Getting the Most Out of Your Zombie: Abdominal Sensors and Neural Manipulations Help Jewel Wasps Find the Roach's Weak Spot.

The parasitoid emerald jewel wasp (Ampulex compressa) subdues the American cockroach (Periplaneta americana) with a sting to the 1st thoracic ganglion, followed by a sting to the roach's brain, causing long-term pacification. The wasp then leads the cockroach to a hole where it lays an egg on the roach middle leg before barricading the entrance and departing. Although many aspects of the wasp's initial attack have been investigated, few studies have detailed the egg-laying process and the subsequent fate of the larvae. Here I show that larval survival depends on precise egg positioning on the cockroach by the female wasp. Ablation of sensory hairs on the wasp's abdomen resulted in mislaid eggs, which seldom survived. In addition, the cockroach femur may block the oviposition site. The wasp contended with this challenge with a newly discovered suite of stings, 3 directed into the 2nd thoracic ganglion which resulted in extension of the femur, thus exposing the oviposition site and removing a potential barrier to the wasp's successful reproduction. When the femur was glued in place, the wasp stung the cockroach over 100 times, in an apparent fixed action pattern triggered by the obscured oviposition target. These findings highlight the importance of proper egg placement by the wasp, and reveal sensors and new neural manipulations that facilitate the process.

Leaping eels electrify threats, supporting Humboldt's account of a battle with horses.

In March 1800, Alexander von Humboldt observed the extraordinary spectacle of native fisherman collecting electric eels (Electrophorus electricus) by "fishing with horses" [von Humboldt A (1807) Ann Phys 25:34-43]. The strategy was to herd horses into a pool containing electric eels, provoking the eels to attack by pressing themselves against the horses while discharging. Once the eels were exhausted, they could be safely collected. This legendary tale of South American adventures helped propel Humboldt to fame and has been recounted and illustrated in many publications, but subsequent investigators have been skeptical, and no similar eel behavior has been reported in more than 200 years. Here I report a defensive eel behavior that supports Humboldt's account. The behavior consists of an approach and leap out of the water during which the eel presses its chin against a threatening conductor while discharging high-voltage volleys. The effect is to short-circuit the electric organ through the threat, with increasing power diverted to the threat as the eel attains greater height during the leap. Measurement of voltages and current during the behavior, and assessment of the equivalent circuit, reveal the effectiveness of the behavior and the basis for its natural selection.

How Not to Be Turned into a Zombie.

The emerald jewel wasp (Ampulex compressa) is renowned for its ability to zombify the American cockroach (Periplaneta americana) with a sting to the brain. When the venom takes effect, the cockroach becomes passive and can be led by its antenna into a hole, where the wasp deposits an egg and then seals the exit with debris. The cockroach has the ability to walk, run, or fly if properly stimulated, but it does not try to escape as it is slowly eaten alive by the developing wasp larva. Although the composition and effects of the wasp's venom have been investigated, no studies have detailed how cockroaches might prevent this grim fate. Here it is shown that many cockroaches deter wasps with a vigorous defense. Successful cockroaches elevated their bodies, bringing their neck out of reach, and kicked at the wasp with their spiny hind legs, often striking the wasp's head multiple times. Failing this, the elevated, "on-guard" position allowed cockroaches to detect and evade the wasp's lunging attack. If grasped, the cockroaches parried the stinger with their legs, used a "stiff-arm" defense to hold back the stinger, and could stab at, and dislodge, the wasp with tibial spines. Lastly, cockroaches bit at the abdomen of wasps delivering the brain sting. An aggressive defense from the outset was most successful. Thus, for a cockroach not to become a zombie, the best strategy is: be vigilant, protect your throat, and strike repeatedly at the head of the attacker.

Behavioral pieces of neuroethological puzzles.

In this review, I give a first-person account of surprising insights that have come from the behavioral dimension of neuroethological studies in my laboratory. These studies include the early attempts to understand the function of the nose in star-nosed moles and to explore its representation in the neocortex. This led to the discovery of a somatosensory fovea that parallels the visual fovea of primates in several ways. Subsequent experiments to investigate the assumed superiority of star-nosed moles to their relatives when locating food led to the unexpected discovery of stereo olfaction in common moles. The exceptional olfactory abilities of common moles, in turn, helped to explain an unusual bait-collecting technique called "worm-grunting" in the American southeast. Finally, the predatory behavior of tentacled snakes was best understood not by exploring their nervous system, but rather by considering fish nervous systems. These experiences highlight the difficulty of predicting the abilities of animals that have senses foreign to the investigator, and also the rewards of discovering the unexpected.

