Chromatic and luminance processing during eye movements in human early visual cortex

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2025

Authors

Zhang, Yuan

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Karl Gegenfurtner, Karl
Dörschner-Boyaci, Katja
Kaiser, Daniel
Schuetz, Alexander

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DOI:
https://doi.org/10.22029/jlupub-20480

Abstract

Human vision is not a passive process. Rather, our visual perception of the world emerges from a dynamic and adaptive interplay between sensory input and motor action, whereby perception continually guides movements, and these movements in turn reshape perceptual experience. Eye movements are essential for acquiring clear visual input in natural viewing. Despite substantial progress in understanding how eye movements are generated, controlled, and functionally organized, fundamental questions remain about how early visual processing is modulated by natural viewing behaviors, and how different types of eye movements influence neural mechanisms encoding color and luminance. This dissertation addresses these questions by combining precise neurophysiological measurement techniques with carefully controlled behavioral paradigms. Our eyes move frequently to keep objects of interest projected onto the fovea for a clear image. Among these movements, saccades are rapid, ballistic shifts of gaze that move the eyes from one location to another, while smooth pursuit keeps a moving target within the foveal region through continuous, slow eye rotations that closely match the target’s speed and direction. When the gaze is relatively stable and directed at a single point, the eye is in a state of fixation. These three types of eye movements are fundamental for acquiring visual information from the environment. Visual scenes are encoded by the L, M, and S cones in the retina and then relayed via three pathways: the magnocellular pathway (L+M, luminance), the parvocellular pathway (L–M, red-green opponency), and the koniocellular pathway (S–[L+M], blue-yellow opponency). These pathways transmit information in parallel up to the primary visual cortex (V1), where their signals are subsequently processed through partially distinct yet interacting cortical circuits (for reviews, see Gegenfurtner, 2003; S. H. C. Hendry & Reid, 2000; Nassi & Callaway, 2009). Given that V1 is the first cortical site where luminance and chromatic signals converge and begin to interact, a key unresolved question is how these signals are modulated by different types of eye movements during natural viewing. To explore the neural mechanisms underlying these processes, this thesis employed steady-state visual evoked potentials (SSVEPs) to track neural responses in the early visual cortex. SSVEPs are brain oscillations elicited by periodic visual stimulation (Adrian & Matthews, 1934; for review, see Norcia et al., 2015), originating primarily from V1 (Di Russo et al., 2007; Müller et al., 1997). SSVEPs possess high temporal resolution and exhibit narrowband spectral responses locked precisely to the stimulation frequency, making them highly resistant to eye movement artifacts (e.g., J. Chen et al., 2017a, 2017b; J. Chen, Valsecchi, et al., 2019). Those properties make SSVEPs a reliable tool for studying visual processing in the human early visual cortex during eye movements. In Study 1, we investigated the effect of chromatic (L–M) adaptation during prolonged fixation. Results showed that SSVEP responses to chromatic stimuli progressively decrease as stimulation duration increased, following an exponential decay with a half-life of approximately 20 seconds. In contrast, responses to luminance stimuli did not show any systematic adaptation. After characterizing this sustained visual adaptation, Study 2 then investigated transient modulations of visual cortical responses induced by saccadic eye movements. Results demonstrated comparable saccadic suppression effects on SSVEP responses to both chromatic (L–M) and luminance stimuli. Further modeling of contrast response functions revealed that saccades selectively reduced response gain without altering contrast gain, suggesting that visual attenuation involves a multiplicative mechanism operating similarly within both the parvocellular and magnocellular pathways. To enhance the quality of SSVEP data, the third study evaluated various EEG referencing methods and introduced the Laplacian reference as an optimal strategy for signal derivation. Results showed that the Laplacian reference significantly improved the signal-to-noise ratio (SNR) and reliability of neural measurements, while also being straightforward to implement across different experimental settings. Taken together, these findings underscore the critical role of eye movements in modulating both luminance and chromatic signals within the early visual cortex. This work demonstrates that perception is dynamically shaped by the continuous interplay between sensory input and oculomotor behavior, offering new insights into how active vision operates under natural viewing conditions.

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