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Sensory guidance in arthropod behaviour: Common principles and experimental approaches
Camp. Bio&em. Physiot. Vol. WA, No. 4, pp. 625432, Printed in Great Britain
1993
MINI
0300-9629/93 $6.00 + 0.00 Q 1993 Pergamon Press Ltd
REVIEW
SENSORY GUIDANCE IN ARTHROPOD BEHAVIOUR: COMMON PRINCIPLES AND EXPERIMENTAL APPROACHES W. J. P. BARNES Department of Zoology, University of Glasgow,
Glasgow
G12 8QQ,
U.K.
(Received 2 September 1992; accepted 26 October 1992) Abstract-l. Ex~rimental approaches to the study of sensory guidance m~hanisms in arthropods are reviewed. The classical techniques of ethology and neurophysiology combine with controi systems analysis and computer modelling to cast new light on the ways in which these animals orientate, steer, navigate, learn routes and find a mate. 2. Common principles of sensory guidance include negative feedback, reafference, multisensory convergence and matching. Occurring in functionally diverse systems, they relate to the accuracy and efficiency of sensory guidance, and reflect the fact that natural selection acts to maximise the return from any investment.
INTRODUCIION
Sensory guidance, the way in which animals find their way about the world, is a fascinating area of research. To the zoologist, the intricate physiological and behavioural adaptations that animals have evolved to recognise where they are, find a mate, or simply get from A to B provide much to marvel at. No less interested in this area are neuroetholo~sts trying to understand how behaviour is controlled by the nervous system. When the behaviour in question is directed towards a goal, and involves well-defined sensory cues, the task of gaining some physiological understanding of it is that much easier. Finally, although most research in this area is basic as opposed to applied, it is already clear that this field is relevant to robotics. For instance, an understanding of visual sensory guidance mechanisms in arthropods is likely to be crucial for the design of new hardware for devices that move in cluttered worlds to help them avoid obstacles and reach their goals (Horridge, 1992). Indeed, one such robot has already been constructed by Franceschini et al. (1992) on the principles of insect vision, which avoids objects by visually evaluating its own motion relative to that of the environment. The study of behaviour defines &he sensory guidance mechanisms that animals use. Indeed, the success of the majority of the studies reported here depends upon behavioural work that has specified the task that the animal accomplishes. In some cases, the behavioural investigation leads directly to models of how the behaviour is carried out; in others, it forms the basis for neurophysioiogical studies. In
such neurophysiological studies, visual orientation in flies being a good example (Egelhaaf et al., 1988), a knowledge of the relationship between stimulus and response allows one to specify the computations that are required before the task can be carried out. Indeed, in this example, behavioural experiments led to a precisely formulated model for movement detection (Hassenstein and Reichardt, 1956; Borst and Egelhaaf, 1989). This model was then used to formulate hypotheses for neural function that permitted the design of experiments that could specify the functions of neurones and pathways. In such a manner, a formal model can develop into a model based on neurophysiological data. Sensory guidance should not, however, be viewed purely in terms of sense organ function. ultimately, sensory systems must progress to motor systems. Viewed as sensory-motor networks, sensory guidance mechanisms may provide clues to the operational principles that govern the integration of sensory and motor pathways. At first sight, the task may appear difficult. How, for instance, are the neural messages that signal deviations from course used by a flying locust to produce correcting manoeuvres? But the solution often turns out to be remarkably simple. The locust gates the deviation signals at wing beat frequency so that they only reach the motor neurones during the appropriate phase of the wing beat cycle for the flight correction to be carried out (Rowe11 et al., 1985). As in many other sensory guidance systems, a short cut has evolved that provides an elegantly simple solution. As well as providing an overview of the reviews that follow, this paper reviews the history of the study 625
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of sensory guidance mechanisms in animals and makes a case for their being common principles governing sensory guidance in functionally diverse systems. Many of these principles can be related to the accuracy and efficiency of these guidance systems, and reflects the fact that natural selection acts to maximize the return from any investment.
HISTORICAL
APPROACHES TO THE SENSORY GUIDANCE
STUDY
OF
Classification of orienting movements Some activities of animals are performed without orientation to the environment. At the reflex level, retraction of a crab’s eye into its socket, once elicited by the appropriate stimulation, has no special spatial ~lationship to objects in the environment (Sandernan, 1967). Similarly with some examples of more complex behaviour. For instance, grooming behaviour in Drosophila (or for that matter a number of other insects), once triggered by some external or more often internal stimulus, proceeds in a more or less stereotyped manner without reference to the environment (Szebenyi, 1969). For the most part, however, animals regulate their activities in a spatial relationship with the environment. Locomotion is guided towards goals; escape responses directed away from predators; courtship aimed at a mate; prey-catching movements directed towards prey. Such orientation responses frequently exploit the predictable nature of environmental stimuli. Olfactory cues are carried downstream or downwind by water or wind; the horizon is horizonArWlclsl Bark
tal; gravity acts downwards. It has become customary to separate orientation responses into two broad categories: (1) primary orientation, the assumption of the basic position of the body in space; and (2) secondary orientation, orientation or movement in space with a particular relationship to environmental stimuli. As an example of primary orientation, let us consider the stimuli which two species of moth (~elano~op~~a canaduria and Catocafa ultron~u) utilize to align prominent markings on their wings with vertical fissures on the bark of trees. In these experiments, carried out by Sargent (1969), the moths were allowed to settle on artificial bark, aligned either vertically or horizontally (Fig. I). The experiment was then repeated but with tactile cues no longer available, the artificial bark being covered by a sheet of clear plastic. The results show that Mehnolophia orients using tactile cues provided by the fissures themselves and thus fails to show a preferred orientation when no tactile cues are available, while Catocala simply responds to gravity and always rests head down. The study of secondary orientation has been much influenced by the work of Fraenkel and Gunn, whose monograph “The Orientation of Animals” was first published in 1940. In Fraenkel and Gunn’s analysis, orientation responses are classified according to the m~hanism involved. The basic distinction in this scheme is between kineses and taxes. In the former, animals respond to differences in environmental stimulation with differential rates of turning or speeds of movement. As a result, they decrease the time they AItitlcisl Bark Covered by Trsnspsrent
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Fig. 1. Experimental analysis of stimuli used by the moths ~e~aff~~o~~jucunu&ric and Curoculu ultrotriu to align prominent markings on their wings with vertical fissures on the bark of trees. In the first experiment (left), the moths were allowed to settle on artificial bark (strips of thick tape). aligned either vertically or horizontally. The numbers represent the numbers of moths aligning their wings either parallel with or at right angles to ridges on the bark as indicated on the diagrams. In the second experiment (right), which was otherwise identical to the first, a piece of transparent perspex was placed over the strips of tape before the moths were released. After Sargent (1969).