Electrical Potential of Leaping Eels.

When approached by a large, partially submerged conductor, electric eels (Electrophorus electricus) will often defend themselves by leaping from the water to directly shock the threat. Presumably, the conductor is interpreted as an approaching terrestrial or semiaquatic animal. In the course of this defensive behavior, eels first make direct contact with their lower jaw and then rapidly emerge from the water, ascending the conductor while discharging high-voltage volleys. In this study, the equivalent circuit that develops during this behavior was proposed and investigated. First, the electromotive force and internal resistance of four electric eels were determined. These values were then used to estimate the resistance of the water volume between the eel and the conductor by making direct measurements of current with the eel and water in the circuit. The resistance of the return path from the eel's lower jaw to the main body of water was then determined, based on voltage recordings, for each electric eel at the height of the defensive leap. Finally, the addition of a hypothetical target for the leaping defense was considered as part of the circuit. The results suggest the defensive behavior efficiently directs electrical current through the threat, producing an aversive and deterring experience by activating afferents in potential predators.

Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes.

Ampullary organ electroreceptors excited by weak cathodal electric fields are used for hunting by both cartilaginous and non-teleost bony fishes. Despite similarities of neurophysiology and innervation, their embryonic origins remain controversial: bony fish ampullary organs are derived from lateral line placodes, whereas a neural crest origin has been proposed for cartilaginous fish electroreceptors. This calls into question the homology of electroreceptors and ampullary organs in the two lineages of jawed vertebrates. Here, we test the hypothesis that lateral line placodes form electroreceptors in cartilaginous fishes by undertaking the first long-term in vivo fate-mapping study in any cartilaginous fish. Using DiI tracing for up to 70 days in the little skate, Leucoraja erinacea, we show that lateral line placodes form both ampullary electroreceptors and mechanosensory neuromasts. These data confirm the homology of electroreceptors and ampullary organs in cartilaginous and non-teleost bony fishes, and indicate that jawed vertebrates primitively possessed a lateral line placode-derived system of electrosensory ampullary organs and mechanosensory neuromasts.

Compartmentation of the cerebellar cortex: adaptation to lifestyle in the star-nosed mole Condylura cristata.

The adult mammalian cerebellum is histologically uniform. However, concealed beneath the simple laminar architecture, it is organized rostrocaudally and mediolaterally into complex arrays of transverse zones and parasagittal stripes that is both highly reproducible between individuals and generally conserved across mammals and birds. Beyond this conservation, the general architecture appears to be adapted to the animal's way of life. To test this hypothesis, we have examined cerebellar compartmentation in the talpid star-nosed mole Condylura cristata. The star-nosed mole leads a subterranean life. It is largely blind and instead uses an array of fleshy appendages (the "star") to navigate and locate its prey. The hypothesis suggests that cerebellar architecture would be modified to reduce regions receiving visual input and expand those that receive trigeminal afferents from the star. Zebrin II and phospholipase Cß4 (PLCß4) immunocytochemistry was used to map the zone-and-stripe architecture of the cerebellum of the adult star-nosed mole. The general zone-and-stripe architecture characteristic of all mammals is present in the star-nosed mole. In the vermis, the four typical transverse zones are present, two with alternating zebrin II/PLCß4 stripes, two wholly zebrin II+/PLCß4-. However, the central and nodular zones (prominent visual receiving areas) are proportionally reduced in size and conversely, the trigeminal-receiving areas (the posterior zone of the vermis and crus I/II of the hemispheres) are uncharacteristically large. We therefore conclude that cerebellar architecture is generally conserved across the Mammalia but adapted to the specific lifestyle of the species.

An Optimized Biological Taser: Electric Eels Remotely Induce or Arrest Movement in Nearby Prey.

Despite centuries of interest in electric eels, few studies have investigated the mechanism of the eel's attack. Here, I review and extend recent findings that show eel electric high-voltage discharges activate prey motor neuron efferents. This mechanism allows electric eels to remotely control their targets using two different strategies. When nearby prey have been detected, eels emit a high-voltage volley that causes whole-body tetanus in the target, freezing all voluntary movement and allowing the eel to capture the prey with a suction feeding strike. When hunting for cryptic prey, eels emit doublets and triplets, inducing whole-body twitch in prey, which in turn elicits an immediate eel attack with a full volley and suction feeding strike. Thus, by using their modified muscles (electrocytes) as amplifiers of their own motor efferents, eel's motor neurons remotely activate prey motor neurons to cause movement (twitch and escape) or immobilization (tetanus) facilitating prey detection and capture, respectively. These results explain reports that human movement is 'frozen' by eel discharges and shows the mechanism to resemble a law-enforcement Taser.

