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Biology subjects

Shamble, P. S.

Publications and source records attributed to Shamble, P. S..

4 recordsLinked to original sources

Biological point-light displays scanning by the principal eyes of a jumping spider

The semi-rigid structure of bodies forces mobile animals to move in rhythmic patterns shared by all creatures with skeletons, exoskeletons, or limb connections. This pattern, known as biological motion, is instantly recognizable and conveys "animacy," even when body shape is removed and only a cloud of moving dots is shown. Indeed, motion alone is so informative that some animals can infer the original shape based on the dots concurrent activity. Jumping spiders, highly visual arthropods, divide motion detection and shape recognition between their four pairs of eyes. Previous studies found that they can distinguish biological from non-biological motion using only their motion-detecting anterior lateral eyes yet seemed unable to extract shape from motion. In this study, we examined how the anterior medial eyes of jumping spiders--which are used for shape recognition--respond to dot clouds depicting biological or non-biological motion. Using a custom eye tracker, we monitored retinal movements during presentation of static and moving stimuli. We found spiders change their retinal shifting pattern based on both the targets motion (biological or not) and implied structure (i.e., whether dots suggest a coherent shape). These results reveal that jumping spiders analyze motion with more complexity than previously thought, suggesting a deeper integration of motion and form processing within their minuscule, modular brains.

animal behavior and cognition↗

Eye-specific detection and a multi-eye integration model of biological motion perception

The term biological motion refers to the peculiar kinematics of living organisms. Their interconnected joints move at a fixed distance from each other, a pattern that is common among all locomotive, rigid animals. Across the animal kingdom, many species have developed specialized circuitry to visually recognize biologically moving stimuli and discriminate them from other patterns. Recently, this skill has also been observed in the distributed visual system of jumping spiders. These eight-eyed animals use three of their eye pairs to perceive motion. Then, the gaze of the remaining pair is shifted towards the detected object for further inspection. When presented with a biologically moving stimulus and a random one, jumping spiders turn to face the latter, demonstrating discrimination. In the current paper, we systematically tested the ability of jumping spiders to discriminate biological from random displays using every single eye-pair, by blocking the others with paint. The animals were able to discriminate the stimuli only when the anterior-lateral eyes were unblocked, performing at chance level with the other pairs. Crucially, the spiders preferred the biological stimulus, not the random one. To explain this preference reversal we hypothesized a model, describing how the anterior-lateral eyes specialization in detecting biological motion feeds into a multi-eye integration system, generating more complex behavior from the combination of the simple, single-eye responses. We propose that this in-built modularity may be a solution to the limited resources of these invertebrates brains, constituting a novel approach to visual processing.

animal behavior and cognition↗

Perception of biological motion in point-light displays by jumping spiders

Over the last 50 years, point-light displays have been successfully used to explore how animals respond to dynamic visual stimuli--specifically, differentiation of the biological from the non-biological. These stimuli are designed to preserve movement patterns while minimizing static detail, with single dots representing each of the main joints of a moving animal. Imposed by their internal skeleton, vertebrate movements follow a specific semi-rigid dynamic pattern, termed "biological-motion", which can be used to distinguish animate from inanimate objects. Although biological motion detection has not been studied in invertebrates, rigid exoskeletons force many species to also follow semi-rigid movement principles. Due to their highly developed visual system and complex visual behaviors, we investigated the capability of jumping spiders to discriminate biological from non-biological motion using point-light display stimuli. By constraining spiders so that they could rotate but not move directionally, we simultaneously presented two point-light display stimuli with specific dynamic traits and registered their preference by observing which pattern they turned towards. Jumping spiders clearly demonstrated the ability to discriminate between stimuli. However, spiders showed no preference when both stimuli presented patterns with semi-rigid movements, results that are directly comparable to responses in vertebrate systems. This represents the first demonstration of biological motion recognition in an invertebrate, posing crucial questions about the evolutionary history of this ability and complex visual processing in non-vertebrate systems.

animal behavior and cognition↗

Neural computations combine low- and high-order motion cues similarly, in dragonfly and monkey

Visual motion analysis is fundamental to survival across the animal kingdom. In insects, our understanding of the underlying computations has centered on the Hassenstein-Reichardt motion detector, which computes two-point cross-correlation via multiplication; in mammalian cortex, it is postulated that a similar signal is computed by comparing matched squaring operations. Both of these operations are difficult to implement biophysically in a precise fashion; moreover, they fail to detect the more complex multipoint local motion cues present in the visual environment. Here, via single-unit recordings in two visual specialists, dragonfly \"(Odonata)\" and macaque, and via model simulations, we show that neuronal computations are not simply approximations to idealized behaviors forced by biological constraints, but rather, are signatures of a common computational strategy to capture multiple local motion cues. The similarity of motion computations at the neuronal level in the brains of two extremely dissimilar animals, with evolutionary divergence of over 700 Myr1, suggests convergence on a common computational scheme for detecting visual motion.

neuroscience↗