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Introduction: Neohelice granulata crabs live in mudflats where they prey upon smaller crabs. Predatory behavior can be elicited in the laboratory by a dummy moving at ground level in an artificial arena. Previous research found that crabs do not use apparent dummy size nor its retinal speed as a criterion to initiate attacks, relying instead on actual size and distance to the target. To estimate the distance to an object on the ground, Neohelice could rely on angular declination below the horizon or, since they are broad-fronted with eye stalks far apart, on stereopsis. Unlike other animals, binocular vision does not widen the visual field of crabs since they already cover 360° monocularly. There exist nonetheless areas of the eye with increased resolution. Methods: We tested how predatory responses towards the dummy changed when animals' vision was monocular (one eye occluded by opaque black paint) compared to binocular. Results: Even though monocular crabs could still perform predatory behaviors, we found a steep reduction in the number of attacks. Predatory performance defined by the probability of completing the attacks and the success rate (the probability of making contact with the dummy once the attack was initiated) was impaired too. Monocular crabs tended to use frontal, ballistic jumps (lunge behavior) less, and the accuracy of those attacks was reduced. Monocular crabs used prey interception (moving toward the dummy while it approached the crab) more frequently, favoring attacks when the dummy was ipsilateral to the viewing eye. Instead, binocular crabs' responses were balanced in the right and left hemifields. Both groups mainly approached the dummy using the lateral field of view, securing speed of response. Conclusion: Although two eyes are not strictly necessary for eliciting predatory responses, binocularity is associated with more frequent and precise attacks.

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When an animal rotates (whether it is an arthropod, a fish, a bird or a human) a drift of the visual panorama occurs over its retina, termed optic flow. The image is stabilized by compensatory behaviours (driven by the movement of the eyes, head or the whole body depending on the animal) collectively termed optomotor responses. The dipteran lobula plate has been consistently linked with optic flow processing and the control of optomotor responses. Crabs have a neuropil similarly located and interconnected in the optic lobes, therefore referred to as a lobula plate too. Here we show that the crabs' lobula plate is required for normal optomotor responses since the response was lost or severely impaired in animals whose lobula plate had been lesioned. The effect was behaviour-specific, since avoidance responses to approaching visual stimuli were not affected. Crabs require simpler optic flow processing than flies (because they move slower and in two-dimensional instead of three-dimensional space), consequently their lobula plates are relatively smaller. Nonetheless, they perform the same essential role in the visual control of behaviour. Our findings add a fundamental piece to the current debate on the evolutionary relationship between the lobula plates of insects and crustaceans.

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The visual neuropils (lamina, medulla, and lobula complex) of malacostracan crustaceans and hexapods have many organizational principles, cell types, and functional properties in common. Information about the cellular elements that compose the crustacean lobula is scarce especially when focusing on small columnar cells. Semiterrestrial crabs possess a highly developed visual system and display conspicuous visually guided behaviors. In particular, Neohelice granulata has been previously used to describe the cellular components of the first two optic neuropils using Golgi impregnation technique. Here, we present a comprehensive description of individual elements composing the third optic neuropil, the lobula, of that same species. We characterized a wide variety of elements (140 types) including input terminals and lobula columnar, centrifugal, and input columnar elements. Results reveal a very dense and complex neuropil. We found a frequently impregnated input element (suggesting a supernumerary cartridge representation) that arborizes in the third layer of the lobula and that presents four variants each with ramifications organized following one of the four cardinal axes suggesting a role in directional processing. We also describe input elements with two neurites branching in the third layer, probably connecting with the medulla and lobula plate. These facts suggest that this layer is involved in the directional motion detection pathway in crabs. We analyze and discuss our findings considering the similarities and differences found between the layered organization and components of this crustacean lobula and the lobula of insects.

