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Invertebrate solutions for sensing gravity

2009; Elsevier BV; Volume: 19; Issue: 5 Linguagem: Inglês

10.1016/j.cub.2008.12.024

1879-0445

John A. Bender, Mark A. Frye,

Children's Physical and Motor Development

Gravity is fundamental to life on Earth — plants and animals alike must compensate for the force of gravity to maintain a right-side-up posture. Accordingly, detecting gravity may be one of the first sensory capacities to have evolved in animals. Furthermore, whether running, swimming, or flying, animals that move around with coordination and direction must also account for gravity during locomotion. To estimate their orientation relative to the earth, humans and many other animals are highly reliant on vision: the sky is light, the ground is dark, the horizon is horizontal, and many environmental edges are vertical. However, we can also walk normally in the dark, yet a person who sees well but loses the ability to detect gravitational forces acting on his or her limbs becomes severely impaired. How can an organism measure gravity? Newtonian physics provide a convenient conceptual framework. Although the force of gravity is effectively constant, its vector direction relative to an animal's body varies with any rotation of the body. There are two general strategies used for estimating the gravitational vector: integrating directional forces measured across the whole body or measuring acceleration at a single point (Figure 1). These solutions are not mutually exclusive and can be implemented in tandem. In humans, muscle spindles and Golgi organs measure tension on joints while the vestibular system senses rotational velocity and acceleration, providing complementary signals necessary to maintain the relatively unstable bipedal posture. Just as we mammals have evolved highly acute sensory mechanisms to detect gravity acting on our bodies and appendages, so have invertebrates developed these capacities. For invertebrates, perceiving gravity's pull presents a number of fascinating challenges, which are accentuated by their diminutive stature. For tiny animals, the gravitational force can be vanishingly small, requiring exquisite sensitivity in order to measure it. Invertebrates have correlates of each of the gravity-sensing systems found in humans, some by shared ancestry and some by convergent evolution. Additional exotic solutions highlight the performance demands of invertebrate locomotion. Here we will discuss strategies for gravity detection by invertebrates during terrestrial, aquatic, and aerial locomotion. Notwithstanding the obvious architectural and developmental disparities, we shall, where possible, compare their solutions to our own. In the absence of wind, an animal standing at rest is acted upon only by the force of gravity. An animal might not explicitly calculate the global gravitational vector per se, but rather may actively modulate local joint angles and torques to implicitly compensate for gravity's pull. In many instances, insects and crustaceans measure the angles of their appendages' joints using clusters of mechanosensitive hairs, called hair plates. In one such cluster, the prosternal organ of insects, a grove of hairs sprout from the forward part of the thorax (Figure 2). As the animal's head moves, it brushes against these hairs. By monitoring the deformation of each hair, the animal can precisely determine the orientation of its head relative to its thorax. The prosternal organs are especially well-developed in highly visual animals such as flies and mantids — animals for which the body-centered location of visual stimuli is very important. Hair plates also serve similar roles on leg, wing, and body joints. In addition to measuring joint position, invertebrates also have specializations for measuring joint load. Whereas our bones have no active sensory capacity and instead our sensors are imbedded in surrounding, soft tissues, many invertebrates are equipped with sensory arrays embedded in the exoskeleton at strategic points and with specific orientations. Called campaniform sensilla in insects, lyriform organs in arachnids and centipedes, and cuticular stress detectors in crustaceans, these are similar in mechanism to the stretch and pressure sensors in human skin. It is not known whether these receptors were inherited from a common ancestor, but they clearly have convergent functions. Each of these invertebrate stretch receptors is composed of an oval-shaped slit which can be deformed by pressure along its short axis. This induced deformation leads to ion flux, which is transduced and relayed to the central nervous system by dedicated afferent neurons. Insects possess additional stretch receptors called scolopidial organs. A subset of these, called chordotonal organs, are attached to inflexible connective tissue spanning joints inside the exoskeleton. Scolopidial organs act as strain sensors, measuring the distance between their attachment points as well as its rate of change. Joint angle and load can also be measured less directly. A class of sensors called muscle receptor organs may encode muscle stretch in a manner similar to the muscle spindles in our own skeletal muscles, and another group known only as multipolar receptors may act like our Golgi tendon organs — the very sensors stimulated by tapping the tendon beneath your kneecap. In addition, liquid-feeding insects are known