Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-26T07:35:16.995Z Has data issue: false hasContentIssue false
  • English
  • Français

A model of the dynamics of retinal activity during natural visual fixation

Published online by Cambridge University Press:  19 July 2007

GAËLLE DESBORDES  and
MICHELE RUCCI
GAËLLE DESBORDES
Affiliation:
Division of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts
MICHELE RUCCI
Affiliation:
Department of Cognitive and Neural Systems, Boston University, Boston, Massachusetts
Get access Rights & Permissions [Opens in a new window]

Abstract

During visual fixation, small eye movements keep the retinal image continuously in motion. It is known that neurons in the visual system are sensitive to the spatiotemporal modulations of luminance resulting from this motion. In this study, we examined the influence of fixational eye movements on the statistics of neural activity in the macaque's retina during the brief intersaccadic periods of natural visual fixation. The responses of parvocellular (P) and magnocellular (M) ganglion cells in different regions of the visual field were modeled while their receptive fields scanned natural images following recorded traces of eye movements. Immediately after the onset of fixation, wide ensembles of coactive ganglion cells extended over several degrees of visual angle, both in the central and peripheral regions of the visual field. Following this initial pattern of activity, the covariance between the responses of pairs of P and M cells and the correlation between the responses of pairs of M cells dropped drastically during the course of fixation. Cell responses were completely uncorrelated by the end of a typical 300-ms fixation. This dynamic spatial decorrelation of retinal activity is a robust phenomenon independent of the specifics of the model. We show that it originates from the interaction of three factors: the statistics of natural scenes, the small amplitudes of fixational eye movements, and the temporal sensitivities of ganglion cells. These results support the hypothesis that fixational eye movements, by shaping the statistics of retinal activity, are an integral component of early visual representations.