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The hypothesis of a common origin for high-order memory centers in bilateral animals presents the question of how different brain structures, such as the vertebrate hippocampus and the arthropod mushroom bodies, are both structurally and functionally comparable. Obtaining evidence to support the hypothesis that crustaceans possess structures equivalent to the mushroom bodies that play a role in associative memories has proved challenging. Structural evidence supports that the hemiellipsoid bodies of hermit crabs, crayfish and lobsters, spiny lobsters, and shrimps are homologous to insect mushroom bodies. Although a preliminary description and functional evidence supporting such homology in true crabs (Brachyura) has recently been shown, other authors consider the identification of a possible mushroom body homolog in Brachyura as problematic. Here we present morphological and immunohistochemical data in Neohelice granulata supporting that crabs possess well-developed hemiellipsoid bodies that are resolved as mushroom bodies-like structures. Neohelice exhibits a peduncle-like tract, from which processes project into proximal and distal domains with different neuronal specializations. The proximal domains exhibit spines and en passant-like processes and are proposed here as regions mainly receiving inputs. The distal domains exhibit a "trauben"-like compartmentalized structure with bulky terminal specializations and are proposed here as output regions. In addition, we found microglomeruli-like complexes, adult neurogenesis, aminergic innervation, and elevated expression of proteins necessary for memory processes. Finally, in vivo calcium imaging suggests that, as in insect mushroom bodies, the output regions exhibit stimulus-specific activity. Our results support the shared organization of memory centers across crustaceans and insects.

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All animals need information about the direction of motion to be able to track the trajectory of a target (prey, predator, cospecific) or to control the course of navigation. This information is provided by direction selective (DS) neurons, which respond to images moving in a unique direction. DS neurons have been described in numerous species including many arthropods. In these animals, the majority of the studies have focused on DS neurons dedicated to processing the optic flow generated during navigation. In contrast, only a few studies were performed on DS neurons related to object motion processing. The crab Neohelice is an established experimental model for the study of neurons involved in visually-guided behaviors. Here, we describe in male crabs of this species a new group of DS neurons that are highly directionally selective to moving objects. The neurons were physiologically and morphologically characterized by intracellular recording and staining in the optic lobe of intact animals. Because of their arborization in the lobula complex, we called these cells lobula complex directional cells (LCDCs). LCDCs also arborize in a previously undescribed small neuropil of the lateral protocerebrum. LCDCs are responsive only to horizontal motion. This nicely fits in the behavioral adaptations of a crab inhabiting a flat, densely crowded environment, where most object motions are generated by neighboring crabs moving along the horizontal plane.SIGNIFICANCE STATEMENT Direction selective (DS) neurons are key to a variety of visual behaviors including, target tracking (preys, predators, cospecifics) and course control. Here, we describe the physiology and morphology of a new group of remarkably directional neurons exclusively responsive to horizontal motion in crabs. These neurons arborize in the lobula complex and in a previously undescribed small neuropil of the lateral protocerebrum. The strong sensitivity of these cells for horizontal motion represents a clear example of functional neuronal adaptation to the lifestyle of an animal inhabiting a flat environment.

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Animals, from invertebrates to humans, stabilize the panoramic optic flow through compensatory movements of the eyes, the head or the whole body, a behavior known as optomotor response (OR). The same optic flow moved clockwise or anticlockwise elicits equivalent compensatory right or left turning movements, respectively. However, if stimulated monocularly, many animals show a unique effective direction of motion, i.e., a unidirectional OR. This phenomenon has been reported in various species from mammals to birds, reptiles, and amphibious, but among invertebrates, it has only been tested in flies, where the directional sensitivity is opposite to that found in vertebrates. Although OR has been extensively investigated in crabs, directional sensitivity has never been analyzed. Here, we present results of behavioral experiments aimed at exploring the directional sensitivity of the OR in two crab species belonging to different families: the varunid mud crab Neohelice granulata and the ocypode fiddler crab Uca uruguayensis. By using different conditions of visual perception (binocular, left or right monocular) and direction of flow field motion (clockwise, anticlockwise), we found in both species that in monocular conditions, OR is effectively displayed only with progressive (front-to-back) motion stimulation. Binocularly elicited responses were directional insensitive and significantly weaker than monocular responses. These results are coincident with those described in flies and suggest a commonality in the circuit underlying this behavior among arthropods. Additionally, we found the existence of a remarkable eye dominance for the OR, which is associated to the size of the larger claw. This is more evident in the fiddler crab where the difference between the two claws is huge.

