Karl Kral

Motion detection in insect orientation and navigation

The visual systems of insects are exquisitely sensitive to motion. Over the past 40 years or so, motion processing in insects has been studied and characterised primarily through the optomotor response. This response, which is a turning response evoked by the apparent movement of the visual environment, serves to stabilise the insects orientation with respect to the environment. Research over the past decade, however, is beginning to reveal the existence of a variety of other behavioural responses in insects, that use motion information in different ways. Here we review some of the recently characterised behaviours, describe the inferred properties of the underlying movement-detecting processes, and propose modified or new models to account for them.

Behavioural–analytical studies of the role of head movements in depth perception in insects, birds and mammals

In this review, studies of the role of head movements in generating motion parallax which is used in depth perception are examined. The methods used and definitiveness of the results vary with the animal groups studied. In the case of insects, studies which quantify motor outputs have provided clear evidence that motion parallax evoked by head movements is used for distance estimation and depth perception. In the case of birds and rodents, training studies and analyses of the head movements themselves have provided similar indications. In the case of larger mammals, due to a lack of systematic experiments, the evidence is less conclusive.

Motion parallax as a source of distance information in locusts and mantids

This review article is devoted to results on distance measurement in locusts (e.g., Wallace, 1959; Collett, 1978; Sobel, 1990) and mantids. Before locusts or mantids jump toward a stationary object, they perform characteristic pendulum movements with the head or body, called peering movements, in the direction of the object. The fact that the animals over- or underestimate the distance to the object when the object is moved with or against the peering movement, and so perform jumps that are too long or short, would seem to indicate that motion parallax is used in this distance measurement. The behavior of the peering parameters with different object distances also indicates that not only retinal image motion but also the animal’s own movement is used in calculating the distance.

Side-to-side head movements to obtain motion depth cues: A short review of research on the praying mantis.

In the case of a visual field comprised of stationary objects, retinal image motion and motion parallax initiated by the observer can be used to determine the absolute and relative distance of objects. The principle is simple: when the observer moves, the retinal images of objects close to the eye are displaced more quickly-and through a larger angle-than are the retinal images of more distant objects. It is remarkable that not only in humans, but throughout the animal kingdom, from primates down to insects, retinal image motion and motion parallax generated with the aid of head movements is used as a means of distance estimation. In the case of praying mantids, translatory side-to-side movements of the head in a horizontal plane are performed to determine the jump distance to stationary objects. The relevant parameter for determining the distance to the object is the speed of retinal image motion. The motion of the head must, however, also be monitored. This requires a multisensory regulatory circuit. Motion parallax information seems to be mediated by a movement-detecting neuronal mechanism which is sensitive to the speed of horizontal image motion, irrespective of its spatial structure or direction.

Visual deprivation and distance estimation in the praying mantis larva

Abstract. Young larvae of the praying mantis, Tenodera sinensis Saussure, were placed on an off‐centre island surrounded by a round arena with six black bars painted on a white inner wall. In this situation, it was shown that the horizontal peering movements of the head often seen in mantids are in fact used to measure distances; motion parallax may be involved in this process. Aimed jumps that followed peering were taken to be the distinct result of an absolute distance measurement. Specific visual deprivation such as painting over of certain parts of the eye with opaque black varnish or degeneration of the fovea with sulforhodamine showed that: absolute evaluation of distance is only possible with two fully intact eyes; the peering mechanism is under visual control; and visual experience has a long‐term effect on distance measurement involving peering movements.

Fine structural localisation of acetylcholinesterase activity in the compound eye of the honeybee (Apis mellifica L.)

SummaryAcetylcholinesterase (AChE) activity was demonstrated histochemically at the electron microscopic level in the compound eye of the worker bee (Apis mellifica L.) by use of the method of Lewis and Shute (1969).All photoreceptor axons (short and long visual fibres) display AChE activity. The reaction product is located in the axoplasm and at the plasma membrane. Substantial amounts of the reaction product can be detected in the intercellular spaces between the visual fibres. Along the visual fibres, the enzyme activity is unevenly distributed. High AChE activity is present in the distal parts of the axons, in contrast to lower enzyme levels in the lamina. However, AChE is also present in the proximal terminals of the visual fibres as well as in the intercellular spaces between visual fibre terminals and the postsynaptic neurones (monopolar cells). Intracellular enzyme activity is almost absent in the monopolars.The authors assume the high AChE activity in the visual fibres to be indicative of acetylcholine as the transmitter at the first synapse of the compound eye. This hypothesis is discussed in view of the results of autoradiographic, electrophysiological and pharmacological investigations of the compound eye and of the ocellus. Our data are at variance with results of studies on the eyes of Diptera.

