Temporal Coding of Visual Space
2018, Trends in Cognitive Sciences
https://doi.org/10.1016/J.TICS.2018.07.009Abstract
Establishing a representation of space is a major goal of sensory systems. Spatial information, however, is not always explicit in the incoming sensory signals. In most modalities it needs to be actively extracted from cues embedded in the temporal flow of receptor activation. Vision, on the other hand, starts with a sophisticated optical imaging system that explicitly preserves spatial information on the retina. This may lead to the assumption that vision is predominantly a spatial process: all that is needed is to transmit the retinal image to the cortex, like uploading a digital photograph, to establish a spatial map of the world. However, this deceptively simple analogy is inconsistent with theoretical models and experiments that study visual processing in the context of normal motor behavior. We argue here that, as with other senses, vision relies heavily on temporal strategies and temporal neural codes to extract and represent spatial information. Stable Visual Representations, but a Moving Visual Image Like a camera, the eye forms an image of the external scene on its posterior surface where the retina is located, with its dense mosaic of photoreceptor cells (see Glossary) that convert light into electrochemical signals. At each moment in time, all spatial information is present in the visual signals striking the photoreceptors, which explicitly encode space by their position within the retinal array. This camera model of the eye and the spatial coding idea have long dominated visual neuroscience. Although the specific reference frames of spatial representations (e.g., retinotopic vs spatiotopic) have been intensely debated [1,2], spatial information has always been assumed to originate from the receptor layout in the retina. Alas, the eye does not behave like a camera. While a photographer usually takes great care to ensure that the camera does not move, the eyes insist on moving continuously [3-6]. Humans perform rapid gaze shifts, known as saccades, 2-3 times per second. Even though models of the visual system often assume that the visual input is a stationary image during fixational pauses between successive saccades, small eye movements, known as fixational eye movements, continually occur. These movements displace the stimulus by considerable amounts on the retina, therefore continually changing the light signals striking the photoreceptors [7,8] (Box 1). Furthermore, unlike the film in a camera, the visual system depends on temporal transients. Neurons in the retina, thalamus, and later stages of the visual pathways respond strongly to temporal changes [9-13]. Visual percepts tend to fade away in the complete absence of temporal transients [14-17], and spatial changes that occur too slowly are not even detected by humans [18,19]. These considerations do not appear compatible with the standard idea that space is encoded solely by the position of neurons within spatial maps. They suggest that the visual system combines spatial sampling with temporal processing to extract and encode spatial information.
References (105)
- Burr, D.C. and Morrone, M.C. (2011) Spatiotopic coding and remapping in humans. Philos. Trans. R. Soc. B Biol. Sci. 366, 504-515
- Hall, N.J. and Colby, C.L. (2011) Remapping for visual stability. Philos. Trans. R. Soc. Lond. B Biol. Sci. 366, 528-539
- Barlow, H.B. (1952) Eye movements during fixation. J. Physiol. 116, 290-306
- Ratliff, F. and Riggs, L.A. (1950) Involuntary motions of the eye during monocular fixation. J. Exp. Psychol. 40, 687-701
- Ditchburn, R.W. (1973) Eye-Movements and Visual Perception, Oxford University Press
- Steinman, R.M. et al. (1973) Miniature eye movement. Science 181, 810-819
- Kowler, E. (2011) Eye movements: the past 25 years. Vision Res. 51, 1457-1483
- Rucci, M. and Poletti, M. (2015) Control and functions of fixa- tional eye movements. Annu. Rev. Vis. Sci. 1, 499-518