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The lobula plate is part of the lobula complex, the third optic neuropil, in the optic lobes of insects. It has been extensively studied in dipterous insects, where its role in processing flow-field motion information used for controlling optomotor responses was discovered early. Recently, a lobula plate was also found in malacostracan crustaceans. Here, we provide the first detailed description of the neuroarchitecture, the input and output connections and the retinotopic organization of the lobula plate in a crustacean, the crab Neohelice granulata using a variety of histological methods that include silver reduced staining and mass staining with dextran-conjugated dyes. The lobula plate of this crab is a small elongated neuropil. It receives separated retinotopic inputs from columnar neurons of the medulla and the lobula. In the anteroposterior plane, the neuropil possesses four layers defined by the arborizations of such columnar inputs. Medulla projecting neurons arborize mainly in two of these layers, one on each side, while input neurons arriving from the lobula branch only in one. The neuropil contains at least two classes of tangential elements, one connecting with the lateral protocerebrum and the other that exits the optic lobes toward the supraesophageal ganglion. The number of layers in the crab's lobula plate, the retinotopic connections received from the medulla and from the lobula, and the presence of large tangential neurons exiting the neuropil, reflect the general structure of the insect lobula plate and, hence, provide support to the notion of an evolutionary conserved function for this neuropil.

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Predator avoidance and prey capture are among the most vital of animal behaviors. They require fast reactions controlled by comparatively straightforward neural circuits often containing giant neurons, which facilitates their study with electrophysiological techniques. Naturally occurring avoidance behaviors, in particular, can be easily and reliably evoked in the laboratory, enabling their neurophysiological investigation. Studies in the laboratory alone, however, can lead to a biased interpretation of an animal's behavior in its natural environment. In this Review, we describe current knowledge - acquired through both laboratory and field studies - on the visually guided escape behavior of the crab Neohelice granulata Analyses of the behavioral responses to visual stimuli in the laboratory have revealed the main characteristics of the crab's performance, such as the continuous regulation of the speed and direction of the escape run, or the enduring changes in the strength of escape induced by learning and memory. This work, in combination with neuroanatomical and electrophysiological studies, has allowed the identification of various giant neurons, the activity of which reflects most essential aspects of the crabs' avoidance performance. In addition, behavioral analyses performed in the natural environment reveal a more complex picture: crabs make use of much more information than is usually available in laboratory studies. Moreover, field studies have led to the discovery of a robust visually guided chasing behavior in Neohelice Here, we describe similarities and differences in the results obtained between the field and the laboratory, discuss the sources of any differences and highlight the importance of combining the two approaches.

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For many animals, the visual detection of looming stimuli is crucial at any stage of their lives. For example, human babies of only 6 days old display evasive responses to looming stimuli (Bower et al. [1971]: Percept Psychophys 9: 193-196). This means the neuronal pathways involved in looming detection should mature early in life. Locusts have been used extensively to examine the neural circuits and mechanisms involved in sensing looming stimuli and triggering visually evoked evasive actions, making them ideal subjects in which to investigate the development of looming sensitivity. Two lobula giant movement detectors (LGMD) neurons have been identified in the lobula region of the locust visual system: the LGMD1 neuron responds selectively to looming stimuli and provides information that contributes to evasive responses such as jumping and emergency glides. The LGMD2 responds to looming stimuli and shares many response properties with the LGMD1. Both neurons have only been described in the adult. In this study, we describe a practical method combining classical staining techniques and 3D neuronal reconstructions that can be used, even in small insects, to reveal detailed anatomy of individual neurons. We have used it to analyze the anatomy of the fan-shaped dendritic tree of the LGMD1 and the LGMD2 neurons in all stages of the post-embryonic development of Locusta migratoria. We also analyze changes seen during the ontogeny of escape behaviors triggered by looming stimuli, specially the hiding response.

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Crustaceans are widely distributed and inhabit very different niches. Many of them are highly visual animals. Nevertheless, the neural composition of crustacean optic neuropils deeper than the lamina is mostly unknown. In particular, semiterrestrial crabs possess a highly developed visual system and display conspicuous visually guided behaviors. A previous study shows that the first optic neuropil, the lamina of the crab Neohelice granulata, possesses a surprisingly high number of elements in each cartridge. Here, we present a comprehensive description of individual elements composing the medulla of that same species. Using Golgi impregnation, we characterized a wide variety of cells. Only considering the class of transmedullary neurons, we describe over 50 different morphologies including small- and large-field units. Among others, we describe a type of centrifugal neuron hitherto not identified in other crustaceans or insects that probably feeds back information to every cartridge in the medulla. The possible functional role of such centrifugal elements is discussed in connection with the physiological and behavioral information on visual processing available for this crab. Taken together, the results reveal a very dense and complex neuropil in which several channels of information processing would be acting in parallel. We further examine our results considering the similarities and differences found between the layered organization and components of this crustacean medulla and the medullae of insects.