Sensory guidance in arthropod behaviour
spend in unfavourable habitats and increase the time spent in favourable habitats compared to randomly moving individuals, but achieve this without directional movement. By such mechanisms as these, woodlice (Porce[lio scaber) tend to aggregate in moist places, and the human body louse in smelly, warm ones (Wigglesworth, 1941). In contrast, a taxis is defined as an orientation response in which the animal moves at a particular orientation to the stimulus-at a particular angle to the sun, towards a source of sound etc. More detailed levels of classification depend on the nature of the stimulus to which the animal is responding4.g. geotaxis (gravity) or phototaxis (light)--or on the way in which the sensory information is obtained. In a klinotuxis, the direction of movement is determined by successive comparisons of the stimulation impinging on its receptors as they are turned from side to side, while in a tropotaxis (Fig. 2A) the sensory inputs received by left and right sense organs are balanced simultaneously. A telotaxis, on the other hand, does not depend upon simple balance; if there are two sources of stimulation, the animal orients to one or the other. Figure 2B shows this for hermit crabs orienting to one or other of two lights. Orientation need not be directly towards or away from the stimulus. In a menotaxis or light compass response, the orientation is at a constant angle to the stimulus direction, while in a mnemotaxis it involves a memory of local landmarks (cf. Collett, 1993 in this issue). This system of labelling has, over the years, provided good shorthand descriptions for different orientation behaviours, and brought about a degree of order to the huge diversity of different responses. However, except at its most basic level, it has probably outlived its usefulness. Why is this so? In part, it is because this system of classification does not guarantee that responses bearing the same label share the same physiological mechanism. Assignment of a particular label to an orientation response depends on an assessment of the role of individual receptor organs, not on an analysis of all that happens between stimulus and response. Fraenkel and Gunn’s classification is thus useful insofar as it refers to
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different types of spatial manoeuvre, but can be dangerous if taken to imply types of physiological mechanism (Hinde, 1970). Secondly, the different categories have been largely analysed in laboratory studies in simplified situations. As will become clear in the following reviews, studies carried out in the field or in more complex laboratory situations show Fraenkel and Gunn’s categories to be of limited use. The responses tend to be complex, involving a number of senses, and different types of orientation occur together or in close succession. Thus they do not fall conveniently into any of Fraenkel and Gunn’s categories. Indeed, it is probably fair to say that, in the same way that reflexes form components of many mechanisms of motor control, so Fraenkel and Gunn’s classification at best describes the building blocks from which whole sensory guidance mechanisms are constructed. Analysis of orientation in terms of control systems For a more detailed analysis of orientation mechanisms, simple labels become inadequate, and the results can only be expressed in terms of the actual relationships between stimulus and response. This is the field of the control systems engineer. Indeed, the application of control theory to this field of biology, pioneered by Mittelstaedt in the early 1960s (Mittelstaedt, 1960, 1961, 1962, 1964), has made a major contribution to our understanding of many orientation behaviours. The control theory or cybernetic approach is an example of a “black box” approach, viewing the system as a whole and describing it mathematically from its input/output characteristics; i.e. we try to find a set of equations or a model to fit the relation by which the behavioural output is governed by the stimulus over a range of stimulus variables such as intensity, frequency, spatial pattern and so on. Applying these methods to orientation behaviour, one can distinguish a sensory system or systems that receive information from the outside world, a motor system for changing course or orientation, and mechanisms for relating the two. What Mittelstaedt (1964) was able to show was that these different
B L
L2
Fig. 2. A: tropotaxis tracks of photopositive woodlice Armadi//idum orienting with respect to two lights of equal intensity. After Miiller (1925). 9: telotaxis tracks of hermit crabs orienting in an equivalent experimental situation. After Fraenkel and Gunn (1940).
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systems could be linked together in either of two fundamentally different ways. If the movement produced by the effecters does not affect the stimulus received by the animal, the system is said to be open loop. For instance, male fireihes orient to flashes of light produced by females. Since the males orient correctly even though they do not start to turn until after the female’s flash is over (Mast, 1912), the output (the change in the orientation) cannot affect the input (the angle between the flash and the body axis). This system, called a uniiaterai mesh, is illustrated in Fig. 3A. Another good example of an open loop system is provided by the strike of the praying mantis, analysed by Mittelstaedt (1962). Information about the direction of prey is perceived by the compound eyes. The output of the system is the deviation of the strike from the body axis. In theory, information regarding the direction of the strike could be fed back into the system by the eyes while the strike is in progress, but in practice the transmission time for such a correction is longer than the time taken to extend the forelegs. The system is thus akin to firing a gun; you cannot change the direction of the bullet once it has left the barrel! In contrast to the above, systems in which the output influences the input (and which thus involve feedback) are said to be ciosed loop. Visual tracking responses (see Land, 1992) and optomotor responses are good examples of closed loop control systems. As illustrated in Fig. 3B, which represents the optomotor
A. Unilateralmesh -
reaction of the fly, the system output (the rotation of the fly) is fed back and subtracted from the input (the rotation of the striped pattern) because the eyes move with the body. The velocity actually seen by the fly is thus the input minus the output, and the system can be said to incorporate a negative feedback loop (Mittelstaedt, 1964). From these descriptions, it will be apparent that the correct functioning of open loop systems depends upon the precision of their calibrations, while closed loop systems allow continuous correction of errors. Additionally, closed loop systems are able to correct for disturbances (e.g. the effect of wind on a flying insect), a property not shared by open loop systems. The control theory approach is now an established feature of the orientation literature. In this collection of reviews, it is utilized in the study of the eye movements of crabs (Barnes and Nalbach, 1993). It does not offer a complete solution, but it does give one an understanding of the system as a whole. Thus it remains an important step in the analysis of many sensory guidance mechanisms. It has been argued that such non-physiological models are a poor substitute for physiological ones, in that they fail to provide any understanding at the neuronal level (Hansel], 1985). This is not altogether fair. They are useful, even if they do not provide a complete story. Some behaviours such as flight steering in locusts (see Reichert, 1993 in this issue) do lend themselves to the neurophysiological approach; others such as landmark orientation in bees (see Collett, 1993 in this issue) do not (at least yet!). The same argument can be used in the study of memory. The cellular and molecular approaches can hope to elucidate what happens at particular synapses, but they are ill equipped to understand how memories are organized in the brain. Recent approaches to the stuu(v of sensory guidance
Et. Negative feedback loop
Fig. 3. Control systems for orientational homeostasis. A. open loop system (unilateral mesh) for orientation of male fireflies to flash of female. zdeviation of flash of female firefly from body axis of male. y-change in orientation of male firefly. Error (x) is zero if the product of B, and Bt (the systems for detecting the deviation of the flash and for turning the body, respectively) is equal to I, for then y will equal z. B. Closed loop system involving negative feedback for fly optomotor response. z-rotational velocity of striped pattern rotated around the fly. y-rotational velocity of fly. Error (x) is low if the product of B, and B, (the systems for detecting movement and for turning the fly, respectively) is high. Modified from Mittelstaedt (1964).