to use stretch receptors that span segments of the abdomen in order to monitor distension (and thus satiety). These could be used to regulate posture more generally, but none of these sensor types has been studied extensively. Finally, some insects have dedicated gravity sensors. The cerci (singular: cercus) are cone-shaped appendages extending horizontally from the rear of an insect, especially prominent in crickets and earwigs. In many species, these are covered with mechanosensory hairs which monitor air currents in the animal's vicinity. Like the antennae, the cerci can also include chemosensors. As if that were not enough, the cerci of at least some crickets and cockroaches have specialized, club-shaped hairs that deflect like a pendulum under gravity's pull. These hairs are important for gravity responses in crickets, but their effects have not been explored in other insects. Animals that spend most of their time underwater are subject to different physical constraints than those that dwell on land. In an aqueous environment, the ability of an animal to measure gravity using joint-based sensors is limited. This is due in part to the high viscosity of water relative to air, which serves to dampen the effects of gravity on the body. The buoyancy of the animal's body diminishes gravitational signals even further, potentially beyond the point of detection. Self-motion in a high-viscosity medium also enhances drag forces, which stimulate the same sensors as gravity. For these reasons, gravity is one of the least prominent forces acting on aquatic locomotion. Though its influence may be small, gravity does, of course, exist underwater and in many situations it is important for animals to measure. For example, food may not be distributed evenly in the vertical dimension, and oviposition sites may be restricted to the floor. One way to counteract the problem of decreased gravitational forces due to buoyancy and viscosity is to utilize a sensor with a higher density than the rest of the body, such that gravity's effects may be more easily discerned. Many marine invertebrates, including crustaceans and echinoderms, have organs called statocysts consisting of a mineral gel-filled sac lined with sensory hairs. The dynamics of the heavy mineral mass are more sensitive to gravity than are the lower-density body tissues, and as expected, the associated sensory hairs respond physiologically to accelerations. Statocysts are at least analogous and likely homologous to the otolith organs of the vertebrate inner ear. They emerged very early in animal evolution, appearing in hydromedusae before the divergence of Bilateria, and are observed in virtually every metazoan phylum. The situation for flying invertebrates, especially very small ones, is physically comparable to that encountered by swimming animals. Their size and speed make air seem viscous, making gravity harder to distinguish from other forces such as drag. Yet, unlike swimming, flight stability does not benefit from added buoyancy. Nevertheless, animals predominantly fly right-side-up, suggesting that they somehow determine the direction of the gravity vector. Some of this stability may not require active sensation; for instance, an insect with a heavy abdomen will tend to passively maintain a 'nose-up' posture. However, many airborne insects, such as houseflies or dragonflies, regularly careen into corkscrews and barrel rolls during their aerobatic pursuits of prey or conspecifics, thus requiring a more active sense of their own body angle with respect to the earth. Many flying invertebrates are highly visual and use this modality to help maintain an upright posture, but some nocturnal moths and mosquitoes can remain airborne in complete darkness. One of the means by which they may do so is by measuring accelerations acting on their bodies. Diptera (two-winged flies, gnats, and mosquitoes) and a little-known order of insects called the Strepsiptera are equipped with highly specialized acceleration sensors, called halteres, in place of one of their wing pairs. These small, club-shaped organs actively beat back and forth like the wings (Figure 3A), setting up a situation whereby a rotation of the animal's body produces a Coriolis force on the vibrating haltere, acting just like a gyroscope. Small deflections of the haltere from its stroke plane produce strain on the haltere's stalk. These strains are transduced into electrical signals by a field of campaniform sensilla near the base of the haltere. Afferent neurons from these sensors are electrically coupled to motor neurons of the wing-steering muscles, providing a very fast feedback loop by which flies sense and react to body accelerations. In principle, any oscillating appendage can be used to detect Coriolis forces, which are formally represented by the cross-product of the momentum of the appendage and the angular velocity of the body. For instance, in Lepidoptera (moths and butterflies), the antennae may be used as force sensors during flight, in addition to their other functions as 'noses' and 'ears'. Scolopidial organs at the base of the antenna detect passive deflections and respond specifically to vibrations near wing-beat frequency and at twice this rate, corresponding to signals generated during flight. Indeed, the mass of the antennae is required for the maintenance of normal flight in the hawk moth. Moths with amputated antennae crash into walls, but reattaching