Vision for navigation: What can we learn from ants?

The visual systems of all animals are used to provide information that can guide behaviour. In some cases insects demonstrate particularly impressive visually-guided behaviour and then we might reasonably ask how the low-resolution vision and limited neural resources of insects are tuned to particular behavioural strategies. Such questions are of interest to both biologists and to engineers seeking to emulate insect-level performance with lightweight hardware. One behaviour that insects share with many animals is the use of learnt visual information for navigation. Desert ants, in particular, are expert visual navigators. Across their foraging life, ants can learn long idiosyncratic foraging routes. What's more, these routes are learnt quickly and the visual cues that define them can be implemented for guidance independently of other social or personal information. Here we review the style of visual navigation in solitary foraging ants and consider the physiological mechanisms that underpin it. Our perspective is to consider that robust navigation comes from the optimal interaction between behavioural strategy, visual mechanisms and neural hardware. We consider each of these in turn, highlighting the value of ant-like mechanisms in biomimetic endeavours.     

Three spectrally distinct photoreceptors in diurnal and nocturnal Australian ants

Ants are thought to be special among Hymenopterans in having only dichromatic colour vision based on two spectrally distinct photoreceptors. Many ants are highly visual animals, however, and use vision extensively for navigation. We show here that two congeneric day- and night-active Australian ants have three spectrally distinct photoreceptor types, potentially supporting trichromatic colour vision. Electroretinogram recordings show the presence of three spectral sensitivities with peaks (λ_max) at 370, 450 and 550 nm in the night-active Myrmecia vindex and peaks at 370, 470 and 510 nm in the day-active Myrmecia croslandi. Intracellular electrophysiology on individual photoreceptors confirmed that the night-active M. vindex has three spectral sensitivities with peaks (λ_max) at 370, 430 and 550 nm. A large number of the intracellular recordings in the night-active M. vindex show unusually broad-band spectral sensitivities, suggesting that photoreceptors may be coupled. Spectral measurements at different temporal frequencies revealed that the ultraviolet receptors are comparatively slow. We discuss the adaptive significance and the probability of trichromacy in Myrmecia ants in the context of dim light vision and visual navigation.     

Swarm cognition on off-road autonomous robots

This paper contributes with the first validation of swarm cognition as a useful framework for the design of autonomous robots controllers. The proposed model is built upon the authors’ previous work validated on a simulated robot performing local navigation on a 2-D deterministic world. Based on the ant foraging metaphor and motivated by the multiple covert attention hypothesis, the model consists of a set of simple virtual agents inhabiting the robot’s visual input, searching in a collectively coordinated way for obstacles. Parsimonious and accurate visual attention, operating on a by-need basis, is attained by making the activity of these agents modulated by the robot’s action selection process. A by-product of the system is the maintenance of active, parallel and sparse spatial working memories. In short, the model exhibits the self-organisation of a relevant set of features composing a cognitive system. To show its robustness, the model is extended in this paper to handle the challenges of physical off-road robots equipped with noisy stereoscopic vision sensors. Furthermore, an extensive aggregate of biological arguments sustaining the model is provided. Experimental results show the ability of the model to robustly control the robot on a local navigation task, with less than 1% of the robot’s visual input being analysed. Hence, with this system the computational cost of perception is considerably reduced, thus fostering robot miniaturisation and energetic efficiency. This confirms the advantages of using a swarm-based system, operating in an intricate way with action selection, to judiciously control visual attention and maintain sparse spatial memories, constituting a basic form of swarm cognition.     

A lightweight,inexpensive robotic system for insect vision

Designing hardware for miniaturized robotics which mimics the capabilities of flying insects is of interest, because they share similar constraints (i.e. small size, low weight, and low energy consumption). Research in this area aims to enable robots with similarly efficient flight and cognitive abilities. Visual processing is important to flying insects' impressive flight capabilities, but currently, embodiment of insect-like visual systems is limited by the hardware systems available. Suitable hardware is either prohibitively expensive, difficult to reproduce, cannot accurately simulate insect vision characteristics, and/or is too heavy for small robotic platforms. These limitations hamper the development of platforms for embodiment which in turn hampers the progress on understanding of how biological systems fundamentally work. To address this gap, this paper proposes an inexpensive, lightweight robotic system for modelling insect vision. The system is mounted and tested on a robotic platform for mobile applications, and then the camera and insect vision models are evaluated. We analyse the potential of the system for use in embodiment of higher-level visual processes (i.e. motion detection) and also for development of navigation based on vision for robotics in general. Optic flow from sample camera data is calculated and compared to a perfect, simulated bee world showing an excellent resemblance.     

