Fiddler crabs are unique in timing their escape responses based on speed-dependent visual cues.

Predation risk imposes strong selection pressures on visual systems to quickly and accurately identify the position and movement of potential predators.1,2 Many invertebrates and other small animals, however, have limited capacity for distance perception due to their low spatial resolution and closely situated eyes.3,4 Consequently, they often rely on simplified decision criteria, essentially heuristics or "rules of thumb", to make decisions. The visual cues animals use to make escape decisions are surprisingly consistent, especially among arthropods, with the timing of escape commonly triggered by size-dependent visual cues such as angular size or angular size increment.5,6,7,8,9,10 Angular size, however, confuses predator size and distance and provides no information about the speed of the attack. Here, we show that fiddler crabs (Gelasimus dampieri) are unique among the arthropods studied to date as they timed their escape response based on the speed of an object's angular expansion. The crabs responded reliably by running away from visual stimuli that expanded at approximately 1.7 degrees/s, irrespective of stimulus size, speed, or its initial distance from the crabs. Though the threshold expansion speed was consistent across different stimulus conditions, we found that the escape timing was modulated by the elevation at which the stimulus approached, suggesting that other risk factors can bias the expansion speed threshold. The results suggest that the visual escape cues used by arthropods are less conserved than previously thought and that lifestyle and environment are significant drivers determining the escape cues used by different species.

Escaping from multiple visual threats: modulation of escape responses in Pacific staghorn sculpin (Leptocottus armatus).

Fish perform rapid escape responses to avoid sudden predatory attacks. During escape responses, fish bend their bodies into a C-shape and quickly turn away from the predator and accelerate. The escape trajectory is determined by the initial turn (stage 1) and a contralateral bend (stage 2). Previous studies have used a single threat or model predator as a stimulus. In nature, however, multiple predators may attack from different directions simultaneously or in close succession. It is unknown whether fish are able to change the course of their escape response when startled by multiple stimuli at various time intervals. Pacific staghorn sculpin (Leptocottus armatus) were startled with a left and right visual stimulus in close succession. By varying the timing of the second stimulus, we were able to determine when and how a second stimulus could affect the escape response direction. Four treatments were used: a single visual stimulus (control); or two stimuli coming from opposite sides separated by a 0 ms (simultaneous treatment), 33 ms or 83 ms time interval. The 33 ms and 83 ms time intervals were chosen to occur either side of a predicted 60 ms visual escape latency (i.e. during stage 1). The 0 ms and 33 ms treatments influenced both the escape trajectory and the stage 1 turning angle, compared with a single stimulation, whereas the 83 ms treatment had no effect on the escape trajectory. We conclude that Pacific staghorn sculpin can modulate their escape trajectory only between stimulation and the onset of the response, but the escape trajectory cannot be modulated after the body motion has started.

Reduced neural responsiveness to looming stimuli is associated with increased aggression.

While neuro-cognitive work examining aggression has examined patients with conditions at increased risk for aggression or individuals self-reporting past aggression, little work has attempted to identify neuro-cognitive markers associated with observed/recorded aggression. The goal of the current study was to determine the extent to which aggression by youth in the first three months of residential care was associated with atypical responsiveness to threat stimuli. This functional MRI study involved 98 (68 male; mean age = 15.96 [sd = 1.52]) adolescents in residential care performing a looming threat task involving images of threatening and neutral human faces or animals that appeared to be either loom or recede. Level of aggression was negatively associated with responding to looming stimuli (irrespective of whether these were threatening or neutral) within regions including bilateral inferior frontal gyrus, right inferior parietal lobule, right superior/middle temporal gyrus and a region of right uncus proximal to the amygdala. These data indicate that aggression level is associated with a decrease in responsiveness to a basic threat cue-looming stimuli. Reduced threat responsiveness likely results in the individual being less able to represent the negative consequences that may result from engaging in aggression, thereby increasing the risk for aggressive episodes.

Retinal ganglion cell defects cause decision shifts in visually evoked defense responses.

A variety of visual cues can trigger defensive reactions in mice and other species. In mice, looming stimuli that mimic an approaching aerial predator elicit flight or freezing reactions, while sweeping stimuli that mimic an aerial predator flying parallel to the ground typically elicit freezing. The retinal ganglion cell (RGC) types involved in these circuits are largely unknown. We previously discovered that loss of RGC subpopulations in Brn3b knockout mice results in distinct visual response deficits. Here, we report that retinal or global loss of Brn3b selectively ablates the fleeing response to looming stimuli while leaving the freeze response intact. In contrast, freezing responses to sweeping stimuli are significantly affected. Genetic manipulations removing three RGC subpopulations (Brn3a+ betta RGCs, Opn4+Brn3b+, and Brn3c+Brn3b+ RGCs) result in milder phenocopies of Brn3b knockout response deficits. These findings show that flight and freezing responses to distinct visual cues are mediated by circuits that can already be separated at the level of the retina, potentially by enlisting dedicated RGC types.NEW & NOTEWORTHY Flight and freezing response choices evoked by visual stimuli are controlled by brain stem and thalamic circuits. Genetically modified mice with loss of specific retinal ganglion cell (RGC) subpopulations have altered flight versus freezing choices in response to some but not other visual stimuli. This finding suggests that "threatening" visual stimuli may be computed already at the level of the retina and communicated via dedicated pathways (RGCs) to the brain.

