Optic flow parsing in the macaque monkey

Abstract

During self-motion, an independently moving object generates retinal motion that is the vector sum of its world-relative motion and the optic flow caused by the observer's self-motion. A hypothesized mechanism for the computation of an object's world-relative motion is flow parsing, in which the optic flow field due to self-motion is globally subtracted from the retinal flow field. This subtraction generates a bias in perceived object direction (in retinal coordinates) away from the optic flow vector at the object's location. Despite psychophysical evidence for flow parsing in humans, the neural mechanisms underlying the process are unknown. To build the framework for investigation of the neural basis of flow parsing, we trained macaque monkeys to discriminate the direction of a moving object in the presence of optic flow simulating self-motion. Like humans, monkeys showed biases in object direction perception consistent with subtraction of background optic flow attributable to self-motion. The size of perceptual biases generally depended on the magnitude of the expected optic flow vector at the location of the object, which was contingent on object position and self-motion velocity. There was a modest effect of an object's depth on flow-parsing biases, which reached significance in only one of two subjects. Adding vestibular self-motion signals to optic flow facilitated flow parsing, increasing biases in direction perception. Our findings indicate that monkeys exhibit perceptual hallmarks of flow parsing, setting the stage for the examination of the neural mechanisms underlying this phenomenon.

A neural mechanism for detecting object motion during self-motion

“…We have recently demonstrated flow parsing in macaque monkeys ( Peltier et al, 2020 ), including the observation that optic flow in one visual hemi-field can influence perception of object direction in the opposite hemi-field, as demonstrated previously in humans ( Warren and Rushton, 2009b ). These observations imply a global contribution to flow parsing, as might be implemented through feedback from the dorsal subdivision of the medial superior temporal area (MSTd) ( Layton and Fajen, 2016b ; Layton and Fajen, 2020 ).…”

“…Several studies Warren and Rushton, 2007 ; Warren and Rushton, 2008 ; Warren and Rushton, 2009a ; Warren et al, 2012 ; Foulkes et al, 2013 ; Rushton et al, 2018 have provided strong behavioral support for the flow-parsing hypothesis in humans, including some which suggest strongly that it involves a global motion process ( Warren and Rushton, 2009b ). In addition, a recent study has demonstrated flow parsing in macaque monkeys ( Peltier et al, 2020 ). If flow parsing completely discounts background motion due to self-motion, then the computations for detecting scene-relative object motion would be greatly simplified and would be essentially the same as when there is no self-motion.…”

“…However, flow parsing alone may not be sufficient to detect scene-relative object motion. Recent evidence ( Niehorster and Li, 2017 ; Peltier et al, 2020 ) indicates that the gain of flow parsing can be well below unity, such that background motion is only partially discounted. In this case, the output of a flow-parsing mechanism may not be sufficient to detect scene-relative object motion, and a mechanism such as we found in area MT would be valuable.…”

“…Because this mechanism relies on sensitivity to local discrepancies between disparity and motion parallax cues, it allows detection of object motion without the need for more complex computations that discount the global flow field. Thus, this local mechanism may be relatively economical for the nervous system to implement and likely provides a complementary approach to mechanisms for computing scene-relative object motion based on optic flow parsing ( Rushton and Warren, 2005 ; Warren and Rushton, 2008 ; Warren and Rushton, 2009b , a; Layton and Fajen, 2016b ; Niehorster and Li, 2017 ; Layton and Niehorster, 2019 ; Layton and Fajen, 2020 ; Peltier et al, 2020 ).…”

Causal contribution of optic flow signal in Macaque extrastriate visual cortex for roll perception

“…Note though, that MSTd also contains another large population of incongruent neurons with nearly opposite heading preference based on vestibular and that simulated from optic flow. It has been hypothesized that different populations of neurons in MSTd with either visuo-vestibular congruent or conflict relations could be used to segregate independent object-motion from self-motion 93 – 97 .…”