Joint representation of translational and rotational components of optic flow in parietal cortex

Abstract

Terrestrial navigation naturally involves translations within the horizontal plane and eye rotations about a vertical (yaw) axis to track and fixate targets of interest. Neurons in the macaque ventral intraparietal (VIP) area are known to represent heading (the direction of selftranslation) from optic flow in a manner that is tolerant to rotational visual cues generated during pursuit eye movements. Previous studies have also reported that eye rotations modulate the response gain of heading tuning curves in VIP neurons. We tested the hypothesis that VIP neurons simultaneously represent both heading and horizontal (yaw) eye rotation velocity by measuring heading tuning curves for a range of rotational velocities of either real or simulated eye movements. Three findings support the hypothesis of a joint representation. First, we show that rotation velocity selectivity based on gain modulations of visual heading tuning is similar to that measured during pure rotations. Second, gain modulations of heading tuning are similar for self-generated eye rotations and visually simulated rotations, indicating that the representation of rotation velocity in VIP is multimodal, driven by both visual and extraretinal signals. Third, we show that roughly one-half of VIP neurons jointly represent heading and rotation velocity in a multiplicatively separable manner. These results provide the first evidence, to our knowledge, for a joint representation of translation direction and rotation velocity in parietal cortex and show that rotation velocity can be represented based on visual cues, even in the absence of efference copy signals.self-motion | optic flow | rotation | heading | ventral intraparietal area A s we navigate through the world, our motion can be described as combinations of translations (T) and rotations (R). Patterns of image motion associated with T and R are added together in the retinal flow field during navigation (Fig. 1A). The rotational component of self-motion can arise from a variety of sources, including eye, head, and body rotations as well as traveling along a curved path. Hence, to perform specific tasks, we may need to estimate our translation, rotation, or both. One way that this could be accomplished is by decomposing optic flow into its translational and rotational components (1-6).Information about rotational velocity is necessary for navigational tasks, such as interpreting optic flow to deduce the instantaneous direction of translation in the presence of eye (or head/ body) rotations, estimating the velocity of a tracked object, and determining the curvature of one's trajectory. Despite the importance of representing rotation velocity during self-motion, many psychophysical and electrophysiological studies have mainly considered rotations as something to be "subtracted out" to estimate our direction of translation (5,(7)(8)(9)(10)(11)(12). These studies have shown that the visual system can represent translations with tolerance to rotation but do not address the question of representing rotation in...

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

“…Alternatively, other groups proposed retinal slip is separated from flow due to selfmotion by combining tuning shifts with gain modulation of neuronal responses (Beintema and van den Berg, 1998). Analysis of single-unit responses in VIP to flow patterns with different combinations of translational and rotational components revealed that some cells showed joint, inseparable tuning for specific combinations (Sunkara et al, 2016). These responses were similar to those seen in real pursuit, suggesting that VIP simultaneously represents both the distorted retinal flow pattern and the veridical heading, which could be extracted by a downstream area.…”

Gravity estimation and verticality perception

“…For example, large-field angular visual motion heavily biases SVV and elicits abnormally large postural sway in patients with spinocerebellar ataxia type 6 (Bunn et al, 2015; Dakin et al, 2018). Neural representations of large-field angular visual motion, which may contribute to head orientation estimates, have been identified in multiple brain regions of monkeys, including the cerebellum (Kano et al, 1990, 1991), brainstem (Waespe and Henn, 1977), and ventral intraparietal area (Sunkara et al, 2016). The semi-circular canals (Fig.…”

Coordinated Control of Three-Dimensional Components of Smooth Pursuit to Rotating and Translating Textures

“…48 Areas MT and MST also have reciprocal connections with ventral intraparietal area (VIP), a site that contributes to pursuit 49 and combines translational and rotational components of self-motion. 19 …”

“…18 On the other hand, recent studies have shown coupling of translational and rotational components of optic flow stimuli in brain areas that are also involved with pursuit, such as ventral intraparietal area (VIP). 19 Here we propose that pursuit is a fully three-dimensional task that utilizes all three degrees of freedom of the eye's rotation, including torsion. We will refer to this as ''texture pursuit'' and refer to the classical experimental paradigm, utilizing stimuli without significant spatial extent (and hence without detectable rotation), as ''point pursuit.''…”