Layerwise complexity-matched learning yields an improved model of cortical area V2.

Human ability to recognize complex visual patterns arises through transformations performed by successive areas in the ventral visual cortex. Deep neural networks trained end-to-end for object recognition approach human capabilities, and offer the best descriptions to date of neural responses in the late stages of the hierarchy. But these networks provide a poor account of the early stages, compared to traditional hand-engineered models, or models optimized for coding efficiency or prediction. Moreover, the gradient backpropagation used in end-to-end learning is generally considered to be biologically implausible. Here, we overcome both of these limitations by developing a bottom-up self-supervised training methodology that operates independently on successive layers. Specifically, we maximize feature similarity between pairs of locally-deformed natural image patches, while decorrelating features across patches sampled from other images. Crucially, the deformation amplitudes are adjusted proportionally to receptive field sizes in each layer, thus matching the task complexity to the capacity at each stage of processing. In comparison with architecture-matched versions of previous models, we demonstrate that our layerwise complexity-matched learning (LCL) formulation produces a two-stage model (LCL-V2) that is better aligned with selectivity properties and neural activity in primate area V2. We demonstrate that the complexity-matched learning paradigm is responsible for much of the emergence of the improved biological alignment. Finally, when the two-stage model is used as a fixed front-end for a deep network trained to perform object recognition, the resultant model (LCL-V2Net) is significantly better than standard end-to-end self-supervised, supervised, and adversarially-trained models in terms of generalization to out-of-distribution tasks and alignment with human behavior.

How does V1 population activity inform perceptual certainty?

Neural population activity in sensory cortex informs our perceptual interpretation of the environment. Oftentimes, this population activity will support multiple alternative interpretations. The larger the spread of probability over different alternatives, the more uncertain the selected perceptual interpretation. We test the hypothesis that the reliability of perceptual interpretations can be revealed through simple transformations of sensory population activity. We recorded V1 population activity in fixating macaques while presenting oriented stimuli under different levels of nuisance variability and signal strength. We developed a decoding procedure to infer from V1 activity the most likely stimulus orientation as well as the certainty of this estimate. Our analysis shows that response magnitude, response dispersion, and variability in response gain all offer useful proxies for orientation certainty. Of these three metrics, the last one has the strongest association with the decoder's uncertainty estimates. These results clarify that the nature of neural population activity in sensory cortex provides downstream circuits with multiple options to assess the reliability of perceptual interpretations.

Primary visual cortex straightens natural video trajectories.

Many sensory-driven behaviors rely on predictions about future states of the environment. Visual input typically evolves along complex temporal trajectories that are difficult to extrapolate. We test the hypothesis that spatial processing mechanisms in the early visual system facilitate prediction by constructing neural representations that follow straighter temporal trajectories. We recorded V1 population activity in anesthetized macaques while presenting static frames taken from brief video clips, and developed a procedure to measure the curvature of the associated neural population trajectory. We found that V1 populations straighten naturally occurring image sequences, but entangle artificial sequences that contain unnatural temporal transformations. We show that these effects arise in part from computational mechanisms that underlie the stimulus selectivity of V1 cells. Together, our findings reveal that the early visual system uses a set of specialized computations to build representations that can support prediction in the natural environment.

Representation of visual uncertainty through neural gain variability.

Uncertainty is intrinsic to perception. Neural circuits which process sensory information must therefore also represent the reliability of this information. How they do so is a topic of debate. We propose a model of visual cortex in which average neural response strength encodes stimulus features, while cross-neuron variability in response gain encodes the uncertainty of these features. To test this model, we studied spiking activity of neurons in macaque V1 and V2 elicited by repeated presentations of stimuli whose uncertainty was manipulated in distinct ways. We show that gain variability of individual neurons is tuned to stimulus uncertainty, that this tuning is specific to the features encoded by these neurons and largely invariant to the source of uncertainty. We demonstrate that this behavior naturally arises from known gain-control mechanisms, and illustrate how downstream circuits can jointly decode stimulus features and their uncertainty from sensory population activity.

Perceptual straightening of natural videos.

Many behaviors rely on predictions derived from recent visual input, but the temporal evolution of those inputs is generally complex and difficult to extrapolate. We propose that the visual system transforms these inputs to follow straighter temporal trajectories. To test this 'temporal straightening' hypothesis, we develop a methodology for estimating the curvature of an internal trajectory from human perceptual judgments. We use this to test three distinct predictions: natural sequences that are highly curved in the space of pixel intensities should be substantially straighter perceptually; in contrast, artificial sequences that are straight in the intensity domain should be more curved perceptually; finally, naturalistic sequences that are straight in the intensity domain should be relatively less curved. Perceptual data validate all three predictions, as do population models of the early visual system, providing evidence that the visual system specifically straightens natural videos, offering a solution for tasks that rely on prediction.

Author Correction: Perceptual straightening of natural videos.

The original and corrected figures are shown in the accompanying Author Correction.