And so I bring this brief historical survey up to the present day. We are no longer satisfied with a mere classification of orientation or navigation mechanisms; nor are most of us completely content with the models of the control systems engineer, useful though they are. Instead, we are using a variety of approaches, anatomical, physiological, biomechanical and behavioural, to try to understand precisely how sensory guidance mechanisms work. The neurophysiological approach to sensory guidance has been made possible by a number of important technical advances. These include advances in microelectrode recording techniques, which enable one to record intracellularly from single neurones in the central nervous system, and the development of dyes such as Lucifer Yellow (Stewart, 1981) which, when injected into the cell through the microelectrode, allow the neurone’s anatomy to be fully visualized. Arthropods have proved particularly advantageous for such studies, both because large numbers of neurones can be
individually
recognized and because they are very
Sensory guidance in arthropod behaviour tolerant of dissection. This means that many components of orientation behaviours can be studied in preparations sufficiently dissected to permit microelectrode recording. Advances in the availability, user-friendliness and sophistication of computers has also played an important part in these studies. They have allowed more complicated forms of data analysis, and led to an increase in the use of computer simulation as a way of testing models of sensory guidance mechanisms. But most of the studies that are reviewed here are at least partly behavioural, a field in which the development of ideas as much as of techniques has led to the rapid advances that have occurred. Thus it is appropriate to emphasise the ingenuity of the scientists themselves. For this is not a field where scientists are mere technicians gathering routine data, but one where inventiveness and lateral thinking are essential requirements for success. The reviews that follow illustrate the variety of sensory guidance mechanisms used by arthropods. The behavioural approach is exemplified by the study of navigation by bees using polarized light (Rossei, 1993), landmark guidance in insects (Collett, 1993) and courtship behaviour in spiders (Barth, 1993). In different ways all are remarkable behaviours. The bees use of polarized light employs a sense that we humans lack; their use of landmarks requires learning and memory of the relative positions of features of their environment, which is no mean feat for an animal with such a simple nervous system; while courtship in different members of the spider genus, Cupiennius, involves communication by way of vibration signals transmitted through the leaves of the plants in which they live. The study of the eye movements of freely moving crabs (Barnes and Nalbach, 1993), where it appears that the crabs are performing a simple form of flow field analysis, lends itself to the control systems approach, since inputs and outputs can be precisely measured. Indeed, in flies (Egelhaaf and Borst, 1993) the study of visual orientation has been taken a stage further, to the analysis of the neurophysioiogicai mechanisms used to generate optomotor and tracking responses. Such neurophysiological approaches are appropriate wherever components of sensory guidance can be obtained in partly dissected preparations. The equilibrium responses of lobsters (Neil, 1993) have been successfuliy studied in this manner, as has the control of flight orientation in locusts (Reichert, 1993). Indeed, the latter study probably provides the most detailed understanding at the neural level that we have of any sensory guidance mechanism. Amongst several further examples, computer simulations have played an important role in the study of the mechanisms of motion detection in flies (Egeihaaf and Borst, 1993), while biomechanical studies have played a role in the study of spider pre-copulatory behaviour (Barth, 1993) and crustacean equilibrium responses (Neil, 1993). As well as illustrating these different
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experimental approaches to sensory guidance, the studies that comprise this issue of Comparative Biochemistry and Physiology have been chosen to illustrate common features that are shared by many such behaviours. These are briefly discussed below. COMMON
FEATURES OF SENSORY GUIDANCE MECHANISMS
Negative feedback
The relevance of control systems analysis to the study of sensory guidance is no accident. Sensory guidance mechanisms are control systems and, moreover, control systems in which the critical variables can be measured and manipulated (Mittelstaedt, 1964). A few of these systems invoive open loop control. The strike of the praying mantis and the mechanism by which fireflies find a mate have already been mentioned. A further example is provided by the prey capture behaviour of the semi-aquatic spider, Dolomedes, which obtains information on the direction and distance of its prey from the ripples they generate on the water surface (Bl~kmann, 1988). The vast majority, however, are closed loop systems incorporating negative feedback. In many cases (e.g. optomotor reactions and visual tracking-see Barnes and Nalbach, 1993 in this issue and Land, 1992), this feedback loop is external to the animal. It results from the movements of the animal reducing the stimulus detected by the sense organs. Due to the time taken for neural conduction and processing, systems involving feedback necessarily incorporate delays. Thus negative feedback systems do not respond as fast as open loop systems. However, they do have the advantages of allowing correction of errors, counteraction of disturban~s and the following of internal commands. When such commands vary according to the time of day, they can lead to responses such as the sun compass reaction. Here, the direction of travel can be at any desired angle to the sun, and changes with time in such a way that the movements of the sun do not lead to navigation errors. This reaction is an important part of the guidance system used by foraging bees (see Rossel, 1993 and Coliett, 1993, both in this issue). As described by Land (1992), the combination of a delay, the high gain required for an adequate performance and a negative feedback loop means that these control systems tend towards instability. To avoid this, most incorporate some form of damping and some switch from smooth pursuit to saccadic tracking during fast movements. Since partial suppression of the visual input occurs during such saccades, instability is avoided by the simple expedient of making the system insensitive to the consequences of its own movements. Reafference
Reafference is the name given to the sensory input that results from an animal’s own movements.
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During the sensory guidance of many kinds of behaviour, it is put to good use. For instance, deviations from an intended flight path in locusts are detected by the compound eyes, ocelli and wind-sensitive hairs on the head. As described in Reichert’s review (Reichert, 1993) the compound eyes can detect angular deviations about all three axes, the ocelli act as horizon detectors and are thus sensitive to roll and pitch deviations, while wind-sensitive hairs, through their directional sensitivity and location on the head, can detect changes in the yaw and pitch planes. Together, these different reafferent inputs serve as the sensing mechanism of the locust’s autopilot, which enables it to fly straight. The nature of the visual flow field that results from an animal’s own movements is fully discussed by Egelhaaf and Borst (1993) and Barnes and Nalbach (1993), both in this issue. Its rotational component provides information on deviations from an intended course as just described for locusts, while its translational component gives information on ground speed and the three dimensional layout of the environment through motion parallax. Additionally, the image expansion that occurs as objects are approached can trigger landing responses (Goodman, 1960). The extent to which all this useful information is utilized is not yet clear, at least in crabs, but as Barnes and Nalbach describe, crabs do perform a simple form of flow field analysis that makes the information available. Reafferent input can also present an animal with problems. The escape responses of cockroaches depend on the detection of the wind generated by approaching predators (Camhi, 1985), but directly the cockroaches start to respond, their own forward running leads to the production of reafferent wind stimuli. Were this reafferent wind to lead to a similar turning response to that produced by the initial predator-generated wind, the results would be disastrous. The cockroach’s solution is a simple one, for the ventral giant interneurones that lead to the initial turning away from the predator are subsequently inhibited so that they do not respond to the reafferent wind, while dorsal giant interneurones, which play a role in the subsequent running away from the predator, can detect shifts in the direction of the reafferent wind and use them to maintain a straight course as described above for locust flight. From the above examples, it is clear that reafference is used to form the input to homeostatic control systems that help the animals to maintain a straight path. How then are voluntary turns produced? The answer is not known, but one attractive possibility is that the motor command to make a turn is accompanied by an efference copy signal that is used to counteract the reafferent input expected from that turn (Fig. 4). In this way, intended turns are not opposed by course maintenance control systems, without the need for these control systems to be shut down. Indeed, since they remain operative, they
w
Fig. 4. Efference copy hypothesis as applied to the fly optomotor response. According to this hypothesis, the command to make a voluntary turn (w) is accompanied by an efference copy signal whose amplitude (A.w) is designed to counterbalance precisely the reafference signal that should be produced by that turn. Since the optomotor loop is still operating, any error between intended and actual turn will be corrected. Accurate following of the command to make a voluntary turn occurs if y = w. To achieve this, it is necessary that the system for turning the fly (B2) has unity gain and that v = 0. Assuming that z = 0 (i.e., there are no disturbing influences), v will equal 0 if the gains of the systems for movement detection (B,) and for producing the efference copy signal (A) are equal (i.e., B, = A). are able to correct any deviations between the actual and intended extent of the turn (von Hoist and Mittelstaedt, 1950). Although it is clear that the fly’s optomotor system remains fully operable during voluntary turns (Mittelstaedt, 1949) there is no neurophysiological evidence in favour of such an efference copy mechanism in any arthropod sensory guidance mechanism. They do, however, occur in electric fish (Bell, 1989), and probably also in arthropod motor control systems (Barnes, 1975). Multisensory convergence
The bee dance-language controversy is one of the more hotly contested arguments in the field of sensory guidance of the last 20 years. It concerned the nature of the communication between foragers. According to von Frisch, the bees’ waggle dance contained information on both distance and direction with respect to the sun so that recruits could use a sun compass reaction to reach their goal (von Frisch, 1967, 1974; see also Rossel, 1993 and Collett, 1993, both in this issue). In contrast, Wenner and his colleagues claimed that the recruits picked up the scent of the food source from the returning foragers and used olfactory cues to search for the food source (Johnson, 1967; Wenner, 1967, 1971). It now seems certain (Gould, 1976) that, as in many other complex sensory guidance mechanisms, useful information is gathered from more than one source, in this case the oscillation of air currents produced by the dancing bee and the scent of the food source (Michelson et al., 1987). Such multisensory convergence has now been studied electrophysiologically in a number of systems, of which the control of flight orientation in insects and the control of eye movements and righting responses in Crustacea will be mentioned here.
