scholarly journals V1 neurons encode the perceptual compensation of “false torsion” arising from Listing’s law

2018 ◽  
Author(s):  
Mohammad Farhan Khazali ◽  
Peter Thier
Keyword(s):  
Eye Movements ◽  
Visual System ◽  
Eye Position ◽  
V1 Neurons ◽  
Listing's Law ◽  
Listing’S Law ◽  
Torsional Component

AbstractWe try to deploy the retinal fovea to optimally scrutinize an object of interest by directing our eyes to it. Horizontal and vertical components of these fixation eye movements are determined by the object’s location. However, fixation eye movements also involve a torsional component, which according to Listing’s law is fully determined by the 2D eye position acquired. According to Von Helmholtz knowledge of the torsion provided by this law alleviates the perceptual interpretation of the image tilt that changes with fixation, a view supported by psychophysical experiments he pioneered. We address the question where and how Listing’s law is implemented in the visual system and we show that neurons in monkey area V1 use knowledge of torsion to compensate the image tilt associated with specific eye positions as set by Listing’s law.

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

2020 ◽  
Vol 117 (31) ◽  
pp. 18799-18809
Author(s):  
Mohammad Farhan Khazali ◽  
Hamidreza Ramezanpour ◽  
Peter Thier
Keyword(s):  
Visual System ◽  
Eye Position ◽  
Two Dimensional ◽  
V1 Neurons ◽  
Listing's Law ◽  
Listing’S Law ◽  
Torsional Component ◽  
Eye Torsion

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.

Human Oculomotor System Accounts for 3-D Eye Orientation in the Visual-Motor Transformation for Saccades

1998 ◽  
Vol 80 (5) ◽  
pp. 2274-2294 ◽  
Author(s):  
Eliana M. Klier ◽  
J. Douglas Crawford
Keyword(s):  
Reference Frame ◽  
Oculomotor System ◽  
Gaze Direction ◽  
Eye Position ◽  
Look Up Table ◽  
Listing's Law ◽  
Listing’S Law ◽  
Reference Frame Transformation ◽  
Visual Motor ◽  
Frame Transformation

Klier, Eliana M. and J. Douglas Crawford. Human oculomotor system accounts for 3-D eye orientation in the visual-motor transformation for saccades. J. Neurophysiol. 80: 2274–2294, 1998. A recent theoretical investigation has demonstrated that three-dimensional (3-D) eye position dependencies in the geometry of retinal stimulation must be accounted for neurally (i.e., in a visuomotor reference frame transformation) if saccades are to be both accurate and obey Listing's law from all initial eye positions. Our goal was to determine whether the human saccade generator correctly implements this eye-to-head reference frame transformation (RFT), or if it approximates this function with a visuomotor look-up table (LT). Six head-fixed subjects participated in three experiments in complete darkness. We recorded 60° horizontal saccades between five parallel pairs of lights, over a vertical range of ±40° ( experiment 1), and 30° radial saccades from a central target, with the head upright or tilted 45° clockwise/counterclockwise to induce torsional ocular counterroll, under both binocular and monocular viewing conditions ( experiments 2 and 3). 3-D eye orientation and oculocentric target direction (i.e., retinal error) were computed from search coil signals in the right eye. Experiment 1: as predicted, retinal error was a nontrivial function of both target displacement in space and 3-D eye orientation (e.g., horizontally displaced targets could induce horizontal or oblique retinal errors, depending on eye position). These data were input to a 3-D visuomotor LT model, which implemented Listing's law, but predicted position-dependent errors in final gaze direction of up to 19.8°. Actual saccades obeyed Listing's law but did not show the predicted pattern of inaccuracies in final gaze direction, i.e., the slope of actual error, as a function of predicted error, was only −0.01 ± 0.14 (compared with 0 for RFT model and 1.0 for LT model), suggesting near-perfect compensation for eye position. Experiments 2 and 3: actual directional errors from initial torsional eye positions were only a fraction of those predicted by the LT model (e.g., 32% for clockwise and 33% for counterclockwise counterroll during binocular viewing). Furthermore, any residual errors were immediately reduced when visual feedback was provided during saccades. Thus, other than sporadic miscalibrations for torsion, saccades were accurate from all 3-D eye positions. We conclude that 1) the hypothesis of a visuomotor look-up table for saccades fails to account even for saccades made directly toward visual targets, but rather, 2) the oculomotor system takes 3-D eye orientation into account in a visuomotor reference frame transformation. This transformation is probably implemented physiologically between retinotopically organized saccade centers (in cortex and superior colliculus) and the brain stem burst generator.

