A theory of the influence of eye movements on the refinement of direction selectivity in the cat's primary visual cortex

Trends in Neurosciences

2015

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196

178

How is space represented in the visual system? At first glance, the answer to this fundamental question appears straightforward: spatial information is directly encoded in the locations of neurons within maps. This concept has long dominated visual neuroscience, leading to mainstream theories of how neurons encode information. However, an accumulation of evidence indicates that this purely spatial view is incomplete, and that even for static images, the representation is fundamentally spatiotemporal. The evidence for this new understanding centers on recent experimental findings concerning the functional role of fixational eye movements, the tiny movements humans and other species continually perform, even when attending to a single point. Here, we review some of these findings and discuss their functional implications.

Section: Figurementioning

confidence: 99%

The unsteady eye: an information-processing stage, not a bug

Trends in Neurosciences

2015

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196

178

“…In previous work, we have shown that eye drift profoundly reshapes visual input signals, redistributing the 0 Hz (DC) power of the external static stimulus to non-zero temporal frequencies on the retina (Casile and Rucci, 2006; Casile and Rucci, 2009; Kuang et al, 2012; Aytekin et al, 2014). These modulations appear to be used by humans for the fine spatial discrimination (Rucci et al, 2007; Boi et al, 2017; Ratnam et al, 2017), providing new support to the long-standing proposal that the visual system uses oculo-motor induced luminance fluctuations for encoding spatial information in a temporal format (see Rucci and Victor, 2015b and Rucci et al, 2018 for reviews).…”

Section: Introductionmentioning

confidence: 99%

Contrast sensitivity reveals an oculomotor strategy for temporally encoding space

Casile

2019

eLife

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The contrast sensitivity function (CSF), how sensitivity varies with the frequency of the stimulus, is a fundamental assessment of visual performance. The CSF is generally assumed to be determined by low-level sensory processes. However, the spatial sensitivities of neurons in the early visual pathways, as measured in experiments with immobilized eyes, diverge from psychophysical CSF measurements in primates. Under natural viewing conditions, as in typical psychophysical measurements, humans continually move their eyes even when looking at a fixed point. Here, we show that the resulting transformation of the spatial scene into temporal modulations on the retina constitutes a processing stage that reconciles human CSF and the response characteristics of retinal ganglion cells under a broad range of conditions. Our findings suggest a fundamental integration between perception and action: eye movements work synergistically with the spatio-temporal sensitivities of retinal neurons to encode spatial information.

Contrast sensitivity reveals an oculomotor strategy for temporally encoding space

Casile

2018

Preprint

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The contrast sensitivity function (CSF), how sensitivity varies with the spatial frequency 12 of the stimulus, is a fundamental assessment of visual performance. The CSF is generally assumed 13 to be determined by low-level sensory processes. However, the sensitivities of neurons in the early 14 visual pathways, as measured in experiments with immobilized eyes, diverge from psychophysical 15 CSF measurements in primates. Under natural viewing conditions, as in typical psychophysical 16 measurements, humans continually move their eyes, drifting in a seemingly erratic manner even 17 when looking at a fixed point. Here, we show that the resulting transformation of the visual scene 18 into a spatiotemporal flow on the retina constitutes a processing stage that reconciles human CSF 19 and the response characteristics of retinal ganglion cells under a broad range of conditions. Our 20 findings suggest a fundamental integration between perception and action: eye movements work 21 synergistically with the sensitivities of retinal neurons to encode spatial information. 22 23 30 conditions, the CSF measured with stationary gratings exhibits a well-known band-pass shape that 31 typically peaks around 3-5 cycles/deg and sharply declines at higher and lower spatial frequencies. 32 The mechanisms responsible for this dependence on spatial frequency are not fully understood. 33 At high spatial frequency, a decline in sensitivity is expected for several reasons, including the 34 filtering of the eyes' optics (Campbell and Green, 1965) and the spatial limits in sampling imposed 35 by the cone mosaic on the retina (Hirsch and Miller, 1987; Rossi and Roorda, 2010). At low spatial 36 frequencies, however, the reasons for a reduced sensitivity have remained less clear. 37 A popular theory directly links the low-frequency attenuation in visual sensitivity to the neural 38 mechanisms of early visual encoding (Atick and Redlich, 1990, 1992). Building on theories of 39 efficient coding (Barlow, 1961), it has been argued that this attenuation reflects a form of matching 40 1 of 18 Manuscript submitted to eLife between the characteristics of the natural visual world and the response tuning of neurons in the 41 retina: retinal ganglion cells (henceforth RGCs) respond less strongly at low spatial frequencies so 42 as to counterbalance the spectral distribution of natural scenes. According to this proposal, this 43 filtering eliminates part of the redundancy intrinsic in natural scenes and enables more efficient 44 (i.e., more compact) visual representations. 45 Although very influential, this proposal conflicts with experimental data. Neurophysiological 46 recordings have long shown that the way the responses of retinal ganglion cells vary with spatial 47 frequency deviates sharply from the CSF. The CSF of macaques is very similar to that of humans (De 48 Valois et al., 1974); yet neurons in the macaque retina respond much more strongly at low spatial 49 frequencies than one would expect from behavioral me...