Sensory guidance in arthropod behaviour
As is discussed in Reichert’s review (Reichert, 1993) locusts obtain information on their flight direction from their compound eyes, their ocelli and from wind-sensitive hairs on the head. Contrary to what one might suppose, the system is economical in terms of numbers of neurones, since the interneurones that signal deviations from a straight course are multimodal, carrying spatially compatible information from at least two (or more often all three) of the above sense organs. They would thus signal info~ation such as “roll to the right” or “banked turn to the left”. This does not, however, answer the question as to why information from three different sources is required. The answer is almost certainly to provide a fail-safe mechanism for the locust’s autopilot. For instance, a strong cross wind could upset the signals received from the wind-sensitive hairs, or unusual features of the terrain the input from the compound eyes. Indeed, the signal the locust appears to trust most is that from the ocelli, which act as horizon detectors, since incompatible input from the ocelh can lead to inhibition of these deviation detector neurones. Where flight is directed towards a goal, other senses are also involved. For instance, in male gypsy moths, Lymantria d&par, upwind flight towards a female is achieved by having the neurones that comprise the moth’s autopilot additionally responsive to olfactory inputs (Olberg, 1989). Windinduced transverse drift is thus reduced by the increased gain of the control system stabilizing flight in the presence of female sex pheromone. In crustaceans, compensatory eye movements can be generated by input from eyes, statocysts and leg proprioceptors (see Barnes and Nalbach, 1993 in this issue), while righting responses can be generated by both vestibular and leg proprioceptor inputs (Neil, 1985 and review in this issue). Here, the importance of utilizing inputs from more than one sense lies in increasing the frequency range over which responses occur, since the vestibular system responds best at high frequencies while the visual and leg proprioceptor systems are both active at inte~ediate and low frequencies. Matching
One of the most familiar principles of sensory processing is the matching of coding to signal (Laughlin, 1989). But this principle also extends into the study of sensory guidance, where the animal uses some form of template, which can be hard or soft wired, to aid its orientation to specific environmental stimuli. An excellent example of a hard wired template covered in this collection of reviews is the correspondence between the layout of the polarization-sensitive photoreceptors in the dorsal part of the bee’s compound eyes (the POL area) and the celestial polarization pattern (Rossel, 1993). This array of ultraviolet-sensitive receptors provides a matched filter that solves the sun compass problem by acting as a template, for when the bee has
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successfully matched the sky’s polarization pattern to its ultraviolet-sensitive receptor mosaic, it will be facing the sun, even if the sun itself is hidden from view. Although guidance mechanisms such as the sun compass reaction enable arthropods to arrive in the vicinity of their goals, precise localization requires a memory of landmarks. As described in Collett’s review (Collett, 1993), a bee behaves as if it compares its memory of a group of landmarks with its current image of them, and moves so as to reduce the mismatch between the two. Once the mismatch has been eliminated, the bee will have arrived at its destination. The nature of these memories is still a matter of conjecture. They have been modelled as a set of adjusted synaptic connections within a network of neurones that acts as a template for the location of landmarks in the vicinity of the goal (Collett, unpublished). Such memories are thus an example of a soft wired template. In the solitary wasp, Cerceris, landmark memories are formed during orientation flights which consist of a series of loops around the nest entrance (Zeil, 1989). REFERENCES
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L. J. (1960) of insects. I. The landing response the fly, Lucilia sericara and other Calliphorinae. J. exp. Biol. 37, 854878. Gould J. L. (1976) The dance-language controversy. Q. Rev. Biol. 51, 21 l-244.
Hansel1 M. H. (1985) Ethology. In Comprehensive Insect Physiology Biochemistry and Pharmacology (Edited by Kerkut G. A. and Gilbert L. I.), Vol. 9, pp. I-93. Pergamon Press, Oxford. Hassenstein B. and Reichardt W. (1956) Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des RiisselkHfers Chlorophanus. Z. Naturf. llb, 513-524. Hinde R. A. (1970) Animal Behaviour: a Synthesis of Ethology and Comparative Psychology, 2nd edition. McGraw-Hill, Kogakusha, Tokyo. Holst E. von and Mittelstaedt H. (1950) Das Reafferenzprinzip. Naturwissenschafren 37, 464476. Horridge G. A. (1992) What can engineers learn from insect vision? Phil. Trans. R. Sot. B337, 271-282. Johnson D. L. (1967) Honey bees: do they use the directional information contained in their dance manoeuver? Science N. Y. 155, 844847. Land M. F. (1992) Visual tracking and pursuit: humans and arthropods compared. J. Insect Phyiiol. (in press). Laughlin S. B. (1989) Principles of sensory coding and processing: general introduction. J. exp. Biol. 146, i-viii. Mast S. 0. (1912) Behavior of fireflies, with special reference to the problem of orientation. J. Anim. Behav. 2,256-272. Michelson A. (1987) The acoustic near field of a dancing honeybee. J. camp. Physiol. 161, 633-643. Mittelstaedt H. (1949) Telotaxis und Ontomotorik von Eristalis bei Augeninversion. Naturwissenschaften 36, 90-9 1. Mittelstaedt H. (1960) The analysis of behavior in terms of control systems. In Trans. 5th Conference on Group Processes, 1958. Josiah Macy, Jr. Foundation, New York. Mittelstaedt H. (1961) Die Regelungstheorie als methodisches Werkzeug der Verhaltensanalyse. Naturwissenschaften 48, 246254.
Mittelstaedt H. (1962) Control systems of orientation in insects. A. Rev. Em. 7, 177-198. Mittelstaedt H. (1964) Basic control patterns of orientational homeostasis. Symp. Sot. exp. Biol. 18, 365-386. Miiller A. (1925) uber Lichtreaktionen von Landasseln. Z. vergl. Physiol. 3,
I 13-144.