Maintaining a cognitive map in darkness: the need to fuse boundary knowledge with path integration

Spatial navigation requires the processing of complex, disparate and often ambiguous sensory data. The neurocomputations underpinning this vital ability remain poorly understood. Controversy remains as to whether multimodal sensory information must be combined into a unified representation, consistent with Tolman's "cognitive map", or whether differential activation of independent navigation modules suffice to explain observed navigation behaviour. Here we demonstrate that key neural correlates of spatial navigation in darkness cannot be explained if the path integration system acted independently of boundary (landmark) information. In vivo recordings demonstrate that the rodent head direction (HD) system becomes unstable within three minutes without vision. In contrast, rodents maintain stable place fields and grid fields for over half an hour without vision. Using a simple HD error model, we show analytically that idiothetic path integration (iPI) alone cannot be used to maintain any stable place representation beyond two to three minutes. We then use a measure of place stability based on information theoretic principles to prove that featureless boundaries alone cannot be used to improve localization above chance level. Having shown that neither iPI nor boundaries alone are sufficient, we then address the question of whether their combination is sufficient and - we conjecture - necessary to maintain place stability for prolonged periods without vision. We addressed this question in simulations and robot experiments using a navigation model comprising of a particle filter and boundary map. The model replicates published experimental results on place field and grid field stability without vision, and makes testable predictions including place field splitting and grid field rescaling if the true arena geometry differs from the acquired boundary map. We discuss our findings in light of current theories of animal navigation and neuronal computation, and elaborate on their implications and significance for the design, analysis and interpretation of experiments.     

Proximate and ultimate causes of variable visual sensitivities: Insights from cichlid fish radiations

Animals vary in their sensitivities to different wavelengths of light. Sensitivity differences can have fitness implications in terms of animals' ability to forage, find mates, and avoid predators. As a result, visual systems are likely selected to operate in particular lighting environments and for specific visual tasks. This review focuses on cichlid vision, as cichlids have diverse visual sensitivities, and considerable progress has been made in determining the genetic basis for this variation. We describe both the proximate and ultimate mechanisms shaping cichlid visual diversity using the structure of Tinbergen's four questions. We describe (1) the molecular mechanisms that tune visual sensitivities including changes in opsin sequence and expression; (2) the evolutionary history of visual sensitivity across the African cichlid flocks; (3) the ontological changes in visual sensitivity and how modifying this developmental program alters sensitivities among species; and (4) the fitness benefits of spectral tuning mechanisms with respect to survival and mating success. We further discuss progress to unravel the gene regulatory networks controlling opsin expression and suggest that a simple genetic architecture contributes to the lability of opsin gene expression. Finally, we identify unanswered questions including whether visual sensitivities are experiencing selection, and whether similar spectral tuning mechanisms shape visual sensitivities of other fishes. genesis 54:299–325, 2016. © 2016 Wiley Periodicals, Inc.     

The human visual system is optimised for processing the spatial information in natural visual images

A fundamental tenet of visual science is that the detailed properties of visual systems are not capricious accidents, but are closely matched by evolution and neonatal experience to the environments and lifestyles in which those visual systems must work. This has been shown most convincingly for fish and insects. For mammalian vision, however, this tenet is based more upon theoretical arguments than upon direct observations. Here, we describe experiments that require human observers to discriminate between pictures of slightly different faces or objects. These are produced by a morphing technique that allows small, quantifiable changes to be made in the stimulus images. The independent variable is designed to give increasing deviation from natural visual scenes, and is a measure of the Fourier composition of the image (its second-order statistics). Performance in these tests was best when the pictures had natural second-order spatial statistics, and degraded when the images were made less natural. Furthermore, performance can be explained with a simple model of contrast coding, based upon the properties of simple cells in the mammalian visual cortex. The findings thus provide direct empirical support for the notion that human spatial vision is optimised to the second-order statistics of the optical environment.     

