V1 neurons encode the perceptual compensation of false torsion arising from Listing’s law

Significance Eye movements have three degrees of freedom, the ability to move horizontally, vertically, and torsionally. Eye movements serving the fovea strictly control eye torsion. The amount of torsion associated with a particular eye position is specified by Listing’s law. Because of prior knowledge of the torsion set by Listing’s law, we perceive the world as upright although its retinal image may be tilted by varying degrees. We first show that also monkeys use a torsion prior to ensure a veridical perceptual reinterpretation of image tilt. We then demonstrate that this reinterpretation is a consequence of the fact that V1 neurons use the torsion prior to adjust their orientation preferences and to reposition their receptive fields relative to the retina. We try to deploy the retinal fovea to optimally scrutinize an object of interest by directing our eyes to it. The horizontal and vertical components of eye positions acquired by goal-directed saccades are determined by the object’s location. However, the eccentric eye positions also involve a torsional component, which according to Donder’s law is fully determined by the two-dimensional (2D) eye position acquired. According to von Helmholtz, knowledge of the amount of torsion provided by Listing’s law, an extension of Donder’s law, alleviates the perceptual interpretation of the image tilt that changes with 2D eye position, a view supported by psychophysical experiments he pioneered. We address the question of where and how Listing’s law is implemented in the visual system and we show that neurons in monkey area V1 use knowledge of eye torsion to compensate the image tilt associated with specific eye positions as set by Listing’s law.