Serotonin-immunoreactive neurones in the visual system of the praying mantis: An immunohistochemical, confocal laser scanning and electron microscopic study

The distribution, number, and morphology of serotonin-immunoreactive (5-HTi) neurones in the optic lobe of the praying mantis Tenodera sinensis were studied using conventional microscopy and confocal laser scanning microscopy. Five or six 5-HTi neurones connect the lobula complex with the medulla, and at least 50 5-HTi neurones appear to be confined to the medulla. In addition, a few large 5-HTi processes from the protocerebrum supply the lobula complex, and two large 5-HTi processes from the protocerebrum ramify in the medulla and lamina, where they show wide field arborisations. In order to provide a basis for understanding the action of serotonin in the lamina, the ultrastructure of its 5-HTi terminals was examined by conventional and immunohistochemical electron microscopy. The 5-HTi profiles were filled with dense core vesicles and made synapses. Output synapses from 5-HTi profiles outnumbered inputs by about 3 to 1. The terminals of the 5-HTi neurones were in close contact with cells of various types, including large monopolar cells, but close apposition to photoreceptor terminals was rare, and no synapses were found between 5-HTi terminals and photoreceptor terminals.

The visual orientation strategies of Mantis religiosa and Empusa fasciata reflect differences in the structure of their visual surroundings

In the present study, peering behaviour, which is used to measure distance by the image motion caused by head movement, is examined in two types of mantid. Mantis religiosa inhabits a region of dense grass consisting of uniform, generally uniformly aligned, and closely spaced elements and executes slow, simple peering movements. In contrast, Empusa fasciata climbs about in open regions of shrubs and bushes which consist of irregular, variably aligned and variably spaced elements and it executes comparatively quick, complex peering movements. Hence, it seems that in these two species of mantid, the same orientation mechanism has been adapted to the unique structures of their visual surroundings. Apparently M. religiosa uses motion parallax and E. fasciata uses a combination of motion parallax and forward and backward movements (image expansion/contraction over time) to detect object distances.

Spatial Vision in the Course of an Insect’s Life

Praying mantises are considered to be phylogenetically ancient insects with their roots in the palaeozoic Protoblattoidea. They have evolved two mechanisms for spatial vision: (a) estimating the distance to moving prey objects with the use of binocular disparity [Rossel, 1983] and (b) estimating the distance to stationary target objects with motion parallax produced by head movements [Poteser and Kral, 1995]. There is no doubt that the ability to use both visual cues is congenital, but the degree to which either mechanism is developed and its significance to the individual depends to some extent upon the animal’s age and exposure to prey species and environmental cues. Experience and learning play an important role. It appears that young mantises can perform both binocular and monocular calculations of distance but they grow to depend more on the binocular mechanism. Motion parallax plays an important role in movement strategy throughout the course of a mantis’s life, but this mechanism appears to be particularly in early life.

Influence of Visual Deprivation on Levels of Dopamine and Serotonin in the Visual System of House Crickets, Acheta domesticus

Abstract High-performance liquid chromatography (HPLC) with electrochemical detection was used to determine some biogenic amines in the compound eyes and optic lobes of crickets (Acheta domesticus) qualitatively or, in the case of dopamine and 5-hydroxytryptamine (5-HT), quantitatively. When animals with one completely occluded eye were kept under a normal day-night cycle (12 h light: 12 h dark) there was a distinct increase in the concentration of dopamine after 4 days and of 5-HT after 7 days on the ipsilateral side as compared to controls. In the intact contralateral eye, the levels of both dopamine and 5-HT rose after 4 days; dopamine increases somewhat more, and 5-HT much more than on the occluded side. Animals kept in total darkness showed the same increase in dopamine concentration (× 1.3) and 5-HT (× 1.6) after just 3 days as animals with one occluded eye showed on the ipsilateral side after 8 days. The findings indicate that (i) the dopamine and 5-HT levels can depend not only on circadian but also on external daily modulation; and (ii) there is a reciprocal binocular relationship. With constant illumination, after 3 days the dopamine values were 1.9 times and the 5-HT values 3 times greater than control values; this would seem to be due to stress.