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BACKGROUND: Due to the complexity and variability of natural environments, the ability to adaptively modify behavior is of fundamental biological importance. Motion vision provides essential cues for guiding critical behaviors such as prey, predator, or mate detection. However, when confronted with the repeated sight of a moving object that turns out to be irrelevant, most animals will learn to ignore it. The neural mechanisms by which moving objects can be ignored are unknown. Although many arthropods exhibit behavioral adaptation to repetitive moving objects, the underlying neural mechanisms have been difficult to study, due to the difficulty of recording activity from the small columnar neurons in peripheral motion detection circuits. RESULTS: We developed an experimental approach in an arthropod to record the calcium responses of visual neurons in vivo. We show that peripheral columnar neurons that convey visual information into the second optic neuropil persist in responding to the repeated presentation of an innocuous moving object. However, activity in the columnar neurons that convey the visual information from the second to the third optic neuropil is suppressed during high-frequency stimulus repetitions. In accordance with the animal's behavioral changes, the suppression of neural activity is fast but short lasting and restricted to the retina's trained area. CONCLUSIONS: Columnar neurons from the second optic neuropil are likely the main plastic locus responsible for the modifications in animal behavior when confronted with rapidly repeated object motion. Our results demonstrate that visually guided behaviors can be determined by neural plasticity that occurs surprisingly early in the visual pathway.

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Experiments with insects and crabs have demonstrated their remarkable capacity to learn and memorize complex visual features (Giurfa et al., 2001; Pedreira and Maldonado, 2003; Chittka and Niven, 2009). Such abilities are thought to require modular brain processing similar to that occurring in vertebrates (Menzel and Giurfa, 2001). Yet, physiological evidence for this type of functioning in the small brains of arthropods is still scarce (Liu et al., 1999, 2006; Menzel and Giurfa, 2001). In the crab Chasmagnathus granulatus, the learning rate as well as the long-term memory of a visual stimulus has been found to be reflected in the performance of identified lobula giant neurons (LGs) (Tomsic et al., 2003). The memory can only be evoked in the training context, indicating that animals store two components of the learned experience, one related to the visual stimulus and one related to the visual context (Tomsic et al., 1998; Hermitte et al., 1999). By performing intracellular recordings in the intact animal, we show that the ability of crabs to generalize the learned stimulus into new space positions and to distinguish it from a similar but unlearned stimulus, two of the main attributes of stimulus memory, is reflected by the performance of the LGs. Conversely, we found that LGs do not support the visual context memory component. Our results provide physiological evidence that the memory traces regarding "what" and "where" are stored separately in the arthropod brain.

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Investigations using invertebrate species have led to a considerable progress in our understanding of the mechanisms underlying learning and memory. In this review we describe the main behavioral and neuronal findings obtained by studying the habituation of the escape response to a visual danger stimulus in the crab Chasmagnathus granulatus. Massed training with brief intertrial intervals lead to a rapid reduction of the escape response that recovers after a short term. Conversely, few trials of spaced training renders a slower escape reduction that endures for many days. As predicted by Wagner's associative theory of habituation, long-term habituation in the crab proved to be determined by an association between the contextual environment of the training and the unconditioned stimulus. By performing intracellular recordings in the brain of the intact animal at the same time it was learning, we identified a group of neurons that remarkably reflects the short- and long-term behavioral changes. Thus, the visual memory abilities of crabs, their relatively simple and accessible nervous system, and the recording stability that can be achieved with their neurons provide an opportunity for uncovering neurophysiological and molecular events that occur in identifiable neurons during learning.

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Crustaceans are among the most extensively distributed arthropods, occupying many ecologies and manifesting a great variety of compound eye optics; but in comparison with insects, relatively little is known about the organization and neuronal morphologies of their underlying optic neuropils. Most studies, which have been limited to descriptions of the first neuropil--the lamina--suggest that different species have approximately comparable cell types. However, such studies have been limited with regard to the types of neurons they identify and most omit their topographic relationships. It is also uncertain whether similarities, such as they are, are independent of visual ecologies. The present account describes and compares the morphologies and dispositions of monopolar and other efferent neurons as well as the organization of tangential and smaller centrifugal neurons in two grapsoid crabs, one from the South Atlantic, the other from the North Pacific. Because these species occupy significantly disparate ecologies we ask whether this might be reflected in differences of cell arrangements within the most peripheral levels of the visual system. The present study identifies such differences with respect to the organization of centrifugal neurons to the lamina. We also identify in both species neurons in the lamina that have hitherto not been identified in crustaceans and we draw specific comparisons between the layered organization of the grapsoid lamina and layered laminas of insects.

