Rats spontaneously perceive global motion direction of drifting plaids

Author summary Inferring motion direction of visual objects is computationally challenging. This is because natural objects are made of multiple oriented features. Neurons in low-level visual areas, such as primary visual cortex (V1), can see only these local features through their small receptive fields. As a result, these neurons (known as component cells) will report the presence of many oriented edges, each moving along a direction that is orthogonal to the edge itself. How can the brain compute the global direction of the whole object from this cacophony of disparate, local motion signals? Decades of studies in primates have shown that neurons in downstream, higher-order visual areas (known as pattern cells) integrate and combine motion signals encoded by component cells to represent global motion direction of the whole object. Although pattern cells have also been found in rodent visual cortex, they are so few that it is unclear whether they can support perception of global motion. In our study, we showed that rats are indeed capable of perceiving global motion direction of complex visual patterns and we verified, through computer simulations, that this ability is consistent with the representation of motion information by a population of pattern cells.

Computing global motion direction of extended visual objects is a hallmark of primate high-level vision. Although neurons selective for global motion have also been found in mouse visual cortex, it remains unknown whether rodents can combine multiple motion signals into global, integrated percepts. To address this question, we trained two groups of rats to discriminate either gratings (G group) or plaids (i.e., superpositions of gratings with different orientations; P group) drifting horizontally along opposite directions. After the animals learned the task, we applied a visual priming paradigm, where presentation of the target stimulus was preceded by the brief presentation of either a grating or a plaid. The extent to which rat responses to the targets were biased by such prime stimuli provided a measure of the spontaneous, perceived similarity between primes and targets. We found that gratings and plaids, when uses as primes, were equally effective at biasing the perception of plaid direction for the rats of the P group. Conversely, for G group, only the gratings acted as effective prime stimuli, while the plaids failed to alter the perception of grating direction. To interpret these observations, we simulated a decision neuron reading out the representations of gratings and plaids, as conveyed by populations of either component or pattern cells (i.e., local or global motion detectors). We concluded that the findings for the P group are highly consistent with the existence of a population of pattern cells, playing a functional role similar to that demonstrated in primates. We also explored different scenarios that could explain the failure of the plaid stimuli to elicit a sizable priming magnitude for the G group. These simulations yielded testable predictions about the properties of motion representations in rodent visual cortex at the single-cell and circuitry level, thus paving the way to future neurophysiology experiments.

Automated summary

Inferring motion direction of visual objects is challenging due to multiple oriented features in natural objects. While neurons in low-level visual areas detect local features, higher-order visual areas integrate motion signals to represent global motion direction. Our study with rats demonstrated their ability to perceive global motion direction of complex visual patterns, consistent with representation by pattern cells.