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Some of the most important tasks of visual and motor systems involve estimating the motion of objects and tracking them over time. Such systems evolved to meet the behavioral needs of the organism in its natural environment, and may therefore be adapted to the statistics of motion it is likely to encounter. By tracking the movement of individual points in movies of natural scenes, we begin to identify common properties of natural motion across scenes. As expected, objects in natural scenes move in a persistent fashion, with velocity correlations lasting hundreds of milliseconds. More subtly, but crucially, we find that the observed velocity distributions are heavy-tailed and can be modeled as a Gaussian scale-mixture. Extending this model to the time domain leads to a dynamic scale-mixture model, consisting of a Gaussian process multiplied by a positive scalar quantity with its own independent dynamics. Dynamic scaling of velocity arises naturally as a consequence of changes in object distance from the observer, and may approximate the effects of changes in other parameters governing the motion in a given scene. This modeling and estimation framework has implications for the neurobiology of sensory and motor systems, which need to cope with these fluctuations in scale in order to represent motion efficiently and drive fast and accurate tracking behavior. 

Everything that the brain sees must first be encoded by the retina, which maintains a reliable representation of the visual world in many different, complex natural scenes while also adapting to stimulus changes. This study quantifies whether and how the brain selectively encodes stimulus features about scene identity in complex naturalistic environments. While a wealth of previous work has dug into the static and dynamic features of the population code in retinal ganglion cells, less is known about how populations form both flexible and reliable encoding in natural moving scenes. We record from the larval salamander retina responding to five different natural movies, over many repeats, and use these data to characterize the population code in terms of single-cell fluctuations in rate and pairwise couplings between cells. Decomposing the population code into independent and cell-cell interactions reveals how broad scene structure is encoded in the retinal output. while the single-cell activity adapts to different stimuli, the population structure captured in the sparse, strong couplings is consistent across natural movies as well as synthetic stimuli. We show that these interactions contribute to encoding scene identity. We also demonstrate that this structure likely arises in part from shared bipolar cell input as well as from gap junctions between retinal ganglion cells and amacrine cells. 

Abstract The renormalization group (RG) is a class of theoretical techniques used to explain the collective physics of interacting, many-body systems. It has been suggested that the RG formalism may be useful in finding and interpreting emergent low-dimensional structure in complex systems outside of the traditional physics context, such as in biology or computer science. In such contexts, one common dimensionality-reduction framework already in use is information bottleneck (IB), in which the goal is to compress an ‘input’ signalXwhile maximizing its mutual information with some stochastic ‘relevance’ variableY. IB has been applied in the vertebrate and invertebrate processing systems to characterize optimal encoding of the future motion of the external world. Other recent work has shown that the RG scheme for the dimer model could be ‘discovered’ by a neural network attempting to solve an IB-like problem. This manuscript explores whether IB and any existing formulation of RG are formally equivalent. A class of soft-cutoff non-perturbative RG techniques are defined by families of non-deterministic coarsening maps, and hence can be formally mapped onto IB, and vice versa. For concreteness, this discussion is limited entirely to Gaussian statistics (GIB), for which IB has exact, closed-form solutions. Under this constraint, GIB has a semigroup structure, in which successive transformations remain IB-optimal. Further, the RG cutoff scheme associated with GIB can be identified. Our results suggest that IB can be used toimposea notion of ‘large scale’ structure, such as biological function, on an RG procedure. 

The visual system must make predictions to compensate for inherent delays in its processing. Yet little is known, mechanistically, about how prediction aids natural behaviors. Here, we show that despite a 20-30ms intrinsic processing delay, the vertical motion sensitive (VS) network of the blowfly achieves maximally efficient prediction. This prediction enables the fly to fine-tune its complex, yet brief, evasive flight maneuvers according to its initial ego-rotation at the time of detection of the visual threat. Combining a rich database of behavioral recordings with detailed compartmental modeling of the VS network, we further show that the VS network has axonal gap junctions that are critical for optimal prediction. During evasive maneuvers, a VS subpopulation that directly innervates the neck motor center can convey predictive information about the fly’s future ego-rotation, potentially crucial for ongoing flight control. These results suggest a novel sensory-motor pathway that links sensory prediction to behavior. 

Responding to stimuli requires that organisms encode information about the external world. Not all parts of the input are important for behavior, and resource limitations demand that signals be compressed. Prediction of the future input is widely beneficial in many biological systems. We compute the trade-offs between representing the past faithfully and predicting the future using the information bottleneck approach, for input dynamics with different levels of complexity. For motion prediction, we show that, depending on the parameters in the input dynamics, velocity or position information is more useful for accurate prediction. We show which motion representations are easiest to re-use for accurate prediction in other motion contexts, and identify and quantify those with the highest transferability. For non-Markovian dynamics, we explore the role of long-term memory in shaping the internal representation. Lastly, we show that prediction in evolutionary population dynamics is linked to clustering allele frequencies into non-overlapping memories. 

Spatially distributed excitation and inhibition collectively shape a visual neuron’s receptive field (RF) properties. In the direction-selective circuit of the mammalian retina, the role of strong null-direction inhibition of On-Off direction-selective ganglion cells (On-Off DSGCs) on their direction selectivity is well-studied. However, how excitatory inputs influence the On-Off DSGC’s visual response is underexplored. Here, we report that On-Off DSGCs have a spatially displaced glutamatergic receptive field along their horizontal preferred-null motion axes. This displaced receptive field contributes to DSGC null-direction spiking during interrupted motion trajectories. Theoretical analyses indicate that population responses during interrupted motion may help populations of On-Off DSGCs signal the spatial location of moving objects in complex, naturalistic visual environments. Our study highlights that the direction-selective circuit exploits separate sets of mechanisms under different stimulus conditions, and these mechanisms may help encode multiple visual features.