Three-dimensional visuo-motor control of saccades

2013 ◽  
Vol 109 (1) ◽  
pp. 183-192 ◽  
Author(s):  
Bernhard J. M. Hess
Keyword(s):  
Motor Control ◽  
Reverse Engineering ◽  
Visual Information ◽  
Three Dimensional ◽  
Engineering Problem ◽  
Line Of Sight ◽  
Eye Position ◽  
Listing's Law ◽  
Saccade Onset ◽  
Listing’S Law

Although the motion of the line of sight is a straightforward consequence of a particular rotation of the eye, it is much trickier to predict the rotation underlying a particular motion of the line of sight in accordance with Listing's law. Helmholtz's notion of the direction-circle together with the notion of primary and secondary reference directions in visual space provide an elegant solution to this reverse engineering problem, which the brain is faced with whenever generating a saccade. To test whether these notions indeed apply for saccades, we analyzed three-dimensional eye movements recorded in four rhesus monkeys. We found that on average saccade trajectories closely matched with the associated direction-circles. Torsional, vertical, and horizontal eye position of saccades scattered around the position predicted by the associated direction-circles with standard deviations of 0.5°, 0.3°, and 0.4°, respectively. Comparison of saccade trajectories with the likewise predicted fixed-axis rotations yielded mean coefficients of determinations (±SD) of 0.72 (±0.26) for torsion, 0.97 (±0.10) for vertical, and 0.96 (±0.11) for horizontal eye position. Reverse engineering of three-dimensional saccadic rotations based on visual information suggests that motor control of saccades, compatible with Listing's law, not only uses information on the fixation directions at saccade onset and offset but also relies on the computation of secondary reference positions that vary from saccade to saccade.

Straight Lines, ‘Uncurved Lines’, and Helmholtz's ‘Great Circles on the Celestial Sphere’

Perception ◽  
10.1068/p5652 ◽  
2007 ◽  
Vol 36 (9) ◽  
pp. 1275-1289 ◽  
Author(s):  
Brian Rogers ◽  
Kenneth Brecher
Keyword(s):  
Visual System ◽  
Visual Space ◽  
Listing's Law ◽  
Lack Of Information ◽  
Listing’S Law ◽  
The World ◽  
Celestial Sphere ◽  
Straight Lines ◽  
Different Parts

Helmholtz's famous pincushioned chessboard figure has been used to make the point that straight lines in the world are not always perceived as straight and, conversely, that curved lines in the world can sometimes be seen as straight. However, there is little agreement as to the cause of these perceptual errors. Some authors have attributed the errors to the shape of the retina, or the amount of cortex devoted to the processing of images falling on different parts of the retina, while others have taken the effects to indicate that visual space itself is curved. Helmholtz himself claimed that the ‘uncurved lines on the visual globe’ corresponded to ‘direction circles’ defined as those arcs described by the line of fixation when the eye moves according to Listing's law. Careful re-reading of Helmholtz together with some additional observations lead us to the conclusion that two other factors are also involved in the effect: (i) a lack of information about the distance of peripherally viewed objects and (ii) the preference of the visual system for seeing the pincushion squares as similar in size.

scholarly journals Chameleon eye position obeys Listing's law

2001 ◽  
Vol 41 (17) ◽  
pp. 2245-2251 ◽  
Author(s):  
Peter S Sándor ◽  
Maarten A Frens ◽  
Volker Henn
Keyword(s):  
Eye Position ◽  
Listing's Law ◽  
Listing’S Law

scholarly journals Mice Make Targeted Saccades

2021 ◽  
Author(s):  
Sebastian H. Zahler ◽  
David E. Taylor ◽  
Julia M. Adams ◽  
Evan H. Feinberg
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Visual System ◽  
Neural Circuit ◽  
Saccadic Eye Movements ◽  
Eye Position ◽  
Innate Behavior ◽  
High Acuity ◽  
Early Origin ◽  
Innate Ability

AbstractHumans read text, recognize faces, and process emotions using targeted saccadic eye movements. In the textbook model, this innate ability to make targeted saccades evolved in species with foveae or similar high-acuity retinal specializations that enable scrutiny of salient stimuli. According to the model, saccades made by species without retinal specializations (such as mice) are never targeted and serve only to reset the eyes after gaze-stabilizing movements. Here we show that mice innately make touch-evoked targeted saccades. Optogenetic manipulations revealed the neural circuit mechanisms underlying targeted saccades are conserved. Saccade probability is a U-shaped function of current eye position relative to the target, mirroring the simulated relationship between an object’s location within the visual field and the probability its next movement carries it out of view. Thus, a cardinal sophistication of our visual system may have had an unexpectedly early origin as an innate behavior that keeps stimuli in view.