Keywords

Retinal ganglion cellsFixational eye movementsNatural imagesPairwise correlationRedundancy reductionMicrosaccade
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 2 , March 2007 , pp. 217 - 230
Copyright
2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abbott, L.F., Varela, J.A., Sen, K. & Nelson, S.B. (1997). Synaptic depression and cortical gain control. Science 275, 220–224.CrossRefGoogle Scholar
Ahissar, E. & Arieli, A. (2001). Figuring space by time. Neuron 32, 185–201.CrossRefGoogle Scholar
Alonso, J.M., Usrey, W.M. & Reid, R.C. (1996). Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815–819.CrossRefGoogle Scholar
Andrews, T.J. & Coppola, D.M. (1999). Idiosyncratic characteristics of saccadic eye movements when viewing different visual environments. Vision Research 39, 2947–2953.CrossRefGoogle Scholar
Arend, L.E. (1973). Spatial differential and integral operations in human vision: Implications of stabilized retinal image fading. Psychological Review 80, 374–395.CrossRefGoogle Scholar
Atick, J.J. (1992). Could information theory provide an ecological theory of sensory processing? Network: Computation in Neural Systems 3, 213–251.Google Scholar
Atick, J.J. & Redlich, A. (1992). What does the retina know about natural scenes? Neural Computation 4, 196–210.Google Scholar
Attneave, F. (1954). Some informational aspects of visual perception. Psychological Review 61, 183–193.CrossRefGoogle Scholar
Averill, H.I. & Weymouth, F.W. (1925). Visual perception and the retinal mosaic, II. The influence of eye movements on the displacement threshold. Journal of Comparative Psychology 5, 147–176.Google Scholar
Barlow, H.B. (1961). Possible principles underlying the transformations of sensory messages. In Sensory Communication, ed. Rosenblith, W.A., pp. 217–234. Cambridge, MA: MIT Press.
Benardete, E.A. & Kaplan, E. (1997). The receptive field of the primate P retinal ganglion cell, I: Linear dynamics. Visual Neuroscience 14, 169–185.CrossRefGoogle Scholar
Benardete, E.A. & Kaplan, E. (1999a). The dynamics of primate M retinal ganglion cells. Visual Neuroscience 16, 355–368.Google Scholar
Benardete, E.A. & Kaplan, E. (1999b). Dynamics of primate P retinal ganglion cells: Responses to chromatic and achromatic stimuli. Journal of Physiology (London) 519.3, 775–790.Google Scholar
Benardete, E.A., Kaplan, E. & Knight, B.W. (1992). Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Visual Neuroscience 8, 483–486.CrossRefGoogle Scholar
Brady, N. & Field, D.J. (2000). Local contrast in natural images: Normalisation and coding efficiency. Perception 29, 1041–55.CrossRefGoogle Scholar
Cai, D., DeAngelis, G.C. & Freeman, R.D. (1997). Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kitten. Journal of Neurophysiology 78, 1045–1061.CrossRefGoogle Scholar
Carandini, M., Demb, J.B., Mante, V., Tolhurst, D.J., Dan, Y., Olshausen, B.A., Gallant, J.L. & Rust, N.C. (2005). Do we know what the early visual system does? Journal of Neuroscience 25, 10577–97.Google Scholar
Casile, A. & Rucci, M. (2006). A theoretical analysis of the influence of fixational instability on the development of thalamo-cortical connectivity. Neural Computation 18, 569–590.CrossRefGoogle Scholar
Crane, H.D. & Steele, C.M. (1985). Generation V dual Purkinje-image eyetracker. Applied Optics 24, 527–537.CrossRefGoogle Scholar
Croner, L.J. & Kaplan, E. (1995). Receptive fields of P and M ganglion cells across the primate retina. Vision Research 35, 7–24.CrossRefGoogle Scholar
Dan, Y., Atick, J.J. & Reid, R.C. (1996). Efficient coding of natural scenes in the lateral geniculate nucleus: Experimental test of a computational theory. Journal of Neuroscience 16, 3351–3362.Google Scholar
Ditchburn, R.W. & Ginsborg, B.L. (1952). Vision with a stabilized retinal image. Nature 170, 36–37.CrossRefGoogle Scholar
Ditchburn, R.W. & Ginsborg, B.L. (1953). Involuntary eye movements during fixation. Journal of Physiology (London) 119, 1–17.CrossRefGoogle Scholar
Eizenman, M., Hallett, P. & Frecker, R.C. (1985). Power spectra for ocular drift and tremor. Vision Research 25, 1635–1640.CrossRefGoogle Scholar
Enroth-Cugell, C., Robson, J.G., Schweitzer-Tong, D.E. & Watson, A.B. (1983). Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation. Journal of Physiology (London) 341, 279–307.CrossRefGoogle Scholar
