Rapid assessment of natural visual motion integration across primate species

Our visual environment is highly dynamic and marked by continuous change. The ability to see moving objects and to interact with them is a fundamental visual skill critical for survival. Many animals rely on visual motion to capture prey or to avoid predators. In humans, visual motion perception is at the heart of daily activities such as driving a car. Since the mid-19th century, a wealth of research has helped characterize humans’ behavioral response to visual motion and elucidated the workings of the brain when viewing moving objects. Psychologists and neuroscientists have developed experimental paradigms to probe responses to visual motion, assessed with a large portfolio of techniques ranging from behavioral (psychophysical) tests, neuronal recordings, and functional magnetic resonance imaging to optogenetics. However, many of these studies used simple visual stimuli such as single dots, multiple moving dots (random dot patterns), or textures with different motion components (e.g., sine-wave gratings, Gabor patterns, and plaids). Without doubt, such synthetic stimuli are powerful in terms of affording experimenter control and limiting observed behavior to the dimension under study. However, they do not capture the dynamics and richness of our visual environment. The PNAS paper by Knoll et al. (1) introduces a highly original paradigm that allows us to assess spatiotemporal integration of visual motion information using eye movements, a continuous natural response. The authors tested three primate species (humans, macaques, and marmosets), who viewed a large display of continuously moving dots, forming an optic flow field that occupied most of the observers’ visual field. These dots moved toward or away from one point in the field [termed the focus of expansion (FOE)]. Dot velocity increased with distance from the FOE. Even though the dot field is a reduced and simplified version of what we experience … [↵][1]1To whom correspondence should be addressed. Email: mspering{at}mail.ubc.ca. [1]: #xref-corresp-1-1

[1]  Thaddeus B. Czuba,et al.  Binocular Mechanisms of 3D Motion Processing. , 2017, Annual review of vision science.

[2]  L. Lagasse,et al.  Global motion perception is independent from contrast sensitivity for coherent motion direction discrimination and visual acuity in 4.5-year-old children , 2015, Vision Research.

[3]  J. Gibson Visually controlled locomotion and visual orientation in animals. , 1998, British journal of psychology.

[4]  B. Borghuis,et al.  The Role of Motion Extrapolation in Amphibian Prey Capture , 2015, The Journal of Neuroscience.

[5]  David A. Leopold,et al.  The marmoset monkey as a model for visual neuroscience , 2015, Neuroscience Research.

[6]  Roslyn Dakin,et al.  Visual guidance of forward flight in hummingbirds reveals control based on image features instead of pattern velocity , 2016, Proceedings of the National Academy of Sciences.

[7]  G. Rhodes,et al.  Sex-specific norms code face identity. , 2011, Journal of vision.

[8]  Mary M. Hayhoe,et al.  Gaze and the Control of Foot Placement When Walking in Natural Terrain , 2018, Current Biology.

[9]  Kathryn Bonnen,et al.  Beyond Trial-Based Paradigms: Continuous Behavior, Ongoing Neural Activity, and Natural Stimuli , 2018, The Journal of Neuroscience.

[10]  W. Warren Collective Motion in Human Crowds , 2018, Current directions in psychological science.

[11]  Catherine Boden,et al.  Deficient motion perception in the fellow eye of amblyopic children , 2005, Vision Research.

[12]  J. Gibson Visually controlled locomotion and visual orientation in animals , 2009 .

[13]  D. Bradley,et al.  Structure and function of visual area MT. , 2005, Annual review of neuroscience.

[14]  Alexander C. Huk,et al.  Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context , 2018, Proceedings of the National Academy of Sciences.

[15]  Alexander C. Schütz,et al.  Eye movements and perception: a selective review. , 2011, Journal of vision.

[16]  M. Land Motion and vision: why animals move their eyes , 1999, Journal of Comparative Physiology A.

[17]  A. Montagnini,et al.  Do we track what we see? Common versus independent processing for motion perception and smooth pursuit eye movements: A review , 2011, Vision Research.

[18]  Kevin J. Riggs,et al.  Motion processing in autism: evidence for a dorsal stream deficiency , 2000, Neuroreport.