Neil M. (1985) Multisensory in the crustacean equilibrium system. In Feedback and Motor Control in Invertebrates and Vertebrates (Edited by Barnes W. J. P. and Gladden M. H.), pp. 277-298. Croom Helm, London. Neil D. M. (1993) Sensory guidance of equilibrium reactions in crustacean posture and locomotion. Camp. Biochem. Physiol. 104, 633-646. Olberg R. M. (1989) Pheromone-modulated visual responses of descending interneurones in the gypsy moth. In Neural Mechanisms of Behavior (Edited by Erber J., Menzel R., PIRiger H.-J. and Todt D.), pp. 255-256. Georg Thieme Verlag, Stuttgart. Reichert H. (1993) Sensory inputs and flight orientation in locusts.
Comp. Biochem. Physiol. 104, 647-657.
Rossel S. (1993) Navigation by bees using polarised light. Camp. Biochem. Physiol. 104, 695-708.
Rowe11 C. H. F., Reichert H. and Bacon J. P. (1985) How locusts fly straight. In Feedback and Motor Conrrol in Invertebrates and Vertebrates (Edited by Barnes W. J. P. and Gladden M. H.), pp. 337-354. Croom Helm, London. Sandeman D. C. (1967) Excitation and inhibition of the reflex eye withdrawal of the crab Carcinus. J. exp. Biol. 46, 475485.
Sargent T. D. (1969) Behavioural adaptations of cryptic moths. III. Resting attitudes of two bark-like species, Melanolophia canadaria and Carocala uhronia. Anim. Behav. 17, 670672.
Stewart W. W. (1981) Lucifer dyes-highly fluorescent dyes for biological tracing. Nature, Lond. 292, 17-21. Szebenyi A. L. (1969) Cleaning behaviour in Drosophila melanogasrer. Anim. Behav. 17, 641651.
Wenner A. M. (1967) Honey bees: do they use the distance information contained in their dance manoeuver? Science N. Y. 155, 847-849. Wenner A. M. (1971) The Bee Language Controversy. Educational Programs Improvement Corp., Boulder, CO. Wigglesworth V. B. (1941) The sensory physiology of the human louse Pediculus humanus corporis de Beer (Anoplura). Parasitology 33, 67-109. Zeil J. (1989) The role of behaviour in depth information processing: orientation flights and landmark orientation in solitary wasps. In Neural Mechanisms of Behaviour (Edited by Erber J., Menzel R., PtXiger H.-J. and Todt D.), pp. 236-237. Georg Thieme Verlag, Stuttgart.
1993
MINI
0300-9629/93 $6.00 + 0.00 Q 1993 Pergamon Press Ltd
REVIEW
SENSORY GUIDANCE IN ARTHROPOD BEHAVIOUR: COMMON PRINCIPLES AND EXPERIMENTAL APPROACHES W. J. P. BARNES Department of Zoology, University of Glasgow,
Glasgow
G12 8QQ,
U.K.
(Received 2 September 1992; accepted 26 October 1992) Abstract-l. Ex~rimental approaches to the study of sensory guidance m~hanisms in arthropods are reviewed. The classical techniques of ethology and neurophysiology combine with controi systems analysis and computer modelling to cast new light on the ways in which these animals orientate, steer, navigate, learn routes and find a mate. 2. Common principles of sensory guidance include negative feedback, reafference, multisensory convergence and matching. Occurring in functionally diverse systems, they relate to the accuracy and efficiency of sensory guidance, and reflect the fact that natural selection acts to maximise the return from any investment.
INTRODUCIION
Sensory guidance, the way in which animals find their way about the world, is a fascinating area of research. To the zoologist, the intricate physiological and behavioural adaptations that animals have evolved to recognise where they are, find a mate, or simply get from A to B provide much to marvel at. No less interested in this area are neuroetholo~sts trying to understand how behaviour is controlled by the nervous system. When the behaviour in question is directed towards a goal, and involves well-defined sensory cues, the task of gaining some physiological understanding of it is that much easier. Finally, although most research in this area is basic as opposed to applied, it is already clear that this field is relevant to robotics. For instance, an understanding of visual sensory guidance mechanisms in arthropods is likely to be crucial for the design of new hardware for devices that move in cluttered worlds to help them avoid obstacles and reach their goals (Horridge, 1992). Indeed, one such robot has already been constructed by Franceschini et al. (1992) on the principles of insect vision, which avoids objects by visually evaluating its own motion relative to that of the environment. The study of behaviour defines &he sensory guidance mechanisms that animals use. Indeed, the success of the majority of the studies reported here depends upon behavioural work that has specified the task that the animal accomplishes. In some cases, the behavioural investigation leads directly to models of how the behaviour is carried out; in others, it forms the basis for neurophysioiogical studies. In
such neurophysiological studies, visual orientation in flies being a good example (Egelhaaf et al., 1988), a knowledge of the relationship between stimulus and response allows one to specify the computations that are required before the task can be carried out. Indeed, in this example, behavioural experiments led to a precisely formulated model for movement detection (Hassenstein and Reichardt, 1956; Borst and Egelhaaf, 1989). This model was then used to formulate hypotheses for neural function that permitted the design of experiments that could specify the functions of neurones and pathways. In such a manner, a formal model can develop into a model based on neurophysiological data. Sensory guidance should not, however, be viewed purely in terms of sense organ function. ultimately, sensory systems must progress to motor systems. Viewed as sensory-motor networks, sensory guidance mechanisms may provide clues to the operational principles that govern the integration of sensory and motor pathways. At first sight, the task may appear difficult. How, for instance, are the neural messages that signal deviations from course used by a flying locust to produce correcting manoeuvres? But the solution often turns out to be remarkably simple. The locust gates the deviation signals at wing beat frequency so that they only reach the motor neurones during the appropriate phase of the wing beat cycle for the flight correction to be carried out (Rowe11 et al., 1985). As in many other sensory guidance systems, a short cut has evolved that provides an elegantly simple solution. As well as providing an overview of the reviews that follow, this paper reviews the history of the study 625
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of sensory guidance mechanisms in animals and makes a case for their being common principles governing sensory guidance in functionally diverse systems. Many of these principles can be related to the accuracy and efficiency of these guidance systems, and reflects the fact that natural selection acts to maximize the return from any investment.