Insect-Inspired Navigation Algorithm for an Aerial Agent Using Satellite Imagery

Humans have long marveled at the ability of animals to navigate swiftly, accurately, and across long distances. Many mechanisms have been proposed for how animals acquire, store, and retrace learned routes, yet many of these hypotheses appear incongruent with behavioral observations and the animals’ neural constraints. The “Navigation by Scene Familiarity Hypothesis” proposed originally for insect navigation offers an elegantly simple solution for retracing previously experienced routes without the need for complex neural architectures and memory retrieval mechanisms. This hypothesis proposes that an animal can return to a target location by simply moving toward the most familiar scene at any given point. Proof of concept simulations have used computer-generated ant’s-eye views of the world, but here we test the ability of scene familiarity algorithms to navigate training routes across satellite images extracted from Google Maps. We find that Google satellite images are so rich in visual information that familiarity algorithms can be used to retrace even tortuous routes with low-resolution sensors. We discuss the implications of these findings not only for animal navigation but also for the potential development of visual augmentation systems and robot guidance algorithms.     

Computational studies of the extraction of visual spatial information from binocular and motion cues

This paper reviews some of the contributions that work in computational vision has made to the study of biological vision systems. We concentrate on two areas where there has been strong interaction between computational and experimental studies: the use of binocular stereo to recover the distances to surfaces in space, and the recovery of the three-dimensional shape of objects from relative motion in the image. With regard to stereo, we consider models proposed for solving the stereo correspondence problem, focussing on the way in which physical properties of the world constrain possible methods of solution. We also show how critical observations regarding human stereo vision have helped to shape these models. With regard to the recovery of structure from motion, we focus on how the constraint of object rigidity has been used in computational models of this process.     

Learning and neural plasticity in visual object recognition

The capability of the adult primate visual system for rapid and accurate recognition of targets in cluttered, natural scenes far surpasses the abilities of state-of-the-art artificial vision systems. Understanding this capability remains a fundamental challenge in visual neuroscience. Recent experimental evidence suggests that adaptive coding strategies facilitated by underlying neural plasticity enable the adult brain to learn from visual experience and shape its ability to integrate and recognize coherent visual objects.     

Odor supported place cell model and goal navigation in rodents

Experiments with rodents demonstrate that visual cues play an important role in the control of hippocampal place cells and spatial navigation. Nevertheless, rats may also rely on auditory, olfactory and somatosensory stimuli for orientation. It is also known that rats can track odors or self-generated scent marks to find a food source. Here we model odor supported place cells by using a simple feed-forward network and analyze the impact of olfactory cues on place cell formation and spatial navigation. The obtained place cells are used to solve a goal navigation task by a novel mechanism based on self-marking by odor patches combined with a Q-learning algorithm. We also analyze the impact of place cell remapping on goal directed behavior when switching between two environments. We emphasize the importance of olfactory cues in place cell formation and show that the utility of environmental and self-generated olfactory cues, together with a mixed navigation strategy, improves goal directed navigation.     

Cambrian view

The analysis of visual systems is a valuable method of assessing phylogenetic processes. As in the present animal world, we find simple and complex systems in the Lower Cambrian. One may detect “simple eyes” for example with an advanced design in lobopodians, while the existence of even more simple “simple eyes” is very probable but still to be proved. More complex systems are to be found. In Leanchoilia illecebrosa Hou, 1987 and Leanchoilia superlata Walcott, 1912 there are probable dorsal median eyes and a pair of fine, stalked ventral eyes. Both systems may contribute to phylogenetic and systematic discussions. These presumably movable stalked eyes may be regarded as an adaptation to a mobile lifestyle. They suggest that the physiologic principle of nystagmus to stabilise the visual world of an animal in motion was already realised in Leanchoilia, perhaps for the first time. To analyse the surface of the early eyes from the Lower Cambrian – not only of Leanchoilia, but of any other forms as well – the number, shape and other parameters of the lenses could lead to further knowledge regarding vision in early invertebrates.     

When assumptions on visual system evolution matter: nestling colouration and parental visual performance in birds

Comparative studies in visual ecology of birds often rely on several assumptions on the evolution of avian vision. In this study, we show that when these assumptions are not upheld, conclusions may be strongly affected. To illustrate this purpose, we reanalysed the data of Avilés & Soler (J. Evol. Biol. 22 : 376–386, 2009) who demonstrated that nestling gape colouration in altricial birds is associated with visual system. We show that a slight change in analysis methodology leads to opposite conclusions. Such conflicting result raises the problem of applying powerful methods developed for continuous variables to a small sample and a small number of independent events of qualitative visual system shift in comparative analyses. Further, we show that the current trend to assume strong phylogenetic inertia of avian visual systems is contradicted by data and that the sequencing of the SWS1 opsin gene should be considered as an alternative approach.     

Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis

The evolution of trichromatic color vision in primates may improve foraging performance as well as intraspecific communication; however, the context in which color vision initially evolved is unknown. We statistically examined the hypothesis that trichromatic color vision in primates represents a preexisting bias for the evolution of red coloration (pelage and/or skin) through sexual selection. Our analyses show that trichromatic color vision evolved before red pelage and red skin, as well as before gregarious mating systems that would promote sexual selection for visual traits and other forms of intraspecific communication via red traits. We also determined that both red pelage and red skin were more likely to evolve in the presence of color vision and mating systems that promote sexual selection. These results provide statistical support for the hypothesis that trichromatic color vision in primates evolved in a context other than intraspecific communication with red traits, most likely foraging performance, but, once evolved, represented a preexisting bias that promoted the evolution of red traits through sexual selection.     

Vision in elasmobranchs and their relatives: 21st century advances

This review identifies a number of exciting new developments in the understanding of vision in cartilaginous fishes that have been made since the turn of the century. These include the results of studies on various aspects of the visual system including eye size, visual fields, eye design and the optical system, retinal topography and spatial resolving power, visual pigments, spectral sensitivity and the potential for colour vision. A number of these studies have covered a broad range of species, thereby providing valuable information on how the visual systems of these fishes are adapted to different environmental conditions. For example, oceanic and deep-sea sharks have the largest eyes amongst elasmobranchs and presumably rely more heavily on vision than coastal and benthic species, while interspecific variation in the ratio of rod and cone photoreceptors, the topographic distribution of the photoreceptors and retinal ganglion cells in the retina and the spatial resolving power of the eye all appear to be closely related to differences in habitat and lifestyle. Multiple, spectrally distinct cone photoreceptor visual pigments have been found in some batoid species, raising the possibility that at least some elasmobranchs are capable of seeing colour, and there is some evidence that multiple cone visual pigments may also be present in holocephalans. In contrast, sharks appear to have only one cone visual pigment. There is evidence that ontogenetic changes in the visual system, such as changes in the spectral transmission properties of the lens, lens shape, focal ratio, visual pigments and spatial resolving power, allow elasmobranchs to adapt to environmental changes imposed by habitat shifts and niche expansion. There are, however, many aspects of vision in these fishes that are not well understood, particularly in the holocephalans. Therefore, this review also serves to highlight and stimulate new research in areas that still require significant attention.     

Monocular vision leads to a dissociation between grip force and grip aperture scaling during reach-to-grasp movements

It has been argued that visual perception and the visual control of action depend upon functionally distinct and anatomically separable brain systems. Electrophysiological evidence indicates that binocular vision may be particularly important for the visuomotor processing within the posterior parietal cortex, and neuropsychological and psychophysical studies confirm that binocular vision is crucial for the accurate planning and control of prehension movements. An unresolved issue concerns the consequences for visuomotor processing of removing binocular vision. By one account, monocular viewing leads to reliance upon pictorial visual cues to calibrate grasping and results in disruption to normal size-constancy mechanisms. This proposal is based on the finding that maximum grip apertures are reduced with monocular vision. By a second account, monocular viewing results in the loss of binocular visual cues and leads to strategic changes in visuomotor processing by way of altered safety margins. This proposal is based on the finding that maximum grip apertures are increased with monocular vision. We measured both grip aperture and grip force during prehension movements executed with binocular and monocular viewing. We demonstrate that each of the above accounts may be correct and can be observed within the same task. Specifically, we show that, while grip apertures increase with monocular vision, consistent with altered visuomotor safety margins, maximum grip force is nevertheless reduced, consistent with a misperception of object size. These results are related to differences in visual processing required for calibrating grip aperture and grip force during reaching.     