- Robson, J.G. (1966) Spatial and temporal contrast-sensitivity functions of the visual system. J. Opt. Soc. Am. 56, 1141
- Nagano, T. (1980) Temporal sensitivity of the human visual system to sinusoidal gratings. J. Opt. Soc. Am. 70, 711-716
- Breitmeyer, B. and Julesz, B. (1975) The role of on and off transients in determining the psychophysical spatial frequency response. Vision Res. 15, 411-415
- Benardete, E.A. and Kaplan, E. (1999) The dynamics of primate M retinal ganglion cells. Vis. Neurosci. 16, 355-368
- Benardete, E.A. and Kaplan, E. (1997) The receptive field of the primate P retinal ganglion cell. II. Nonlinear dynamics. Vis. Neurosci. 14, 187-205
- Troxler, I.P.V. (1804) Über das verschwinden gegebener gegen- stände innerhalb unseres gesichtskreises. Ophthalmol. Bibl. 2, 1-53
- Kelly, D.H. (1979) Motion and vision. I. Stabilized images of stationary gratings. J. Opt. Soc. Am. 69, 1266
- Poletti, M. and Rucci, M. (2010) Eye movements under various conditions of image fading. J. Vis. 10, 1-18
- Steinman, R.M. et al. (1985) Vision in the presence of known natural retinal image motion. J. Opt. Soc. Am. A 2, 226
- Rensink, R.A. (2002) Change detection. Annu. Rev. Psychol. 53, 245-277
- O'Regan, J.K. et al. (1999) Change-blindness as a result of 'mudsplashes'. Nature 398, 34
- Weymouth, F.W. et al. (1928) Visual acuity within the area centralis and its relation to eye movements and fixation. Am. J. Ophthalmol. 11, 947-960
- Jacobs, R.J. (1979) Visual resolution and contour interaction in the fovea and periphery. Vision Res. 19, 1187-1195
- Curcio, C.A. et al. (1990) Human photoreceptor topography. J. Comp. Neurol. 292, 497-523
- Poletti, M. et al. (2013) Microscopic eye movements compen- sate for nonhomogeneous vision within the fovea. Curr. Biol. 23, 1691-1695
- Poletti, M. et al. (2017) Selective attention within the foveola. Nat. Neurosci. 20, 1413-1417
- Ross, J. et al. (2001) Changes in visual perception at the time of saccades. Trends Neurosci. 24, 113-121
- Wurtz, R.H. (2008) Neuronal mechanisms of visual stability. Vision Res. 48, 2070-2089
- Westheimer, G. (2009) Hyperacuity. In Encyclopedia of Neuro- science (Squire, L.R., ed.), pp. 45-50, Academic Press
- Cherici, C. et al. (2012) Precision of sustained fixation in trained and untrained observers. J. Vis. 12, 31-31
- Barlow, H.B. (1957) Increment thresholds at low intensities considered as signal/noise discriminations. J. Physiol. 136, 469-488
- Burr, D.C. (1981) Temporal summation of moving images by the human visual system. Proc. R. Soc. London. Ser. B Biol. Sci. 211, 321-339
- Barlow, H.B. (1979) Reconstructing the visual image in space and time. Nature 279, 189-190
- Burr, D. (1980) Motion smear. Nature 284, 164-165
- Burak, Y. et al. (2010) Bayesian model of dynamic image stabili- zation in the visual system. Proc. Natl. Acad. Sci. U. S. A. 107, 19525-19530
- Packer, O. and Williams, D.R. (1992) Blurring by fixational eye movements. Vision Res. 32, 1931-1939
- Averill, H.L. and Weymouth, F.W. (1925) Visual perception and the retinal mosaic. II. The influence of eye-movements on the displacement threshold. J. Comp. Psychol. 5, 147-176
- Marshall, W.H. and Talbot, S.A. (1942) Recent evidence for neural mechanisms in vision leading to a general theory of sensory acuity. In Biological Symposia -Visual Mechanisms (Kluver, H., ed.), pp. 117-164, Jacques Cattel
- Rucci, M. and Victor, J.D. (2015) The unsteady eye: an informa- tion-processing stage, not a bug. Trends Neurosci. 38, 195-206
- Rucci, M. (2008) Fixational eye movements, natural image statistics, and fine spatial vision. Netw. Comput. Neural Syst. 19, 253-285
- Rucci, M. and Casile, A. (2005) Fixational instability and natural image statistics: implications for early visual representations. Netw. Comput. Neural Syst. 16, 121-138
- Ahissar, E. and Arieli, A. (2012) Seeing via miniature eye movements: a dynamic hypothesis for vision. Front. Comput. Neurosci. 6, 89
- Ahissar, E. and Arieli, A. (2001) Figuring space by time. Neuron 32, 185-201
- Burr, D.C. et al. (1986) Seeing objects in motion. Proc. R. Soc. London. Ser. B Biol. Sci. 227, 249-265