Evolution of brains and behavior for optimal foraging: a tale of two predators.

Star-nosed moles and tentacled snakes have exceptional mechanosensory systems that illustrate a number of general features of nervous system organization and evolution. Star-nosed moles use the star for active touch--rapidly scanning the environment with the nasal rays. The star has the densest concentration of mechanoreceptors described for any mammal, with a central tactile fovea magnified in anatomically visible neocortical modules. The somatosensory system parallels visual system organization, illustrating general features of high-resolution sensory representations. Star-nosed moles are the fastest mammalian foragers, able to identify and eat small prey in 120 ms. Optimal foraging theory suggests that the star evolved for profitably exploiting small invertebrates in a competitive wetland environment. The tentacled snake's facial appendages are superficially similar to the mole's nasal rays, but they have a very different function. These snakes are fully aquatic and use tentacles for passive detection of nearby fish. Trigeminal afferents respond to water movements and project tentacle information to the tectum in alignment with vision, illustrating a general theme for the integration of different sensory modalities. Tentacled snakes act as rare enemies, taking advantage of fish C-start escape responses by startling fish toward their strike--often aiming for the future location of escaping fish. By turning fish escapes to their advantage, snakes increase strike success and reduce handling time with head-first captures. The latter may, in turn, prevent snakes from becoming prey when feeding. Findings in these two unusual predators emphasize the importance of a multidisciplinary approach for understanding the evolution of brains and behavior.

The neurobiology and behavior of the American water shrew (Sorex palustris).

American water shrews (Sorex palustris) are aggressive predators that dive into streams and ponds to find prey at night. They do not use eyesight for capturing fish or for discriminating shapes. Instead they make use of vibrissae to detect and attack water movements generated by active prey and to detect the form of stationary prey. Tactile investigations are supplemented with underwater sniffing. This remarkable behavior consists of exhalation of air bubbles that spread onto objects and are then re-inhaled. Recordings for ultrasound both above and below water provide no evidence for echolocation or sonar, and presentation of electric fields and anatomical investigations provide no evidence for electroreception. Counts of myelinated fibers show by far the largest volume of sensory information comes from the trigeminal nerve compared to optic and cochlear nerves. This is in turn reflected in the organization of the water shrew's neocortex, which contains two large somatosensory areas and much smaller visual and auditory areas. The shrew's small brain with few cortical areas may allow exceptional speed in processing sensory information and producing motor output. Water shrews can accurately attack the source of a water disturbance in only 50 ms, perhaps outpacing any other mammalian predator.

Early destruction of cockroach respiratory system and heart by emerald jewel wasp larvae.

In the 1880s, Henri Fabre was captivated by the "special art of eating", whereby a parasitoid wasp larva fed selectively on host internal organs, avoiding the heart (dorsal vessel) and tracheal system (respiratory system) to preserve life. In Fabre's words: "The ruling feature in this scientific method of eating, which proceeds from parts less to the parts more necessary to preserve a remnant of life, is none the less obvious"1. Subsequent investigators have reported the same for many parasitoid wasps2,3, including for the emerald jewel wasp (Ampulex compressa)4. Here it is reported that larval jewel wasps destroy the dorsal vessel and tracheae (respiratory system) in the thorax of their cockroach host (Periplaneta americana) at their earliest opportunity. Moreover, the broken tracheae release air into the host, which the larval jewel wasp inspires. An increase in larval chewing rate, cotemporaneous with the sudden release of air from the host's broken tracheae, suggests the larva taps into the host respiratory system to support its metabolism while rapidly consuming the host. VIDEO ABSTRACT.

Structure, innervation and response properties of integumentary sensory organs in crocodilians.

Integumentary sensory organs (ISOs) are densely distributed on the jaws of crocodilians and on body scales of members of the families Crocodilidae and Gavialidae. We examined the distribution, anatomy, innervation and response properties of ISOs on the face and body of crocodilians and documented related behaviors for an alligatorid (Alligator mississippiensis) and a crocodylid (Crocodylus niloticus). Each of the ISOs (roughly 4000 in A. mississippiensis and 9000 in C. niloticus) was innervated by networks of afferents supplying multiple different mechanoreceptors. Electrophysiological recordings from the trigeminal ganglion and peripheral nerves were made to isolate single-unit receptive fields and to test possible osmoreceptive and electroreceptive functions. Multiple small (<0.1 mm(2)) receptive fields, often from a single ISO, were recorded from the premaxilla, the rostral dentary, the gingivae and the distal digits. These responded to a median threshold of 0.08 mN. The less densely innervated caudal margins of the jaws had larger receptive fields (>100 mm(2)) and higher thresholds (13.725 mN). Rapidly adapting, slowly adapting type I and slowly adapting type II responses were identified based on neuronal responses. Several rapidly adapting units responded maximally to vibrations at 20-35 Hz, consistent with reports of the ISOs' role in detecting prey-generated water surface ripples. Despite crocodilians' armored bodies, the ISOs imparted a mechanical sensitivity exceeding that of primate fingertips. We conclude that crocodilian ISOs have diverse functions, including detection of water movements, indicating when to bite based on direct contact of pursued prey, and fine tactile discrimination of items held in the jaws.