HISTORICAL
APPROACHES TO THE SENSORY GUIDANCE
STUDY
OF
Classification of orienting movements Some activities of animals are performed without orientation to the environment. At the reflex level, retraction of a crab’s eye into its socket, once elicited by the appropriate stimulation, has no special spatial ~lationship to objects in the environment (Sandernan, 1967). Similarly with some examples of more complex behaviour. For instance, grooming behaviour in Drosophila (or for that matter a number of other insects), once triggered by some external or more often internal stimulus, proceeds in a more or less stereotyped manner without reference to the environment (Szebenyi, 1969). For the most part, however, animals regulate their activities in a spatial relationship with the environment. Locomotion is guided towards goals; escape responses directed away from predators; courtship aimed at a mate; prey-catching movements directed towards prey. Such orientation responses frequently exploit the predictable nature of environmental stimuli. Olfactory cues are carried downstream or downwind by water or wind; the horizon is horizonArWlclsl Bark
tal; gravity acts downwards. It has become customary to separate orientation responses into two broad categories: (1) primary orientation, the assumption of the basic position of the body in space; and (2) secondary orientation, orientation or movement in space with a particular relationship to environmental stimuli. As an example of primary orientation, let us consider the stimuli which two species of moth (~elano~op~~a canaduria and Catocafa ultron~u) utilize to align prominent markings on their wings with vertical fissures on the bark of trees. In these experiments, carried out by Sargent (1969), the moths were allowed to settle on artificial bark, aligned either vertically or horizontally (Fig. I). The experiment was then repeated but with tactile cues no longer available, the artificial bark being covered by a sheet of clear plastic. The results show that Mehnolophia orients using tactile cues provided by the fissures themselves and thus fails to show a preferred orientation when no tactile cues are available, while Catocala simply responds to gravity and always rests head down. The study of secondary orientation has been much influenced by the work of Fraenkel and Gunn, whose monograph “The Orientation of Animals” was first published in 1940. In Fraenkel and Gunn’s analysis, orientation responses are classified according to the m~hanism involved. The basic distinction in this scheme is between kineses and taxes. In the former, animals respond to differences in environmental stimulation with differential rates of turning or speeds of movement. As a result, they decrease the time they AItitlcisl Bark Covered by Trsnspsrent
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Fig. 1. Experimental analysis of stimuli used by the moths ~e~aff~~o~~jucunu&ric and Curoculu ultrotriu to align prominent markings on their wings with vertical fissures on the bark of trees. In the first experiment (left), the moths were allowed to settle on artificial bark (strips of thick tape). aligned either vertically or horizontally. The numbers represent the numbers of moths aligning their wings either parallel with or at right angles to ridges on the bark as indicated on the diagrams. In the second experiment (right), which was otherwise identical to the first, a piece of transparent perspex was placed over the strips of tape before the moths were released. After Sargent (1969).
Sensory guidance in arthropod behaviour
spend in unfavourable habitats and increase the time spent in favourable habitats compared to randomly moving individuals, but achieve this without directional movement. By such mechanisms as these, woodlice (Porce[lio scaber) tend to aggregate in moist places, and the human body louse in smelly, warm ones (Wigglesworth, 1941). In contrast, a taxis is defined as an orientation response in which the animal moves at a particular orientation to the stimulus-at a particular angle to the sun, towards a source of sound etc. More detailed levels of classification depend on the nature of the stimulus to which the animal is responding4.g. geotaxis (gravity) or phototaxis (light)--or on the way in which the sensory information is obtained. In a klinotuxis, the direction of movement is determined by successive comparisons of the stimulation impinging on its receptors as they are turned from side to side, while in a tropotaxis (Fig. 2A) the sensory inputs received by left and right sense organs are balanced simultaneously. A telotaxis, on the other hand, does not depend upon simple balance; if there are two sources of stimulation, the animal orients to one or the other. Figure 2B shows this for hermit crabs orienting to one or other of two lights. Orientation need not be directly towards or away from the stimulus. In a menotaxis or light compass response, the orientation is at a constant angle to the stimulus direction, while in a mnemotaxis it involves a memory of local landmarks (cf. Collett, 1993 in this issue). This system of labelling has, over the years, provided good shorthand descriptions for different orientation behaviours, and brought about a degree of order to the huge diversity of different responses. However, except at its most basic level, it has probably outlived its usefulness. Why is this so? In part, it is because this system of classification does not guarantee that responses bearing the same label share the same physiological mechanism. Assignment of a particular label to an orientation response depends on an assessment of the role of individual receptor organs, not on an analysis of all that happens between stimulus and response. Fraenkel and Gunn’s classification is thus useful insofar as it refers to
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different types of spatial manoeuvre, but can be dangerous if taken to imply types of physiological mechanism (Hinde, 1970). Secondly, the different categories have been largely analysed in laboratory studies in simplified situations. As will become clear in the following reviews, studies carried out in the field or in more complex laboratory situations show Fraenkel and Gunn’s categories to be of limited use. The responses tend to be complex, involving a number of senses, and different types of orientation occur together or in close succession. Thus they do not fall conveniently into any of Fraenkel and Gunn’s categories. Indeed, it is probably fair to say that, in the same way that reflexes form components of many mechanisms of motor control, so Fraenkel and Gunn’s classification at best describes the building blocks from which whole sensory guidance mechanisms are constructed. Analysis of orientation in terms of control systems For a more detailed analysis of orientation mechanisms, simple labels become inadequate, and the results can only be expressed in terms of the actual relationships between stimulus and response. This is the field of the control systems engineer. Indeed, the application of control theory to this field of biology, pioneered by Mittelstaedt in the early 1960s (Mittelstaedt, 1960, 1961, 1962, 1964), has made a major contribution to our understanding of many orientation behaviours. The control theory or cybernetic approach is an example of a “black box” approach, viewing the system as a whole and describing it mathematically from its input/output characteristics; i.e. we try to find a set of equations or a model to fit the relation by which the behavioural output is governed by the stimulus over a range of stimulus variables such as intensity, frequency, spatial pattern and so on. Applying these methods to orientation behaviour, one can distinguish a sensory system or systems that receive information from the outside world, a motor system for changing course or orientation, and mechanisms for relating the two. What Mittelstaedt (1964) was able to show was that these different
B L
L2
Fig. 2. A: tropotaxis tracks of photopositive woodlice Armadi//idum orienting with respect to two lights of equal intensity. After Miiller (1925). 9: telotaxis tracks of hermit crabs orienting in an equivalent experimental situation. After Fraenkel and Gunn (1940).