- Burr, D.C. (1979) Acuity for apparent Vernier offset. Vision Res. 19, 835-837
- Burr, D. and Ross, J. (1986) Visual processing of motion. Trends Neurosci. 9, 304-307
- Croner, L.J. and Kaplan, E. (1995) Receptive fields of P and M ganglion cells across the primate retina. Vision Res. 35, 7-24
- Kagan, I. et al. (2008) Saccades and drifts differentially modulate neuronal activity in V1: effects of retinal image motion, position, and extraretinal influences. J. Vis. 8, 19
- Derrington, A.M. and Lennie, P. (1984) Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J. Physiol. 357, 219-240
- Kuang, X. et al. (2012) Temporal encoding of spatial information during active visual fixation. Curr. Biol. 22, 510-514
- Field, D.J. (1987) Relations between the statistics of natural images and the response properties of cortical cells. J. Opt. Soc. Am. A 4, 2379
- Poletti, M. et al. (2015) Head-eye coordination at a microscopic scale. Curr. Biol. 25, 3253-3259
- Aytekin, M. et al. (2014) The visual input to the retina during natural head-free fixation. J. Neurosci. 34, 12701-12715
- Ko, H.-K. et al. (2010) Microsaccades precisely relocate gaze in a high visual acuity task. Nat. Neurosci. 13, 1549-1553
- Poletti, M. and Rucci, M. (2016) A compact field guide to the study of microsaccades: challenges and functions. Vision Res. 118, 83-97
- Kelly, D.H. (1981) Disappearance of stabilized chromatic gra- tings. Science 214, 1257-1258
- Santini, F. et al. (2007) EyeRIS: a general-purpose system for eye-movement-contingent display control. Behav. Res. Meth- ods 39, 350-364
- Rucci, M. et al. (2007) Miniature eye movements enhance fine spatial detail. Nature 447, 852-855
- Ratnam, K. et al. (2017) Benefits of retinal image motion at the limits of spatial vision. J. Vis. 17, 30
- Boi, M. et al. (2017) Consequences of the oculomotor cycle for the dynamics of perception. Curr. Biol. 27, 1268-1277
- Koenderink, J.J. (1972) Contrast enhancement and the negative afterimage. J. Opt. Soc. Am. 62, 685
- Tulunay-Keesey, U. (1982) Fading of stabilized retinal images. J. Opt. Soc. Am. 72, 440-447
- Kulikowski, J.J. and Tolhurst, D.J. (1973) Psychophysical evi- dence for sustained and transient detectors in human vision. J. Physiol. 232, 149-162
- Greschner, M. et al. (2002) Retinal ganglion cell synchronization by fixational eye movements improves feature estimation. Nat. Neurosci. 5, 341-347
- Krauzlis, R.J. et al. (2017) Neuronal control of fixation and fixa- tional eye movements. Philos. Trans. R. Soc. B Biol. Sci. 372, 20160205
- Leopold, D.A. and Logothetis, N.K. (1998) Microsaccades dif- ferentially modulate neural activity in the striate and extrastriate visual cortex. Exp. Brain Res. 123, 341-345
- Herrington, T.M. et al. (2009) The effect of microsaccades on the correlation between neural activity and behavior in middle tem- poral, ventral intraparietal, and lateral intraparietal areas. J. Neurosci. 29, 5793-5805
- Martinez-Conde, S. et al. (2004) The role of fixational eye move- ments in visual perception. Nat. Rev. Neurosci. 5, 229-240
- Ibbotson, M. and Krekelberg, B. (2011) Visual perception and saccadic eye movements. Curr. Opin. Neurobiol. 21, 553-558
- Segal, I.Y. et al. (2015) Decorrelation of retinal response to natural scenes by fixational eye movements. Proc. Natl. Acad. Sci. U. S. A. 112, 3110-3115
- Snodderly, D.M. et al. (2001) Selective activation of visual cortex neurons by fixational eye movements: implications for neural coding. Vis. Neurosci. 18, 259-277
- Gur, M. et al. (1997) Response variability of neurons in primary visual cortex (V1) of alert monkeys. J. Neurosci. 17, 2914-2920
- Snodderly, D.M. (2016) A physiological perspective on fixational eye movements. Vision Res. 118, 31-47
- Hafed, Z.M. et al. (2009) A neural mechanism for microsaccade generationintheprimatesuperiorcolliculus.Science323,940-943
- Chen, C.-Y. et al. (2015) Neuronal response gain enhancement prior to microsaccades. Curr. Biol. 25, 2065-2074