Olfaction: underwater 'sniffing' by semi-aquatic mammals.

Terrestrial species that forage underwater face challenges because their body parts and senses are adapted for land--for example, it is widely held that mammals cannot use olfaction underwater because it is impossible for them to inspire air (sniff) to convey odorants to the olfactory epithelium. Here I describe a mechanism for underwater sniffing used by the semi-aquatic star-nosed mole (Condylura cristata) and water shrew (Sorex palustris). While underwater, both species exhale air bubbles onto objects or scent trails and then re-inspire the bubbles to carry the smell back through the nose. This newly described behaviour provides a mechanism for mammalian olfaction underwater.

Tentacled snakes turn C-starts to their advantage and predict future prey behavior.

Fish are elusive prey with a short-latency escape behavior--the C-start--initiated to either the left or right by a "race" between 2 giant Mauthner neurons in the fish brainstem. Water disturbances usually excite the ipsilateral neuron, which massively excites contralateral motor neurons, resulting in a rapid turn away from striking predators. Here, it is reported that tentacled snakes (Erpeton tentaculatus) exploit this normally adaptive circuitry by feinting with their body, triggering the Mauthner cell that is furthest from their head milliseconds before a ballistic strike is initiated. As a result, fish that were oriented parallel to the long axis of the snake's head most often turned toward the approaching jaws, sometimes swimming directly into the snake's mouth. When strikes were instead directed at fish oriented at a right angle to the snake's head, snakes anticipated future fish behavior by striking to where fish would later be if they escaped from the snake's body feint, which fish usually did. The results provide an example of a rare predator taking advantage of a prey's normally adaptive escape circuitry and suggest that the snake's sensory-motor system is adapted to predict future behavior.

Hypersensitivity to contact inhibition provides a clue to cancer resistance of naked mole-rat.

The naked mole-rat is the longest living rodent with a maximum lifespan exceeding 28 years. In addition to its longevity, naked mole-rats have an extraordinary resistance to cancer as tumors have never been observed in these rodents. Furthermore, we show that a combination of activated Ras and SV40 LT fails to induce robust anchorage-independent growth in naked mole-rat cells, while it readily transforms mouse fibroblasts. The mechanisms responsible for the cancer resistance of naked mole-rats were unknown. Here we show that naked mole-rat fibroblasts display hypersensitivity to contact inhibition, a phenomenon we termed "early contact inhibition." Contact inhibition is a key anticancer mechanism that arrests cell division when cells reach a high density. In cell culture, naked mole-rat fibroblasts arrest at a much lower density than those from a mouse. We demonstrate that early contact inhibition requires the activity of p53 and pRb tumor suppressor pathways. Inactivation of both p53 and pRb attenuates early contact inhibition. Contact inhibition in human and mouse is triggered by the induction of p27(Kip1). In contrast, early contact inhibition in naked mole-rat is associated with the induction of p16(Ink4a). Furthermore, we show that the roles of p16(Ink4a) and p27(Kip1) in the control of contact inhibition became temporally separated in this species: the early contact inhibition is controlled by p16(Ink4a), and regular contact inhibition is controlled by p27(Kip1). We propose that the additional layer of protection conferred by two-tiered contact inhibition contributes to the remarkable tumor resistance of the naked mole-rat.

Tentacled snakes.

Catania provides an introduction to tentacled snakes and their ingenious ability to capture fish.

Compartmentation of the cerebellar cortex in the naked mole-rat (Heterocephalus glaber).