Looming and receding visual networks in awake marmosets investigated with fMRI.

An object that is looming toward a subject or receding away contains important information for determining if this object is dangerous, beneficial or harmless. This information (motion, direction, identity, time-to-collision, size, velocity) is analyzed by the brain in order to execute the appropriate behavioral responses depending on the context: fleeing, freezing, grasping, eating, exploring. In the current study, we performed ultra-high-field functional MRI (fMRI) at 9.4T in awake marmosets to explore the patterns of brain activation elicited by visual stimuli looming toward or receding away from the monkey. We found that looming and receding visual stimuli activated a large cortical network in frontal, parietal, temporal and occipital cortex in areas involved in the analysis of motion, shape, identity and features of the objects. Looming stimuli strongly activated a network composed of portions of the pulvinar, superior colliculus, putamen, parietal, prefrontal and temporal cortical areas. These activations suggest the existence of a network that processes visual stimuli looming toward peripersonal space to predict the consequence of these stimuli. Together with previous studies in macaque monkeys, these findings indicate that this network is preserved across Old and New World primates.

Frontier of Self and Impact Prediction.

The construction of a coherent representation of our body and the mapping of the space immediately surrounding it are of the highest ecological importance. This space has at least three specificities: it is a space where actions are planned in order to interact with our environment; it is a space that contributes to the experience of self and self-boundaries, through tactile processing and multisensory interactions; last, it is a space that contributes to the experience of body integrity against external events. In the last decades, numerous studies have been interested in peripersonal space (PPS), defined as the space directly surrounding us and which we can interact with (for reviews, see Cléry et al., 2015b; de Vignemont and Iannetti, 2015; di Pellegrino and Làdavas, 2015). These studies have contributed to the understanding of how this space is constructed, encoded and modulated. The majority of these studies focused on subparts of PPS (the hand, the face or the trunk) and very few of them investigated the interaction between PPS subparts. In the present review, we summarize the latest advances in this research and we discuss the new perspectives that are set forth for futures investigations on this topic. We describe the most recent methods used to estimate PPS boundaries by the means of dynamic stimuli. We then highlight how impact prediction and approaching stimuli modulate this space by social, emotional and action-related components involving principally a parieto-frontal network. In a next step, we review evidence that there is not a unique representation of PPS but at least three sub-sections (hand, face and trunk PPS). Last, we discuss how these subspaces interact, and we question whether and how bodily self-consciousness (BSC) is functionally and behaviorally linked to PPS.

Visual approach computation in feeding hoverflies.

On warm sunny days, female hoverflies are often observed feeding from a wide range of wild and cultivated flowers. In doing so, hoverflies serve a vital role as alternative pollinators, and are suggested to be the most important pollinators after bees and bumblebees. Unless the flower hoverflies are feeding from is large, they do not readily share the space with other insects, but instead opt to leave if another insect approaches. We used high-speed videography followed by 3D reconstruction of flight trajectories to quantify how female Eristalis hoverflies respond to approaching bees, wasps and two different hoverfly species. We found that, in 94% of the interactions, the occupant female left the flower when approached by another insect. We found that compared with spontaneous take-offs, the occupant hoverfly's escape response was performed at ∼3 times higher speed (spontaneous take-off at 0.2±0.05 m s-1 compared with 0.55±0.08 m s-1 when approached by another Eristalis). The hoverflies tended to take off upward and forward, while taking the incomer's approach angle into account. Intriguingly, we found that, when approached by wasps, the occupant Eristalis took off at a higher speed and when the wasp was further away. This suggests that feeding hoverflies may be able to distinguish these predators, demanding impressive visual capabilities. Our results, including quantification of the visual information available before occupant take-off, provide important insight into how freely behaving hoverflies perform escape responses from competitors and predators (e.g. wasps) in the wild.

Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles.

Information processing in the vertebrate brain is thought to be mediated through distributed neural networks, but it is still unclear how sensory stimuli are encoded and detected by these networks, and what role synaptic inhibition plays in this process. Here we used a collision avoidance behavior in Xenopus tadpoles as a model for stimulus discrimination and recognition. We showed that the visual system of the tadpole is selective for behaviorally relevant looming stimuli, and that the detection of these stimuli first occurs in the optic tectum. By comparing visually guided behavior, optic nerve recordings, excitatory and inhibitory synaptic currents, and the spike output of tectal neurons, we showed that collision detection in the tadpole relies on the emergent properties of distributed recurrent networks within the tectum. We found that synaptic inhibition was temporally correlated with excitation, and did not actively sculpt stimulus selectivity, but rather it regulated the amount of integration between direct inputs from the retina and recurrent inputs from the tectum. Both pharmacological suppression and enhancement of synaptic inhibition disrupted emergent selectivity for looming stimuli. Taken together these findings suggested that, by regulating the amount of network activity, inhibition plays a critical role in maintaining selective sensitivity to behaviorally-relevant visual stimuli.