Hyperpolarization-activated current (I(h)) in ganglion-cell photoreceptors

Intrinsically photosensitive retinal ganglion cells (ipRGCs) express the photopigment melanopsin and serve as the primary retinal drivers of non-image-forming visual functions such as circadian photoentrainment, the pupillary light reflex, and suppression of melatonin production in the pineal. Past electrophysiological studies of these cells have focused on their intrinsic photosensitivity and synaptic inputs. Much less is known about their voltage-gated channels and how these might shape their output to non-image-forming visual centers. Here, we show that rat ipRGCs retrolabeled from the suprachiasmatic nucleus (SCN) express a hyperpolarization-activated inwardly-rectifying current (I(h)). This current is blocked by the known I(h) blockers ZD7288 and extracellular cesium. As in other systems, including other retinal ganglion cells, I(h) in ipRGCs is characterized by slow kinetics and a slightly greater permeability for K(+) than for Na(+). Unlike in other systems, however, I(h) in ipRGCs apparently does not actively contribute to resting membrane potential. We also explore non-specific effects of the common I(h) blocker ZD7288 on rebound depolarization and evoked spiking and discuss possible functional roles of I(h) in non-image-forming vision. This study is the first to characterize I(h) in a well-defined population of retinal ganglion cells, namely SCN-projecting ipRGCs.     

Ecomorphology of eye shape and retinal topography in waterfowl (Aves: Anseriformes: Anatidae) with different foraging modes

Despite the large body of literature on ecomorphological adaptations to foraging in waterfowl, little attention has been paid to their sensory systems, especially vision. Here, we compare eye shape and retinal topography across 12 species representing 4 different foraging modes. Eye shape was significantly different among foraging modes, with diving and pursuit-diving species having relatively smaller corneal diameters compared to non-diving species. This may be associated with differences in ambient light intensity while foraging or an ability to tightly constrict the pupil in divers in order to facilitate underwater vision. Retinal topography was similar across all species, consisting of an oblique visual streak, a central area of peak cell density, and no discernible fovea. Because the bill faces downwards when the head is held in the normal posture in waterfowl, the visual streak will be held horizontally, allowing the horizon to be sampled with higher visual acuity. Estimates of spatial resolving power were similar among species with only the Canada goose having a higher spatial resolution. Overall, we found no evidence of ecomorphological adaptations to different foraging modes in the retinal ganglion cell layer in waterfowl. Rather, retinal topography in these birds seems to reflect the ‘openness’ of their habitats.     

Navigation Using Sensory Substitution in Real and Virtual Mazes

Under certain specific conditions people who are blind have a perception of space that is equivalent to that of sighted individuals. However, in most cases their spatial perception is impaired. Is this simply due to their current lack of access to visual information or does the lack of visual information throughout development prevent the proper integration of the neural systems underlying spatial cognition? Sensory Substitution devices (SSDs) can transfer visual information via other senses and provide a unique tool to examine this question. We hypothesize that the use of our SSD (The EyeCane: a device that translates distance information into sounds and vibrations) can enable blind people to attain a similar performance level as the sighted in a spatial navigation task. We gave fifty-six participants training with the EyeCane. They navigated in real life-size mazes using the EyeCane SSD and in virtual renditions of the same mazes using a virtual-EyeCane. The participants were divided into four groups according to visual experience: congenitally blind, low vision & late blind, blindfolded sighted and sighted visual controls. We found that with the EyeCane participants made fewer errors in the maze, had fewer collisions, and completed the maze in less time on the last session compared to the first. By the third session, participants improved to the point where individual trials were no longer significantly different from the initial performance of the sighted visual group in terms of errors, time and collision.     

The visual ecology of fiddler crabs

With their eyes on long vertical stalks, their panoramic visual field and their pronounced equatorial acute zone for vertical resolving power, the visual system of fiddler crabs is exquisitely tuned to the geometry of vision in the flat world of inter-tidal mudflats. The crabs live as burrow-centred grazers in dense, mixed-sex, mixed-age and mixed-species colonies, with the active space of an individual rarely exceeding 1 m². The full behavioural repertoire of fiddler crabs can thus be monitored over extended periods of time on a moment to moment basis together with the visual information they have available to guide their actions. These attributes make the crabs superb subjects for analysing visual tasks and the design of visual processing mechanisms under natural conditions, a prerequisite for understanding the evolution of visual systems. In this review we show, on the one hand, how deeply embedded fiddler crab vision is in the behavioural and the physical ecology of these animals and, on the other hand, how their behavioural options are constrained by their perceptual limitations. Studying vision in fiddler crabs reminds us that vision has a topography, that it is context-dependent and pragmatic and that there are perceptual limits to what animals can know and therefore care about. For Mike Land