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When confronted with predators, animals are forced to take crucial decisions such as the timing and manner of escape. In the case of the crab Chasmagnathus, cumulative evidence suggests that the escape response to a visual danger stimulus (VDS) can be accounted for by the response of a group of lobula giant (LG) neurons. To further investigate this hypothesis, we examined the relationship between behavioral and neuronal activities within a variety of experimental conditions that affected the level of escape. The intensity of the escape response to VDS was influenced by seasonal variations, changes in stimulus features, and whether the crab perceived stimuli monocularly or binocularly. These experimental conditions consistently affected the response of LG neurons in a way that closely matched the effects observed at the behavioral level. In other words, the intensity of the stimulus-elicited spike activity of LG neurons faithfully reflected the intensity of the escape response. These results support the idea that the LG neurons from the lobula of crabs are deeply involved in the decision for escaping from VDS.

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There is a mismatch between the documentation of the visually guided behaviors and visual physiology of decapods (Malacostraca, Crustacea) and knowledge about the neural architecture of their visual systems. The present study provides a description of the neuroanatomical features of the four visual neuropils of the grapsid crab Chasmagnathus granulatus, which is currently used as a model for investigating the neurobiology of learning and memory. Visual memory in Chasmagnathus is thought to be driven from within deep retinotopic neuropil by large-field motion-sensitive neurons. Here we describe the neural architecture characterizing the Chasmagnathus lobula, in which such neurons are found. It is shown that, unlike the equivalent region of insects, the malacostracan lobula is densely packed with columns, the spacing of which is the same as that of retinotopic units of the lamina. The lobula comprises many levels of strata and columnar afferents that supply systems of tangential neurons. Two of these, which are known to respond to movement across the retina, have orthogonally arranged dendritic fields deep in the lobula. They also show evidence of dye coupling. We discuss the significance of commonalties across taxa with respect to the organization of the lamina and medulla and contrasts these with possible taxon-specific arrangements of deeper neuropils that support systems of matched filters.

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Although the behavioral repertoire of crustaceans is largely guided by visual information their visual nervous system has been little explored. In search for central mechanisms of visual integration, this study was aimed at identifying and characterizing brain neurons in the crab involved in binocular visual processing. The study was performed in the intact animal, by recording intracellularly the response to visual stimuli of neurons from one of the two optic lobes. Identified neurons recorded from the medulla (second optic neuropil), which include sustaining neurons, dimming neurons, depolarizing and hyperpolarizing tonic neurons and on-off neurons, all presented exclusively monocular (ipsilateral) responses. In contrast, all wide field movement detector neurons recorded from the lobula (third optic neuropil) responded to moving stimuli presented to the ipsilateral and to the contralateral eye. In these cells, the responses evoked by ipsilateral or contralateral stimulation were almost identical, as revealed by analysing the number and amplitude of the elicited postsynaptic potentials and spikes, and the ability to habituate upon repeated visual stimulation. The results demonstrate that in crustaceans important binocular processing takes place at the level of the lobula.

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Ideally, learning-related changes should be investigated while they occur in vivo, but physical accessibility and stability limit intracellular studies. Experiments with insects and crabs demonstrate their remarkable capacity to learn and memorize visual features. However, the location and physiology of individual neurons underlying these processes is unknown. A recently developed crab preparation allows stable intracellular recordings from the optic ganglia to be performed in the intact animal during learning. In the crab Chasmagnathus, a visual danger stimulus (VDS) elicits animal escape, which declines after a few stimulus presentations. The long-lasting retention of this decrement is mediated by an association between contextual cues of the training site and the VDS, therefore, called context-signal memory (CSM). CSM is achieved only by spaced training. Massed training, on the contrary, produces a decline of the escape response that is short lasting and, because it is context independent, is called signal memory (SM). Here, we show that movement detector neurons (MDNs) from the lobula (third optic ganglion) of the crab modify their response to the VDS during visual learning. These modifications strikingly correlate with the rate of acquisition and with the duration of retention of both CSM and SM. Long-term CSM is detectable from the response of the neuron 1 d after training. In contrast to MDNs, identified neurons from the medulla (second optic ganglion) show no changes. Our results indicate that visual memory in the crab, and possibly other arthropods, including insects, is accounted for by functional changes occurring in neurons originating in the optic lobes.

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