Distinct Functional Organizations for Processing Different Motion Signals in V1, V2, and V4 of Macaque

Abstract

Motion perception is qualitatively invariant across different objects and forms, namely, the same motion information can be conveyed by many different physical carriers, and it requires the processing of motion signals consisting of direction, speed, and axis or trajectory of motion defined by a moving object. Compared with the representation of orientation, the cortical processing of these different motion signals within the early ventral visual pathway of the primate remains poorly understood. Using drifting full-field noise stimuli and intrinsic optical imaging, along with cytochrome-oxidase staining, we found that the orientation domains in macaque V1, V2, and V4 that processed orientation signals also served to process motion signals associated with the axis and speed of motion. In contrast, direction domains within the thick stripes of V2 demonstrated preferences that were independent of motion speed. The population responses encoding the orientation and motion axis could be precisely reproduced by a spatiotemporal energy model. Thus, our observation of orientation domains with dual functions in V1, V2, and V4 directly support the notion that the linear representation of the temporal series of retinotopic activations may serve as another motion processing strategy in primate ventral visual pathway, contributing directly to fine form and motion analysis. Our findings further reveal that different types of motion information are differentially processed in parallel and segregated compartments within primate early visual cortices, before these motion features are fully combined in high-tier visual areas.

The Mechanism for Processing Random-Dot Motion at Various Speeds in Early Visual Cortices

“…We found the angular differences for direction were neither significantly changed with speed (p = 0.81, two-way ANOVA) nor with visual area (p = 0.27, two-way ANOVA). The average angular differences in direction were all below 30° in both areas across all speeds tested, suggesting that a similar pattern of differential direction maps is activated at different speeds [15]. This result was found to be caused by the subtraction method used for generating the differential direction maps and was next addressed by single-unit recording of direction-selective cells.…”

Catching the voltage gradient—asymmetric boost of cortical spread generates motion signals across visual cortex: a brief review with special thanks to Amiram Grinvald

“…The following emergence of cortical motion streaks indicates additional integration processes over time. 42,43,62,67,69,103 However, there are some disadvantages of the method worthy of discussion. From a purely technical point of view, besides being restricted to surface cortical regions, the method does not permit the use of freely moving subjects.…”

“…60,[63][64][65] In contrast, it has been shown that information about motion axes is still present across neuronal activity and can be extracted from motion streaks. [66][67][68][69][70] Thus, motion streaks may be analyzed unconsciously and separately over time [71][72][73][74] to contribute to further analysis such as form-from-motion at higher processing stages. 20,21,62,69,70,[75][76][77][78][79][80] Interactions mediated by propagating waves of cortical population activity across V1 have been demonstrated for a variety of mammalian species (for example, see Refs.…”

“…However, regardless of whether the propagating activity as reported here may directly subserve "perceptual knowledge" or initially "hidden" cortical analysis of motion, 71 any retinotopic encoding of motion further downstream through propagating waves must engage mechanisms that emerge from the topography of early cortical areas such as V1. 69,98 Indeed, characterizing human motion detectors in space-time coordinates 99 led to the discovery of a previously unknown brief increase in detector amplitude at motion onset. 100 The perceptual relevance of retinotopic encoding of motion trajectories in V1 (Ref.…”

Grand Research Plan for Neural Circuits of Emotion and Memory — Current status of neural circuit studies in China

“…As for the visual system, different types of motion information are differentially processed in parallel and segregated compartments within primate early visual cortices, before these motion features are fully combined in high-tier visual areas [6,7] . More plasticity and wider generalization in the amblyopic visual system has been found, thus providing a strong empirical and theoretical basis for perceptual learning as a potential treatment for amblyopia.…”