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systems could be linked together in either of two fundamentally different ways. If the movement produced by the effecters does not affect the stimulus received by the animal, the system is said to be open loop. For instance, male fireihes orient to flashes of light produced by females. Since the males orient correctly even though they do not start to turn until after the female’s flash is over (Mast, 1912), the output (the change in the orientation) cannot affect the input (the angle between the flash and the body axis). This system, called a uniiaterai mesh, is illustrated in Fig. 3A. Another good example of an open loop system is provided by the strike of the praying mantis, analysed by Mittelstaedt (1962). Information about the direction of prey is perceived by the compound eyes. The output of the system is the deviation of the strike from the body axis. In theory, information regarding the direction of the strike could be fed back into the system by the eyes while the strike is in progress, but in practice the transmission time for such a correction is longer than the time taken to extend the forelegs. The system is thus akin to firing a gun; you cannot change the direction of the bullet once it has left the barrel! In contrast to the above, systems in which the output influences the input (and which thus involve feedback) are said to be ciosed loop. Visual tracking responses (see Land, 1992) and optomotor responses are good examples of closed loop control systems. As illustrated in Fig. 3B, which represents the optomotor
A. Unilateralmesh -
reaction of the fly, the system output (the rotation of the fly) is fed back and subtracted from the input (the rotation of the striped pattern) because the eyes move with the body. The velocity actually seen by the fly is thus the input minus the output, and the system can be said to incorporate a negative feedback loop (Mittelstaedt, 1964). From these descriptions, it will be apparent that the correct functioning of open loop systems depends upon the precision of their calibrations, while closed loop systems allow continuous correction of errors. Additionally, closed loop systems are able to correct for disturbances (e.g. the effect of wind on a flying insect), a property not shared by open loop systems. The control theory approach is now an established feature of the orientation literature. In this collection of reviews, it is utilized in the study of the eye movements of crabs (Barnes and Nalbach, 1993). It does not offer a complete solution, but it does give one an understanding of the system as a whole. Thus it remains an important step in the analysis of many sensory guidance mechanisms. It has been argued that such non-physiological models are a poor substitute for physiological ones, in that they fail to provide any understanding at the neuronal level (Hansel], 1985). This is not altogether fair. They are useful, even if they do not provide a complete story. Some behaviours such as flight steering in locusts (see Reichert, 1993 in this issue) do lend themselves to the neurophysiological approach; others such as landmark orientation in bees (see Collett, 1993 in this issue) do not (at least yet!). The same argument can be used in the study of memory. The cellular and molecular approaches can hope to elucidate what happens at particular synapses, but they are ill equipped to understand how memories are organized in the brain. Recent approaches to the stuu(v of sensory guidance
Et. Negative feedback loop
Fig. 3. Control systems for orientational homeostasis. A. open loop system (unilateral mesh) for orientation of male fireflies to flash of female. zdeviation of flash of female firefly from body axis of male. y-change in orientation of male firefly. Error (x) is zero if the product of B, and Bt (the systems for detecting the deviation of the flash and for turning the body, respectively) is equal to I, for then y will equal z. B. Closed loop system involving negative feedback for fly optomotor response. z-rotational velocity of striped pattern rotated around the fly. y-rotational velocity of fly. Error (x) is low if the product of B, and B, (the systems for detecting movement and for turning the fly, respectively) is high. Modified from Mittelstaedt (1964).
And so I bring this brief historical survey up to the present day. We are no longer satisfied with a mere classification of orientation or navigation mechanisms; nor are most of us completely content with the models of the control systems engineer, useful though they are. Instead, we are using a variety of approaches, anatomical, physiological, biomechanical and behavioural, to try to understand precisely how sensory guidance mechanisms work. The neurophysiological approach to sensory guidance has been made possible by a number of important technical advances. These include advances in microelectrode recording techniques, which enable one to record intracellularly from single neurones in the central nervous system, and the development of dyes such as Lucifer Yellow (Stewart, 1981) which, when injected into the cell through the microelectrode, allow the neurone’s anatomy to be fully visualized. Arthropods have proved particularly advantageous for such studies, both because large numbers of neurones can be
individually
recognized and because they are very
Sensory guidance in arthropod behaviour tolerant of dissection. This means that many components of orientation behaviours can be studied in preparations sufficiently dissected to permit microelectrode recording. Advances in the availability, user-friendliness and sophistication of computers has also played an important part in these studies. They have allowed more complicated forms of data analysis, and led to an increase in the use of computer simulation as a way of testing models of sensory guidance mechanisms. But most of the studies that are reviewed here are at least partly behavioural, a field in which the development of ideas as much as of techniques has led to the rapid advances that have occurred. Thus it is appropriate to emphasise the ingenuity of the scientists themselves. For this is not a field where scientists are mere technicians gathering routine data, but one where inventiveness and lateral thinking are essential requirements for success. The reviews that follow illustrate the variety of sensory guidance mechanisms used by arthropods. The behavioural approach is exemplified by the study of navigation by bees using polarized light (Rossei, 1993), landmark guidance in insects (Collett, 1993) and courtship behaviour in spiders (Barth, 1993). In different ways all are remarkable behaviours. The bees use of polarized light employs a sense that we humans lack; their use of landmarks requires learning and memory of the relative positions of features of their environment, which is no mean feat for an animal with such a simple nervous system; while courtship in different members of the spider genus, Cupiennius, involves communication by way of vibration signals transmitted through the leaves of the plants in which they live. The study of the eye movements of freely moving crabs (Barnes and Nalbach, 1993), where it appears that the crabs are performing a simple form of flow field analysis, lends itself to the control systems approach, since inputs and outputs can be precisely measured. Indeed, in flies (Egelhaaf and Borst, 1993) the study of visual orientation has been taken a stage further, to the analysis of the neurophysioiogicai mechanisms used to generate optomotor and tracking responses. Such neurophysiological approaches are appropriate wherever components of sensory guidance can be obtained in partly dissected preparations. The equilibrium responses of lobsters (Neil, 1993) have been successfuliy studied in this manner, as has the control of flight orientation in locusts (Reichert, 1993). Indeed, the latter study probably provides the most detailed understanding at the neural level that we have of any sensory guidance mechanism. Amongst several further examples, computer simulations have played an important role in the study of the mechanisms of motion detection in flies (Egeihaaf and Borst, 1993), while biomechanical studies have played a role in the study of spider pre-copulatory behaviour (Barth, 1993) and crustacean equilibrium responses (Neil, 1993). As well as illustrating these different
629
experimental approaches to sensory guidance, the studies that comprise this issue of Comparative Biochemistry and Physiology have been chosen to illustrate common features that are shared by many such behaviours. These are briefly discussed below. COMMON
FEATURES OF SENSORY GUIDANCE MECHANISMS
Negative feedback
The relevance of control systems analysis to the study of sensory guidance is no accident. Sensory guidance mechanisms are control systems and, moreover, control systems in which the critical variables can be measured and manipulated (Mittelstaedt, 1964). A few of these systems invoive open loop control. The strike of the praying mantis and the mechanism by which fireflies find a mate have already been mentioned. A further example is provided by the prey capture behaviour of the semi-aquatic spider, Dolomedes, which obtains information on the direction and distance of its prey from the ripples they generate on the water surface (Bl~kmann, 1988). The vast majority, however, are closed loop systems incorporating negative feedback. In many cases (e.g. optomotor reactions and visual tracking-see Barnes and Nalbach, 1993 in this issue and Land, 1992), this feedback loop is external to the animal. It results from the movements of the animal reducing the stimulus detected by the sense organs. Due to the time taken for neural conduction and processing, systems involving feedback necessarily incorporate delays. Thus negative feedback systems do not respond as fast as open loop systems. However, they do have the advantages of allowing correction of errors, counteraction of disturban~s and the following of internal commands. When such commands vary according to the time of day, they can lead to responses such as the sun compass reaction. Here, the direction of travel can be at any desired angle to the sun, and changes with time in such a way that the movements of the sun do not lead to navigation errors. This reaction is an important part of the guidance system used by foraging bees (see Rossel, 1993 and Coliett, 1993, both in this issue). As described by Land (1992), the combination of a delay, the high gain required for an adequate performance and a negative feedback loop means that these control systems tend towards instability. To avoid this, most incorporate some form of damping and some switch from smooth pursuit to saccadic tracking during fast movements. Since partial suppression of the visual input occurs during such saccades, instability is avoided by the simple expedient of making the system insensitive to the consequences of its own movements. Reafference
Reafference is the name given to the sensory input that results from an animal’s own movements.