- Dan, Y. et al. (1998) Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nat. Neuro- sci. 1, 501-507
- Bruno, R.M. and Sakmann, B. (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312, 1622-1627
- Desbordes, G. and Rucci, M. (2007) A model of the dynamics of retinal activity during natural visual fixation. Vis. Neurosci. 24, 217-230
- Rucci, M. and Casile, A. (2004) Decorrelation of neural activity during fixational instability: possible implications for the refine- ment of V1 receptive fields. Vis. Neurosci. 21, 725-738
- Attneave, F. (1954) Some informational aspects of visual perception. Psychol. Rev. 61, 183-193
- Barlow, H.B. (2012) Possible principles underlying the trans- formations of sensory messages. In Sensory Communication (Rosenblith, W.A., ed.), pp. 216-234, MIT Press
- Atick, J.J. and Redlich, A.N. (1992) What does the retina know about natural scenes? Neural Comput. 4, 196-210
- Ahissar, E. et al. (2016) On the possible roles of microsaccades and drifts in visual perception. Vision Res. 118, 25-30
- Ahissar, E. (1998) Temporal-code to rate-code conversion by neuronal phase-locked loops. Neural Comput. 10, 597-650
- Ahissar, E. and Vaadia, E. (1990) Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. Proc. Natl. Acad. Sci. U. S. A. 87, 8935-8939
- Benedetto, A. and Morrone, M.C. (2017) Saccadic suppression Is embedded within extended oscillatory modulation of sensitiv- ity. J. Neurosci. 37, 3661-3670
- Bengi, H. and Thomas, J.G. (1973) Studies on human ocular tremor. In Perspectives in Biomedical Engineering (Kenedi, R. M., ed.), pp. 281-292, Palgrave Macmillan
- Herrmann, C.J.J. et al. (2017) A self-avoiding walk with neural delays as a model of fixational eye movements. Sci. Rep. 7, 12958
- Havermann, K. et al. (2014) Fine-scale plasticity of microscopic saccades. J. Neurosci. 34, 11665-11672
- Nachmias, J. (1961) Determiners of the drift of the eye during monocular fixation. J. Opt. Soc. Am. 51, 761-766
- Steinman, R.M. et al. (1995) Moveo ergo video: natural retinal image motion and its effect on vision. In Exploratory Vision: The Active Eye (Landy, M.S., ed.), pp. 3-50, Springer
- Legge, G.E. and Kersten, D. (1987) Contrast discrimination in peripheral vision. J. Opt. Soc. Am. A 4, 1594-1598
- Hansen, T. et al. (2009) Color perception in the intermediate periphery of the visual field. J. Vis. 9, 26-26
- Nandy, A.S. and Tjan, B.S. (2012) Saccade-confounded image statistics explain visual crowding. Nat. Neurosci. 15, 463-469
- Cornsweet, T.N. (1956) Determination of the stimuli for involuntary drifts and saccadic eye movements. J. Opt. Soc. Am. 46, 987
- Fiorentini, A. and Ercoles, A.M. (1966) Involuntary eye move- ments during attempted monocular fixation. Atti Fond. Giorgio Ronchi 21, 199-217
- Adler, F.H. and Fliegelman, M. (1934) Influence of fixation on the visual acuity. Arch. Ophthalmol. 12, 475-483
- Ezenman, M. et al. (1985) Power spectra for ocular drift and tremor. Vision Res. 25, 1635-1640
- Ko, H. et al. (2016) Eye movements between saccades: mea- suring ocular drift and tremor. Vision Res. 122, 93-104
- Skavenski, A.A. et al. (1979) Quality of retinal image stabilization during small natural and artificial body rotations in man. Vision Res. 19, 675-683
- Crick, F.H.C. et al. (1981) An information processing approach to understanding the visual cortex. In The Organization of the Cerebral Cortex (Schmitt, F.O., ed.), pp. 505-533, MIT Press
- Shapley, R. and Victor, J. (1986) Hyperacuity in cat retinal ganglion cells. Science 231, 999-1002
- Reichardt, W. (1957) Autokorrelationsauswertung als funktion- sprinzip des zentralnervensystems. Z. Naturforsch. 12, 447-457
- Adelson, E.H. and Bergen, J.R. (1985) Spatiotemporal energy models for the perception of motion. J. Opt. Soc. Am. A 2, 284-299
- Watson, A.B. and Ahumada, A.J. (1985) Model of human visual- motion sensing. J. Opt. Soc. Am. A 2, 322-341
- van Santen, J.P.H. and Sperling, G. (1985) Elaborated Reichardt detectors. J. Opt. Soc. Am. A 2, 300
- Burr, D. and Thompson, P. (2011) Motion psychophysics: 1985-2010. Vision Res. 51, 1431-1456