Despite the apparent uniformity in cellular composition of the adult mammalian cerebellar cortex, it is actually highly compartmentalized into transverse zones and within each zone further subdivided into a reproducible array of parasagittal stripes. This basic cerebellar architecture is highly conserved in birds and mammals. However, different species have very different cerebellar morphologies, and it is unclear if cerebellar architecture reflects taxonomic relations or ecological niches. To explore this, we have examined the cerebellum of the naked mole-rat Heterocephalus glaber, a burrowing rodent with adaptations to a subterranean life that include only a rudimentary visual system. The cerebellum of H. glaber resembles that of other rodents with the remarkable exception that cerebellar regions that are prominent in the handling of visual information (the central zone, nodular zone, and dorsal paraflocculus) are greatly reduced or absent. In addition, there is a notable increase in size in the posterior zone, consistent with an expanded role for the trigeminal somatosensory system. These data suggest that cerebellar architecture may be substantially modified to serve a particular ecological niche.

Asymptotic prey profitability drives star-nosed moles to the foraging speed limit.

Foraging theory provides models for predicting predator diet choices assuming natural selection has favoured predators that maximize their rate of energy intake during foraging. Prey profitability (energy gained divided by prey handling time) is an essential variable for estimating the optimal diet. Time constraints of capturing and consuming prey generally result in handling times ranging from minutes to seconds, yet profitability increases dramatically as handling time approaches zero, providing the potential for strong directional selection for increasing predator speed at high encounter rates (tiny increments in speed increase profitability markedly, allowing expanded diets of smaller prey). We provide evidence that the unusual anatomical and behavioural specializations characterizing star-nosed moles resulted from progressively stronger selection for speed, allowing the progressive addition of small prey to their diet. Here we report handling times as short as 120 ms (mean 227 ms) for moles identifying and eating prey. 'Double takes' during prey identification suggest that star-nosed moles have reached the speed limit for processing tactile information. The exceptional speed of star-nosed moles, coupled with unusual specializations for finding and eating tiny prey, provide new support for optimal foraging theory.

Chemoarchitecture of layer 4 isocortex in the American water shrew (Sorex palustris).

We examined the chemoarchitecture of layer 4 isocortex and the number of myelinated nerve fibers of selected cranial nerves in the American water shrew (Sorex palustris). This study took advantage of the opportunity to examine juvenile brain tissue, which often reveals the most distinctive cortical modules related to different sensory representations. Flattened cortical sections were processed for the metabolic enzyme cytochrome oxidase, revealing a number of modules and septa. Subdivisions related to sensory representations were tentatively identified by performing microelectrode recordings in a single adult shrew in this study, combined with microelectrode recordings and anatomical findings from a previous investigation. Taken together, these results suggest that characteristic chemoarchitectonic borders in the shrew neocortex can be used to delineate and quantify cortical areas. The most obvious subdivisions in the water shrew include a relatively small primary visual cortex which responded to visual stimuli, a larger representation of vibrissae in the primary somatosensory cortex, and a prominent representation of oral structures apparent in the more rostral-lateral cortex. A presumptive auditory area was located in the far caudal cortex. These findings for the cortex are consistent with counts from optic, auditory and trigeminal nerves, suggesting that somatosensory inputs dominate the shrew's senses whereas visual and auditory inputs play a small role in navigation and in finding prey. More generally, we find that shrews share unusual features of cortical organization with moles, supporting their close taxonomic relationship.

Updated neuronal scaling rules for the brains of Glires (rodents/lagomorphs).

Brain size scales as different functions of its number of neurons across mammalian orders such as rodents, primates, and insectivores. In rodents, we have previously shown that, across a sample of 6 species, from mouse to capybara, the cerebral cortex, cerebellum and the remaining brain structures increase in size faster than they gain neurons, with an accompanying decrease in neuronal density in these structures [Herculano-Houzel et al.: Proc Natl Acad Sci USA 2006;103:12138-12143]. Important remaining questions are whether such neuronal scaling rules within an order apply equally to all pertaining species, and whether they extend to closely related taxa. Here, we examine whether 4 other species of Rodentia, as well as the closely related rabbit (Lagomorpha), conform to the scaling rules identified previously for rodents. We report the updated neuronal scaling rules obtained for the average values of each species in a way that is directly comparable to the scaling rules that apply to primates [Gabi et al.: Brain Behav Evol 2010;76:32-44], and examine whether the scaling relationships are affected when phylogenetic relatedness in the dataset is accounted for. We have found that the brains of the spiny rat, squirrel, prairie dog and rabbit conform to the neuronal scaling rules that apply to the previous sample of rodents. The conformity to the previous rules of the new set of species, which includes the rabbit, suggests that the cellular scaling rules we have identified apply to rodents in general, and probably to Glires as a whole (rodents/lagomorphs), with one notable exception: the naked mole-rat brain is apparently an outlier, with only about half of the neurons expected from its brain size in its cerebral cortex and cerebellum.