scholarly journals Revealing the Kinematics of the Oculomotor Plant With Tertiary Eye Positions and Ocular Counterroll

2011 ◽  
Vol 105 (2) ◽  
pp. 640-649 ◽  
Author(s):  
Eliana M. Klier ◽  
Hui Meng ◽  
Dora E. Angelaki
Keyword(s):  
Eye Movements ◽  
Degrees Of Freedom ◽  
Three Dimensional ◽  
Abducens Nerve ◽  
Oculomotor System ◽  
Primary Position ◽  
Listing's Law ◽  
Listing’S Law ◽  
Ocular Counterroll ◽  
Half Angle

Retinal information is two-dimensional, whereas eye movements are three-dimensional. The oculomotor system solves this degrees-of-freedom problem by constraining eye positions to zero torsion (Listing's law) and determining how eye velocities change with eye position (half-angle rule). Here we test whether the oculomotor plant, in the absence of well-defined neural commands, can implement these constrains mechanically, not just in a primary position but for all eye and head orientations. We stimulated the abducens nerve at tertiary eye positions and when ocular counterroll was induced at tilted head orientations. Stimulation-induced eye velocities follow the half-angle rule, even for tertiary eye positions, and microstimulation at tilted head orientations elicits eye positions that adhere to torsionally shifted planes, similar to naturally occurring eye movements. These results support the notion that oculomotor plant can continuously apply these three-dimensional rules correctly and appropriately for all eye and head orientations that obey Listing's law, demonstrating a major role of peripheral biomechanics in motor control.

scholarly journals Visual-Motor Transformations Required for Accurate and Kinematically Correct Saccades

1997 ◽  
Vol 78 (3) ◽  
pp. 1447-1467 ◽  
Author(s):  
J. Douglas Crawford ◽  
Daniel Guitton
Keyword(s):  
Reference Frame ◽  
Eye Position ◽  
Target Displacement ◽  
Listing's Law ◽  
Listing's Plane ◽  
Listing’S Law ◽  
Reference Frame Transformation ◽  
Visual Motor ◽  
Frame Transformation ◽  
Listing’S Plane

Crawford, J. Douglas and Daniel Guitton. Visual-motor transformations required for accurate and kinematically correct saccades. J. Neurophysiol. 78: 1447–1467, 1997. The goal of this study was to identify and model the three-dimensional (3-D) geometric transformations required for accurate saccades to distant visual targets from arbitrary initial eye positions. In abstract 2-D models, target displacement in space, retinal error (RE), and saccade vectors are trivially interchangeable. However, in real 3-D space, RE is a nontrivial function of objective target displacement and 3-D eye position. To determine the physiological implications of this, a visuomotor “lookup table” was modeled by mapping the horizontal/vertical components of RE onto the corresponding vector components of eye displacement in Listing's plane. This provided the motor error (ME) command for a 3-D displacement-feedback loop. The output of this loop controlled an oculomotor plant that mechanically implemented the position-dependent saccade axis tilts required for Listing's law. This model correctly maintained Listing's law but was unable to correct torsional position deviations from Listing's plane. Moreover, the model also generated systematic errors in saccade direction (as a function of eye position components orthogonal to RE), predicting errors in final gaze direction of up to 25° in the oculomotor range. Plant modifications could not solve these problems, because the intrisic oculomotor input-output geometry forced a fixed visuomotor mapping to choose between either accuracy or Listing's law. This was reflected internally by a sensorimotor divergence between input-defined visual displacement signals (inherently 2-D and defined in reference to the eye) and output-defined motor displacement signals (inherently 3-D and defined in reference to the head). These problems were solved by rotating RE by estimated 3-D eye position (i.e., a reference frame transformation), inputting the result into a 2-D–to–3-D “Listing's law operator,” and then finally subtracting initial 3-D eye position to yield the correct ME. This model was accurate and upheld Listing's law from all initial positions. Moreover, it suggested specific experiments to invasively distinguish visual and motor displacement codes, predicting a systematic position dependence in the directional tuning of RE versus a fixed-vector tuning in ME. We conclude that visual and motor displacement spaces are geometrically distinct such that a fixed visual-motor mapping will produce systematic and measurable behavioral errors. To avoid these errors, the brain would need to implement both a 3-D position-dependent reference frame transformation and nontrivial 2-D–to–3-D transformation. Furthermore, our simulations provide new experimental paradigms to invasively identify the physiological progression of these spatial transformations by reexamining the position-dependent geometry of displacement code directions in the superior colliculus, cerebellum, and various cortical visuomotor areas.

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