
  44. Krekelberg B, Lappe M, Whitney D, Cavanagh P, Eagleman DM, Sejnowski TJ (2000) The position of moving objects. Science 289:1107aPubMedCrossRefGoogle Scholar
  45. Krekelberg B, Lappe M (2001) Neuronal latencies and the position of moving objects. Trends Neurosci 24:335–339PubMedCrossRefGoogle Scholar
  46. MacKay DM (1958) Perceptual stability of a stroboscopically lit visual field containing self-luminous objects. Nature 181:507–508PubMedCrossRefGoogle Scholar
  47. Maiche A, Budelli R, Gomez-Sena L (2007) Spatial facilitation is involved in flash-lag effect. Vision Res 47:1655–1661PubMedCrossRefGoogle Scholar
  48. Mateeff S, Hohnsbein J (1988) Percepual latencies are shorter for motion towards the fovea than for motion away. Vision Res 28:711–719PubMedCrossRefGoogle Scholar
  49. Metzger W (1932) Versuch einer gemeinsamen Theorie der Phänomene Fröhlichs und Hazelhoffs und Kritik ihrer Verfahren zur Messung der Empfindungszeit. Psychologishe Forschung 16:176–200CrossRefGoogle Scholar
  50. Müsseler J, Aschersleben G (1998) Localizing the first position of a moving stimulus: The Fröhlich effect and an attention-shifting explanation. Percept Psychophys 60:683–695PubMedCrossRefGoogle Scholar
  51. Nakayama K, Mackeben M (1989) Sustained and transient components of focal visual attention. Vision Res 29:1631–1647Google Scholar
  52. Nicolelis MA, Ghazanfar AA, Stambaugh CR, Oliveira LM, Laubach M, Chapin JK, Nelson RJ, Kaas JH (1998) Simultaneous encoding of tactile information by three primate cortical areas. Nat Neurosci 1:621–630PubMedCrossRefGoogle Scholar
  53. Nijhawan R (1994) Motion extrapolation in catching. Nature 370:256–257PubMedCrossRefGoogle Scholar
  54. Orban GA, Hoffmann KP, Duysens J (1985) Velocity selectivity in the cat visual system. I. Responses of LGN cells to moving bar stimuli: a comparison with cortical areas 17 and 18. J Neurophysiol 54:1026–1049Google Scholar
  55. Petersen C, Grinvald A, Sakmann B (2003) Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J Neurosci 23:1298–1309PubMedGoogle Scholar
  56. Polat U, Sagi D (1993) Lateral interactions between spatial channels: suppression and facilitation revealed by lateral masking experiments. Vision Res 33:993–999PubMedCrossRefGoogle Scholar
  57. 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
  58. Posner MI, Snyder CRR, Davidson BJ (1980) Attention and the detection of signals. J Exp Psychol 109:160–174PubMedCrossRefGoogle Scholar
  59. Pulgarin M, Nevado A, Guo K, Robertson RG, Thiele A, Young MP (2003) Spatio-temporal regularities beyond the classical receptive field affect the information conveyed by the responses of V1 neurons. Soc Neurosci Abstracts 33:910.16Google Scholar
  60. Purushothaman G, Patel SS, Bedell HE, Ogmen H (1999) Moving ahead through differential visual latency. Nature 396:424CrossRefGoogle Scholar
  61. Rao RPN, Ballard DH (1999) Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive field effects. Nat Neurosci 2:79–87PubMedCrossRefGoogle Scholar
  62. Sagi D, Julesz B (1986) Enhanced detection in the aperture of focal attention during simple discrimination tasks. Nature 321:693–695PubMedCrossRefGoogle Scholar
  63. Salinas E, Abbott LF (1994) Vector reconstruction from firing rates. J Comput Neurosci 1:89–107PubMedCrossRefGoogle Scholar
  64. Schlag J, Cai RH, Dorfman A, Mohempour A, Schlag-Rey M (2000) Extrapolating movement without retinal motion. Nature 403:38–39PubMedCrossRefGoogle Scholar
  65. Seriès 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
  66. Sheth BR, Nijhawan R, Shimojo S (2000) Changing objects lead briefly flashed ones. Nat Neurosci 3:489–495PubMedCrossRefGoogle Scholar
  67. Shimojo S, Miyauchi S, Hikosaka O (1997) Visual motion sensation yielded by non-visually driven attention. Vision Res 37:1575–1580PubMedCrossRefGoogle Scholar
  68. Shoham D, Glaser DE, Arieli A, 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 24:791−802Google Scholar
  69. Steinman BA, Steinman SB, Lehmkuhle S (1995) Visual attention mechanisms show a center-surround organization. Vision Res 35:1859–1869PubMedCrossRefGoogle Scholar
  70. Sterkin A, Arieli A, Ferster D, Glaser DE, Grinvald A (1999) Real time optical imaging in cat visual cortex exhibits high similarity to intracellular activity. Abstract of the 5th IBRO World Congress of Neuroscience, p 122Google Scholar
  71. Szulborski RG, Palmer LA (1990) The two-dimensional spatial structure of nonlinear subunits in the RFs of complex cells. Vision Res 30:249–254PubMedCrossRefGoogle Scholar
  72. Tusa RJ, Rosenquist AC, Palmer LA (1979) Retinotopic organization of areas 18 and 19 in the cat. J Comp Neurol 185:657–678PubMedCrossRefGoogle Scholar
  73. van Beers RJ, Wolpert DM, Haggard P (2001) Sensorimotor integration compensates for visual localization errors during smooth pursuit eye movements. J Neurophysiol 85:1914–1922PubMedGoogle Scholar
  74. Victor JD, Purpura K, Katz E, Mao B (1994) Population encoding of spatial frequency, orientation, and color in macaque V1. J Neurophysiol 72:2151–2166PubMedGoogle Scholar
  75. von Grünau M, Faubert J (1994) Intra-attribute and interattribute motion induction. Perception 23:913–928CrossRefGoogle Scholar
  76. von Grünau M, Racette L, Kwas M (1996a) Measuring the attentional speed-up in the motion induction effect. Vision Res 36:2433–2446CrossRefGoogle Scholar
  77. von Grünau M, Dube S, Kwas M (1996b) Two contributions of motion induction: a preattentive effect and facilitation due to attentional capture. Vision Res 36:2447–2457CrossRefGoogle Scholar
  78. Wertheimer M (1912) Experimentelle Studien über das Sehen von Bewegung. Zeitschrift für Psychologie 61:161–265Google Scholar
  79. Whitney D, Murakami I, Cavanagh P (2000) Illusory spatial offset of a flash relative to a moving stimulus is caused by differential latencies for moving and flashed stimuli. Vision Res 40:137–149PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of NeurobiologyRuhr-University BochumBochumGermany

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