Field, D.J. (1987). Relations between the statistics of natural images and the response properties of cortical cells. Journal of the Optical Society of America A, Optics and Image Science 4, 2379–94.CrossRefGoogle Scholar
Greschner, M., Bongard, M., Rujan, P. & Ammermüller, J. (2002). Retinal ganglion cell synchronization by fixational eye movements improves feature estimation. Nature Neuroscience 5, 341–7.CrossRefGoogle Scholar
Greschner, M., Thiel, A., Kretzberg, J. & Ammermüller, J. (2006). Complex spike-event pattern of transient on-off retinal ganglion cells. Journal of Neurophysiology 96, 2845–56.CrossRefGoogle Scholar
Gur, M., Beylin, A. & Snodderly, D.M. (1997). Response variability of neurons in primary visual cortex (V1) of alert monkeys. Journal of Neuroscience 17, 2914–20.Google Scholar
Harris, C.M., Hainline, L., Abramov, I., Lemerise, E. & Camenzuli, C. (1988). The distribution of fixation durations in infants and naive adults. Vision Research 28, 419–432.CrossRefGoogle Scholar
Hering, E. (1899). über die Grenzen der Sehschärfe. berichte der Königlichen Sächsischen Gesellshaft der Wissenschaften. Mathematisch-Physische Klasse 20, 16–24.Google Scholar
Kapoula, Z.A., Robinson, D.A. & Hain, T.C. (1986). Motion of the eye immediately after a saccade. Experimental Brain Research 61, 386–394.CrossRefGoogle Scholar
Lee, B.B. (1996). Receptive field structure in the primate retina. Vision Research 36, 631–44.CrossRefGoogle Scholar
Lee, B.B., Pokorny, J., Smith, V.C. & Kremers, J. (1994). Responses to pulses and sinusoids in macaque ganglion cells. Vision Research 34, 3081–3096.CrossRefGoogle Scholar
Lee, B.B., Pokorny, J., Smith, V.C., Martin, P.R. & Valberg, A. (1990). Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. Journal of the Optical Society of America A, Optics and Image Science 7, 2223–36.CrossRefGoogle Scholar
Leopold, D.A. & Logothetis, N.K. (1998). Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex. Experimental Brain Research 123, 341–345.CrossRefGoogle Scholar
Marshall, W.H. & Talbot, S.A. (1942). Recent evidence for neural mechanisms in vision leading to a general theory of sensory acuity. In Biological Symposia—Visual Mechanisms, ed. Kluver & H., volume 7, pp. 117–164. Lancaster, PA: Cattel.
Martinez-Conde, S., Macknik, S.L. & Hubel, D.H. (2000). Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys. Nature Neuroscience 3, 251–258.CrossRefGoogle Scholar
Martinez-Conde, S., Macknik, S.L. & Hubel, D.H. (2002). The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proceedings of the National Academy of Sciences of the United States of America 99, 13920–13925.CrossRefGoogle Scholar
Martinez-Conde, S., Macknik, S.L., Troncoso, X.G. & Dyar, T.A. (2006). Microsaccades counteract fading during fixation. Neuron 49, 297–305.CrossRefGoogle Scholar
Navon, D. (1977). Forest before trees: The precedence of global features in visual perception. Cognitive Psychology 9, 353–383.CrossRefGoogle Scholar
Ölveczky, B.P., Baccus, S.A. & Meister, M. (2003). Segregation of object and background motion in the retina. Nature 423, 401–408.CrossRefGoogle Scholar
Parker, D.M., Lishman, J.R. & Hughes, J. (1992). Temporal integration of spatially filtered visual images. Perception 21, 147–60.CrossRefGoogle Scholar
Puchalla, J.L., Schneidman, E., Harris, R.A. & Berry, M.J. (2005). Redundancy in the population code of the retina. Neuron 46, 493–504.CrossRefGoogle Scholar
Ratliff, F. & Riggs, L.A. (1950). Involuntary motions of the eye during monocular fixation. Journal of Experimental Psychology 40, 687–701.CrossRefGoogle Scholar
Reid, R.C. & Shapley, R.M. (2002). Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus. Journal of Neuroscience 22, 6158–6175.Google Scholar
Riggs, L.A. & Ratliff, F. (1952). The effects of counteracting the normal movements of the eye. Journal of the Optical Society of America 42, 872–873.Google Scholar
Riggs, L.A., Ratliff, F., Cornsweet, J.C. & Cornsweet, T.N. (1953). The disappearance of steadily fixated visual test objects. Journal of the Optical Society of America 43, 495–501.CrossRefGoogle Scholar
Roelfsema, P.R., Lamme, V.A. & Spekreijse, H. (2004). Synchrony and covariation of firing rates in the primary visual cortex during contour grouping. Nature Neuroscience 7, 982–91.CrossRefGoogle Scholar