either the severed antennae or equivalently heavy sticks rescues near-normal flight performance. A complication of studying gyroscopic mechanisms, whether in moths or flies, is disentangling Coriolis forces from inertial forces. The inertia produced by merely swinging a haltere back and forth is strong and acts in the plane of its stroke. Several fields of campaniform sensilla monitor this 'planar' inertia. (Figure 3B, top). In addition, rotation of the animal's body leads to inertial forces acting on the haltere in proportion to its length and mass (Figure 3B bottom). However, this nonplanar inertia is not a Coriolis force, which acts only on a mass moving orthogonally to the axis of rotation, in proportion to the velocity of the moving mass (Figure 3B, bottom). To understand the difference, imagine holding your arms out from your sides and then twisting your torso. The resulting strain in your shoulders is inertial, due to the mass of your arms. However, to produce a Coriolis force with the same direction vector, you would instead need to flap your arms rapidly up and down and then bow at the waist. In this case, because your arms are so massive and are moving so slowly (relative to a flying insect), the Coriolis force is still very small compared to the inertial acceleration you feel. Both inertial and Coriolis forces are potentially important to a flying animal, and both can be detected by the same biological sensors. However, the two may have very different magnitudes and will develop during different phases of the stroke. A fly's halteres beat roughly 150° up and down. The inertial forces produced by yaw (side-to-side) rotation of the body could have the same vector direction as the Coriolis forces, but the inertial accelerations are much smaller and 90° out of phase. The haltere responses better match the theoretical estimates of the Coriolis forces than the inertial forces. A moth's antennae are actively held in place relative to the head, but also vibrate up and down passively as the animal's body pitches slightly forward and back with each wing stroke. However, because of their larger body size, lower wing-beat frequency, and relatively small movements of the antennae, the inertial forces (proportional to the length of the animal) may be larger than the Coriolis forces (proportional to the angular velocity of the antennae). Nevertheless, by either mechanism, gravitational accelerations of the body can be detected and this information is presumably used to maintain flight stability. The mechanisms by which other types of flying insects such as bees, beetles, or locusts might make use of acceleration measurements is unknown. When an animal is moving, sensing external forces can become quite complicated because there are three main sources of force-related sensations during locomotion. First, the animal's muscles generate torque on its limbs, and the interactions of the limbs and body with the substrate or medium produce additional forces. Second, gravity acting on its mass produces downward forces to account for. Finally, environmental sources such as air or water currents, other animals, or moving objects could give rise to yet more force signals. The latter are generally the stimuli requiring the most urgent action, but how can they be distinguished from the other types? One prominent school of thought is that animals implement a so-called 'forward model' of the expected effects of an action. In this scheme, each motor command produces an output copy — the inverse of the predicted sensory input resulting from the movement — which is stored to be compared with the actual, sensed information. The neural correlates of these output copy signals (referred to as an 'efference copy') are difficult to distinguish from the motor commands themselves, and as such have only been demonstrated in a select few cases. Assuming that the effects of self-motion can be accounted for with efference copy, this then leaves the animal with the challenge of discriminating gravity from other environmental stimuli. One strategy would be to correct for all external perturbations, regardless of their source. This solution would be sufficient to maintain posture or elevation, but then how would an animal determine which stimuli merit a more interactive response? This question is relevant not just to invertebrates, but to humans as well. Possibly, the answer lies in the fact that gravity is constant, whereas stimuli requiring a change in behavior are likely to be unpredictable and thus more salient. Intriguingly, making the distinction between irrelevant and evocative stimuli requires two different neural responses to gravity: postural feedback always needs to account for gravitational pull, but task-level control should be adaptive and ignore such static inputs. We share a physical world with invertebrates, and as such we share the need to detect the effects of air and water currents, temperature, and gravity. Challenged by size and exhibiting tremendous evolutionary diversity, invertebrates exhibit some clever sensory solutions not available to us mammals. However, lessons learned from studies on invertebrate body senses also highlight convergent mechanisms for solving physical problems common to various taxa. Comparative research therefore holds value not just for more fully clarifying the diversity of solutions, but also for understanding how and why we humans arrived at our particular ones.