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During the sensory guidance of many kinds of behaviour, it is put to good use. For instance, deviations from an intended flight path in locusts are detected by the compound eyes, ocelli and wind-sensitive hairs on the head. As described in Reichert’s review (Reichert, 1993) the compound eyes can detect angular deviations about all three axes, the ocelli act as horizon detectors and are thus sensitive to roll and pitch deviations, while wind-sensitive hairs, through their directional sensitivity and location on the head, can detect changes in the yaw and pitch planes. Together, these different reafferent inputs serve as the sensing mechanism of the locust’s autopilot, which enables it to fly straight. The nature of the visual flow field that results from an animal’s own movements is fully discussed by Egelhaaf and Borst (1993) and Barnes and Nalbach (1993), both in this issue. Its rotational component provides information on deviations from an intended course as just described for locusts, while its translational component gives information on ground speed and the three dimensional layout of the environment through motion parallax. Additionally, the image expansion that occurs as objects are approached can trigger landing responses (Goodman, 1960). The extent to which all this useful information is utilized is not yet clear, at least in crabs, but as Barnes and Nalbach describe, crabs do perform a simple form of flow field analysis that makes the information available. Reafferent input can also present an animal with problems. The escape responses of cockroaches depend on the detection of the wind generated by approaching predators (Camhi, 1985), but directly the cockroaches start to respond, their own forward running leads to the production of reafferent wind stimuli. Were this reafferent wind to lead to a similar turning response to that produced by the initial predator-generated wind, the results would be disastrous. The cockroach’s solution is a simple one, for the ventral giant interneurones that lead to the initial turning away from the predator are subsequently inhibited so that they do not respond to the reafferent wind, while dorsal giant interneurones, which play a role in the subsequent running away from the predator, can detect shifts in the direction of the reafferent wind and use them to maintain a straight course as described above for locust flight. From the above examples, it is clear that reafference is used to form the input to homeostatic control systems that help the animals to maintain a straight path. How then are voluntary turns produced? The answer is not known, but one attractive possibility is that the motor command to make a turn is accompanied by an efference copy signal that is used to counteract the reafferent input expected from that turn (Fig. 4). In this way, intended turns are not opposed by course maintenance control systems, without the need for these control systems to be shut down. Indeed, since they remain operative, they
w
Fig. 4. Efference copy hypothesis as applied to the fly optomotor response. According to this hypothesis, the command to make a voluntary turn (w) is accompanied by an efference copy signal whose amplitude (A.w) is designed to counterbalance precisely the reafference signal that should be produced by that turn. Since the optomotor loop is still operating, any error between intended and actual turn will be corrected. Accurate following of the command to make a voluntary turn occurs if y = w. To achieve this, it is necessary that the system for turning the fly (B2) has unity gain and that v = 0. Assuming that z = 0 (i.e., there are no disturbing influences), v will equal 0 if the gains of the systems for movement detection (B,) and for producing the efference copy signal (A) are equal (i.e., B, = A). are able to correct any deviations between the actual and intended extent of the turn (von Hoist and Mittelstaedt, 1950). Although it is clear that the fly’s optomotor system remains fully operable during voluntary turns (Mittelstaedt, 1949) there is no neurophysiological evidence in favour of such an efference copy mechanism in any arthropod sensory guidance mechanism. They do, however, occur in electric fish (Bell, 1989), and probably also in arthropod motor control systems (Barnes, 1975). Multisensory convergence
The bee dance-language controversy is one of the more hotly contested arguments in the field of sensory guidance of the last 20 years. It concerned the nature of the communication between foragers. According to von Frisch, the bees’ waggle dance contained information on both distance and direction with respect to the sun so that recruits could use a sun compass reaction to reach their goal (von Frisch, 1967, 1974; see also Rossel, 1993 and Collett, 1993, both in this issue). In contrast, Wenner and his colleagues claimed that the recruits picked up the scent of the food source from the returning foragers and used olfactory cues to search for the food source (Johnson, 1967; Wenner, 1967, 1971). It now seems certain (Gould, 1976) that, as in many other complex sensory guidance mechanisms, useful information is gathered from more than one source, in this case the oscillation of air currents produced by the dancing bee and the scent of the food source (Michelson et al., 1987). Such multisensory convergence has now been studied electrophysiologically in a number of systems, of which the control of flight orientation in insects and the control of eye movements and righting responses in Crustacea will be mentioned here.
Sensory guidance in arthropod behaviour
As is discussed in Reichert’s review (Reichert, 1993) locusts obtain information on their flight direction from their compound eyes, their ocelli and from wind-sensitive hairs on the head. Contrary to what one might suppose, the system is economical in terms of numbers of neurones, since the interneurones that signal deviations from a straight course are multimodal, carrying spatially compatible information from at least two (or more often all three) of the above sense organs. They would thus signal info~ation such as “roll to the right” or “banked turn to the left”. This does not, however, answer the question as to why information from three different sources is required. The answer is almost certainly to provide a fail-safe mechanism for the locust’s autopilot. For instance, a strong cross wind could upset the signals received from the wind-sensitive hairs, or unusual features of the terrain the input from the compound eyes. Indeed, the signal the locust appears to trust most is that from the ocelli, which act as horizon detectors, since incompatible input from the ocelh can lead to inhibition of these deviation detector neurones. Where flight is directed towards a goal, other senses are also involved. For instance, in male gypsy moths, Lymantria d&par, upwind flight towards a female is achieved by having the neurones that comprise the moth’s autopilot additionally responsive to olfactory inputs (Olberg, 1989). Windinduced transverse drift is thus reduced by the increased gain of the control system stabilizing flight in the presence of female sex pheromone. In crustaceans, compensatory eye movements can be generated by input from eyes, statocysts and leg proprioceptors (see Barnes and Nalbach, 1993 in this issue), while righting responses can be generated by both vestibular and leg proprioceptor inputs (Neil, 1985 and review in this issue). Here, the importance of utilizing inputs from more than one sense lies in increasing the frequency range over which responses occur, since the vestibular system responds best at high frequencies while the visual and leg proprioceptor systems are both active at inte~ediate and low frequencies. Matching
One of the most familiar principles of sensory processing is the matching of coding to signal (Laughlin, 1989). But this principle also extends into the study of sensory guidance, where the animal uses some form of template, which can be hard or soft wired, to aid its orientation to specific environmental stimuli. An excellent example of a hard wired template covered in this collection of reviews is the correspondence between the layout of the polarization-sensitive photoreceptors in the dorsal part of the bee’s compound eyes (the POL area) and the celestial polarization pattern (Rossel, 1993). This array of ultraviolet-sensitive receptors provides a matched filter that solves the sun compass problem by acting as a template, for when the bee has
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successfully matched the sky’s polarization pattern to its ultraviolet-sensitive receptor mosaic, it will be facing the sun, even if the sun itself is hidden from view. Although guidance mechanisms such as the sun compass reaction enable arthropods to arrive in the vicinity of their goals, precise localization requires a memory of landmarks. As described in Collett’s review (Collett, 1993), a bee behaves as if it compares its memory of a group of landmarks with its current image of them, and moves so as to reduce the mismatch between the two. Once the mismatch has been eliminated, the bee will have arrived at its destination. The nature of these memories is still a matter of conjecture. They have been modelled as a set of adjusted synaptic connections within a network of neurones that acts as a template for the location of landmarks in the vicinity of the goal (Collett, unpublished). Such memories are thus an example of a soft wired template. In the solitary wasp, Cerceris, landmark memories are formed during orientation flights which consist of a series of loops around the nest entrance (Zeil, 1989). REFERENCES
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