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Active vision at the foveal scale in the primate superior colliculus

Journal

JOURNAL OF NEUROPHYSIOLOGY
Volume 125, Issue 4, Pages 1121-1138

Publisher

AMER PHYSIOLOGICAL SOC
DOI: 10.1152/jn.00724.2020

Keywords

active vision; fixational eye movements; foveal vision; microsaccades; superior colliculus

Funding

  1. Deutsche Forschungsgemeinschaft (DFG) [276693517 -SFB 1233, BO5681/1-1, HA6749/4-1, 20K22684]
  2. JSPS, Japan

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The primate superior colliculus plays a crucial role in small eye movements and visual processing, particularly at the foveal scale. It integrates visual and movement signals, regulates eye positioning and microeye movements, while also showing sensitivity enhancement and suppression effects in the periphery.
The primate superior colliculus (SC) has recently been shown to possess both a large foveal representation as well as a varied visual processing repertoire. This structure is also known to contribute to eye movement generation. Here, we describe our current understanding of how SC visual and movement-related signals interact within the realm of small eye movements associated with the foveal scale of visuomotor behavior. Within the SC's foveal representation, there is a full spectrum of visual, visualmotor, and motor-related discharge for fixational eye movements. Moreover, a substantial number of neurons only emit movement-related discharge when microsaccades are visually guided, but not when similar movements are generated toward a blank. This represents a particularly striking example of integrating vision and action at the foveal scale. Beyond that, SC visual responses themselves are strongly modulated, and in multiple ways, by the occurrence of small eye movements. Intriguingly, this impact can extend to eccentricities well beyond the fovea, causing both sensitivity enhancement and suppression in the periphery. Because of large foveal magnification of neural tissue, such long-range eccentricity effects are neurally warped into smaller differences in anatomical space, providing a structural means for linking peripheral and foveal visual modulations around fixational eye movements. Finally, even the retinal-image visual flows associated with tiny fixational eye movements are signaled fairly faithfully by peripheral SC neurons with relatively large receptive fields. These results demonstrate how studying active vision at the foveal scale represents an opportunity for understanding primate vision during natural behaviors involving ever-present foveating eye movements.

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