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We have recently shown that fixational eye movements improve discrimination of the orientation of a high spatial frequency grating masked by low-frequency noise, but do not help with a low-frequency grating masked by high-frequency noise (M. Rucci, R. Iovin, M. Poletti, & F. Santini, 2007). In this study, we explored the neural mechanisms responsible for this phenomenon. Models of parvocellular ganglion cells were stimulated by the same visual input experienced by subjects in our psychophysical experiments, i.e., the spatiotemporal signals resulting from viewing stimuli during eye movements. We show that the spatial organization of correlated activity in the model predicts the subjects' performance in the experiments. During viewing of high-frequency gratings, fixational eye movements modulated the responses of modeled neurons in a way that depended on the relative alignment of cell receptive fields. Responses covaried strongly only when receptive fields were aligned parallel to the grating's orientation. Such a dependence on the axis of receptive-field alignment did not occur during viewing of low-frequency gratings. In this case, the responses of cells on the parallel and orthogonal axes were similarly affected by eye movements. These results support a role for oculomotor synchronization of neural activity in the representation of visual information in the retina.
We have recently shown that fixational eye movements improve discrimination of the orientation of a high spatial frequency grating masked by low-frequency noise, but do not help with a low-frequency grating masked by high-frequency noise (M. Rucci, R. Iovin, M. Poletti, & F. Santini, 2007). In this study, we explored the neural mechanisms responsible for this phenomenon. Models of parvocellular ganglion cells were stimulated by the same visual input experienced by subjects in our psychophysical experiments, i.e., the spatiotemporal signals resulting from viewing stimuli during eye movements. We show that the spatial organization of correlated activity in the model predicts the subjects' performance in the experiments. During viewing of high-frequency gratings, fixational eye movements modulated the responses of modeled neurons in a way that depended on the relative alignment of cell receptive fields. Responses covaried strongly only when receptive fields were aligned parallel to the grating's orientation. Such a dependence on the axis of receptive-field alignment did not occur during viewing of low-frequency gratings. In this case, the responses of cells on the parallel and orthogonal axes were similarly affected by eye movements. These results support a role for oculomotor synchronization of neural activity in the representation of visual information in the retina.
A recent theory posits that ocular drifts of fixational eye movements serve to reformat the visual input of natural images, so that the power of the input image is equalized across a range of spatial frequencies. This "spectral whitening" effect is postulated to improve the processing of high-spatial-frequency information and requires normal fixational eye movements. Given that people with macular disease exhibit abnormal fixational eye movements, do they also exhibit spectral whitening? To answer this question, we computed the power spectral density of movies of natural images translated in space and time according to the fixational eye movements (thus simulating the retinal input) of a group of observers with long-standing bilateral macular disease. Just as for people with normal vision, the power of the retinal input at low spatial frequencies was lower than that based on the 1/f 2 relationship, demonstrating spectral whitening. However, the amount of whitening was much less for observers with macular disease when compared with age-matched controls with normal vision. A mediation analysis showed that the eccentricity of the preferred retinal locus adopted by these observers and the characteristics of ocular drifts are important factors limiting the amount of whitening. Finally, we did not find a normal aging effect on spectral whitening. Although these findings alone cannot form a causal link between macular disease and spectral properties of eye movements, they suggest novel potential means of modifying the characteristics of fixational eye movements, which may in turn improve functional vision for people with macular disease.
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.
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