Visual selectivity for heading in the macaque ventral intraparietal area

Abstract

Kaminiarz A, Schlack A, Hoffmann KP, Lappe M, Bremmer F. Visual selectivity for heading in the macaque ventral intraparietal area. J Neurophysiol 112: 2470 -2480, 2014. First published August 13, 2014 doi:10.1152/jn.00410.2014.-The patterns of optic flow seen during self-motion can be used to determine the direction of one's own heading. Tracking eye movements which typically occur during everyday life alter this task since they add further retinal image motion and (predictably) distort the retinal flow pattern. Humans employ both visual and nonvisual (extraretinal) information to solve a heading task in such case. Likewise, it has been shown that neurons in the monkey medial superior temporal area (area MST) use both signals during the processing of self-motion information. In this article we report that neurons in the macaque ventral intraparietal area (area VIP) use visual information derived from the distorted flow patterns to encode heading during (simulated) eye movements. We recorded responses of VIP neurons to simple radial flow fields and to distorted flow fields that simulated self-motion plus eye movements. In 59% of the cases, cell responses compensated for the distortion and kept the same heading selectivity irrespective of different simulated eye movements. In addition, response modulations during real compared with simulated eye movements were smaller, being consistent with reafferent signaling involved in the processing of the visual consequences of eye movements in area VIP. We conclude that the motion selectivities found in area VIP, like those in area MST, provide a way to successfully analyze and use flow fields during self-motion and simultaneous tracking movements.self-motion; primate; parietal cortex; eye movements SELF-MOTION THROUGH AN ENVIRONMENT induces visual, vestibular, tactile, and auditory signals. Neurophysiological research over the last two decades has shown in the animal model, i.e., the macaque monkey, how these signals interact to enhance and disambiguate the perception of heading during self-motion. Two areas of the primate extrastriate and parietal cortex proved to be of specific importance in this context, i.e., the medial superior temporal area (area MST) and the ventral intraparietal area (area VIP). Neurons in area MST respond to visual and vestibular self-motion signals, and their causal role in heading perception has been confirmed (Bremmer et al.

Adaptive heading performance during self‐motion perception

“…However, these previous studies used stimuli containing insufficient visual cues (e.g., lack of depth cue), and this potentially undermined the retinal contributions. In particular, recent neurophysiologic studies using novel optic‐flow stimuli (with enriched visual cues, e.g., depth and perspective cues) have shown that the retinal mechanism played a dominate role in distortion compensation at the single‐neuron level (Bremmer, Kubischik, Pekel, Hoffmann, & Lappe, ; Kaminiarz, Schlack, Hoffmann, Lappe, & Bremmer, ; Manning & Britten, ; Sunkara, DeAngelis, & Angelaki, ). Our result of training‐induced improvement in self‐motion perception without actual eye movement appears to add a new twist to this retinal versus extraretinal debate.…”

Predictive coding in a multisensory path integration task: An fMRI study

“…In complex goal-directed sensorimotor tasks, such as self-motion, sensory stimuli are typically the consequence of one's own action. As an example, the visual optical flow arriving at the retina is the direct consequence of moving forward and hence is predictable (Kaminiarz et al, 2014). Accordingly, and in line with the predictive coding framework, optic flow responses during self-induced (visually simulated) selfmotion might be suppressed.…”

Multisensory Integration in Self Motion Perception

“…Nevertheless, perceptual performance could be further enhanced if single neurons were capable of deducing heading information from visual signals alone. Accordingly, in two recent studies, we investigated if neurons in areas MST and VIP can encode heading solely based on visual signals (Bremmer et al, 2010;Kaminiarz et al, 2014). More specifically, we asked if such neurons would keep their heading selectivity regardless of whether or not the retinal flow resulting from a simulated forward motion was disturbed by superimposed simulated eye movements of various gains.…”

“…All procedures were in accordance with published guidelines on the use of animals in research (European Communities Council Directive 86/609/ECC). Experimental methods followed standard procedures that were described in detail in (Bremmer et al, 2009(Bremmer et al, , 2010Morris et al, 2012, andKaminiarz et al, 2014). Optic flow stimuli were back projected onto a tangent screen (90° x 90°) 48 cm in front of the monkey and simulated self-motion of a virtual observer over an extended horizontal plane located 37cm below eye-level.…”