Rucci, M. & Casile, A. (2004). Decorrelation of neural activity during fixational instability: Possible implications for the refinement of V1 receptive fields. Visual Neuroscience 21, 725–738.CrossRefGoogle Scholar
Rucci, M. & Casile, A. (2005). Fixational instability and natural image statistics: Implications for early visual representations. Network: Computation in Neural Systems 16, 121–138.CrossRefGoogle Scholar
Rucci, M. & Desbordes, G. (2003). Contributions of fixational eye movements to the discrimination of briefly presented stimuli. Journal of Vision 3, 852–64.Google Scholar
Rucci, M., Edelman, G.M. & Wray, J. (2000). Modeling LGN responses during free-viewing: A possible role of microscopic eye movements in the refinement of cortical orientation selectivity. Journal of Neuroscience 20, 4708–4720.CrossRefGoogle Scholar
Ruderman, D.L. (1994). Statistics of natural images. Network: Computation in Neural Systems 5, 517–548.CrossRefGoogle Scholar
Schyns, P.G. & Oliva, A. (1994). From blobs to boundary edges: Evidence for time-and spatial-scale-dependent scene recognition. Psychological Science 5, 195–200.CrossRefGoogle Scholar
Shapley, R.M. & Victor, J.D. (1979). Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. Journal of Physiology (London) 290, 141–61.CrossRefGoogle Scholar
Singer, W. & Gray, C.M. (1995). Visual feature integration and the temporal correlation hypothesis. Annual Review of Neuroscience 18, 555–586.CrossRefGoogle Scholar
Skavenski, A.A., Hansen, R.M., Steinman, R.M. & Winterson, B.J. (1979). Quality of retinal image stabilization during small natural and artificial body rotations in man. Vision Research 19, 675–683.CrossRefGoogle Scholar
Snodderly, D.M. (1987). Effect of light and dark environments on macaque and human fixational eye movements. Vision Research 27, 401–415.CrossRefGoogle Scholar
Snodderly, D.M., Kagan, I. & Gur, M. (2001). Selective activation of visual cortex neurons by fixational eye movements: Implications for neural coding. Visual Neuroscience 18, 259–77.CrossRefGoogle Scholar
Snodderly, D.M. & Kurtz, D. (1985). Eye position during fixation tasks: Comparison of macaque and human. Vision Research 25, 83–98.CrossRefGoogle Scholar
Srinivasan, M.V., Laughlin, S.B. & Dubs, A. (1982). Predictive coding: A fresh view of inhibition in the retina. Proceedings of the Royal Society, Series B: Biological Sciences 216, 427–459.CrossRefGoogle Scholar
Steinman, R.M., Cunitz, R.J., Timberlake, G.T. & Herman, M. (1967). Voluntary control of microsaccades during maintained monocular fixation. Science 155, 1577–1579.CrossRefGoogle Scholar
Steinman, R.M., Haddad, G.M., Skavenski, A.A. & Wyman, D. (1973). Miniature eye movement. Science 181, 810–819.CrossRefGoogle Scholar
Steinman, R.M. & Levinson, J.Z. (1990). The role of eye movements in the detection of contrast and spatial detail. In Eye Movements and Their Role in Visual and Cognitive Processes, ed. Kowler & E., chapter 3, pp. 115–212. Elsevier Science Publishers BV.
Stevenson, S.B. & Roorda, A. (2005). Correcting for miniature eye movements in high resolution scanning laser ophthalmoscopy. In Ophthalmic Technologies XV, ed. Manns, F., Soderberg, P.G., Ho, A., Stuck, B.E. & Belkin, M., volume 5688 of Proceedings of SPIE, pp. 145–151. SPIE–The International Society for Optical Engineering, Bellingham, WA.
Tulunay-Keesey, Ü. & Jones, R.M. (1976). The effect of micromovements of the eye and exposure duration on contrast sensitivity. Vision Research 16, 481–488.CrossRefGoogle Scholar
Usrey, W.M. & Reid, R.C. (1999). Synchronous activity in the visual system. Annual Review of Physiology 61, 435–456.CrossRefGoogle Scholar
Usrey, W.M., Reppas, J.B. & Reid, R.C. (1998). Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 395, 384–387.CrossRefGoogle Scholar
van Hateren, J.H. (1992). A theory of maximizing sensory information. Biological Cybernetics 68, 23–29.CrossRefGoogle Scholar
van Hateren, J.H. & van der Schaaf, A. (1998). Independent component filters of natural images compared with simple cells in primary visual cortex. Proceedings of the Royal Society, Series B: Biological Sciences 265, 359–366.CrossRefGoogle Scholar
Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. Journal of Physiology (London) 386, 219–246.CrossRefGoogle Scholar