Retinal stabilization reveals limited influence of extraretinal signals on heading tuning in the medial superior temporal area

Abstract

Heading perception in primates depends heavily on visual optic-flow cues. Yet during self-motion, heading percepts remain stable even though smooth-pursuit eye movements often distort optic flow. Electrophysiological studies have identified visual areas in monkey cortex, including the dorsal medial superior temporal area (MSTd), that signal the true heading direction during pursuit. According to theoretical work, self-motion can be represented accurately by compensating for these distortions in two ways: via retinal mechanisms or via extraretinal efference-copy signals, which predict the sensory consequences of movement. Psychophysical evidence strongly supports the efference-copy hypothesis, but physiological evidence remains inconclusive. Neurons that signal the true heading direction during pursuit are found in visual areas of monkey cortex, including the dorsal medial superior temporal area (MSTd). Here we measured heading tuning in MSTd using a novel stimulus paradigm, in which we stabilize the optic-flow stimulus on the retina during pursuit. This approach isolates the effects on neuronal heading preferences of extraretinal signals, which remain active while the retinal stimulus is prevented from changing.Our results demonstrate a significant but small influence of extraretinal signals on the preferred heading directions of MSTd neurons. Under our stimulus conditions, which are rich in retinal cues, we find that retinal mechanisms dominate physiological corrections for pursuit eye movements, suggesting that extraretinal cues, such as predictive efference-copy mechanisms, have a limited role under naturalistic conditions. Significance StatementSensory systems discount stimulation caused by the animal's own behavior. For example, eye movements cause irrelevant retinal signals that could interfere with motion perception. The visual system compensates for such self-generated motion, but how this happens is unclear. Two theoretical possibilities are a purely visual calculation or one using an internal signal of eye movements to compensate for their effects. Such a signal can be isolated by experimentally stabilizing the image on a moving retina, but this approach has never been adopted to study motion physiology. Using this method, we find that eyemovement signals have little influence on neural activity in visual cortex, while feed-forward visual calculation has a strong effect and is likely important under real-world conditions. Neurophysiological evidence for retinal versus extraretinal mechanisms in self-motion processing is mixed. Neural responses in heading-selective areas like dorsal medial superior temporal area (MSTd) compensate for changes in the speed (Inaba et al., 2007; Chukoskie and Movshon, 2009) and direction of optic flow during smooth pursuit. Two classic studies reported a large extraretinal influence on the heading-direction preferences of MSTd neurons

The Effects of Depth Cues and Vestibular Translation Signals on the Rotation Tolerance of Heading Tuning in Macaque Area MSTd

“…5,7). A similarly broad range of rotation tolerance has been observed in previous studies of rotation compensation in MSTd (Yang and Gu, 2017;Manning and Britten, 2019) and VIP (Sunkara et al, 2015). Since the problem that eye rotation poses on the visual system is at least partially solved at the level of human behavior (Warren and Hannon, 1988;Royden et al, 1992), rotation compensation may be solved progressively in the brain at the systems level or, perhaps, complete rotation compensation in visual neurons is not necessary to guide behavior (Cutting et al, 1992).…”

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.…”

Retinal optic flow during natural locomotion

“…Video 3 and 12). Interestingly, although neurons in both MST and VIP signal heading, they do not strongly discriminate between the retinal patterns generated by simulated, as opposed to real, eye movements (Sunkara et al, 2015;Manning & Britten, 2019).…”