Optomotor Behavior Research Articles

Hiding responses of locusts to approaching objects

Locusts, Locusta migratoria, sitting on a plant stem hide from dark moving or expanding shapes in their environment. The fore- and middle legs perform this avoidance response by making lateral tilting movements, while the hindlegs slide laterally and guide rotation of the posterior body over the stem. During larger turns, the legs take lateral steps when lateral tilting is limited by the joints. Slow hiding movements of less than 300 degrees s-1 of angular velocity are induced by slowly changing (looming) shapes, and interposed stops or slowing of the movement can delay the progress of this hiding manoeuvre. Fast hiding movements with angular velocities between 120 degrees s-1 and 860 degrees s-1 proceed continuously and rapidly in response to rapidly expanding stimuli. Hiding responses to expanding shapes occur only after the expanding image has exceeded a threshold visual angle of 8-9.5 degrees. Hiding response latencies range between 220 ms and 1.2 s for fast hiding and are approximately 1.2 s for most slow hiding responses. Predator-avoidance responses such as freezing, jerking, crouching, walking backwards, dropping or jumping can be used instead of or in conjunction with hiding behaviour. We conclude that the fast hiding behaviour of locusts is a specific goal-directed type of optomotor behaviour requiring positional information from small-field detectors of shape expansion in the interneurone layers of the locust eye.

Visual system of the european hummingbird hawkmothMacroglossum stellatarum (sphingidae, lepidoptera): Motion-sensitive interneurons of the lobula plate

The European hummingbird hawkmoth Macroglossum stellatarum is a member of the sphingid family, denoted by their ability to hover in place in front of flowers. The fast and acrobatic flight behavior is thought to be under the control of the optomotor system both during normal, forward flight and during stationary, hovering flight. Electrophysiologic and neuroanatomic studies presented here reveal large-field, motion-sensitive neurons in the lobula plate. Anatomic and physiologic features characterize these nerve cells as horizontal and vertical motion-sensitive neurons. Horizontal cells react best to horizontal movement of vertical gratings moving in either direction and show no response to vertically moving horizontal gratings. The dendritic arborizations of horizontal cells are found characteristically in the two outer layers of the lobula plate. In contrast, vertical cells react best to upward or downward motion of horizontal gratings. They are not sensitive to horizontal-moving gratings. The dendritic arborizations of the vertical cells are restricted to the two innermost lobula plate layers. These anatomic and physiologic features, as well as a number of other characteristics, such as tonic responses and cosine-shaped tuning curves, are most reminiscent of neurons that comprise the horizontal and vertical systems described from the fly, thus suggesting comparable roles in the control of optomotor behavior. The present study also identifies a small group of neurons that exhibit phasic responses and reactions to specific orientations of the pattern. These cells are discussed with regard to their possible roles in control tasks, such as edge-orientation detection or the detection of sudden displacements of the visual surround.

Wide distribution of the cysteine string proteins in Drosophila tissues revealed by targeted mutagenesis.

The "cysteine string protein" (CSP) genes of higher eukaryotes code for a novel family of proteins characterized by a "J" domain and an unusual cysteine-rich region. Previous studies had localized the proteins in neuropil and synaptic terminals of larval and adult Drosophila and linked the temperature-sensitive paralysis of the mutants described here to conditional failure of synaptic transmission. We now use the null mutants as negative controls in order to reliably detect even low concentrations of CSPs by immunohistochemistry, employing three monoclonal antibodies. In wild-type flies high levels of cysteine string proteins are found not only in apparently all synaptic terminals of the embryonic, larval, and adult nervous systems, but also in the "tall cells" of the cardia, in the follicle cells of the ovary, in specific structures of the female spermatheca, and in the male testis and ejaculatory bulb. In addition, low levels of CSPs appear to be present in all tissues examined, including neuronal perikarya, axons, muscles, Malpighian tubules, and salivary glands. Western blots of isolated tissues demonstrate that of the four isoforms expressed in heads only the largest is found in non-neural organs. The wide expression of CSPs suggests that at least some of the various phenotypes of the null mutants observed at permissive temperatures, such as delayed development, short adult lifespan, modified electroretinogram, and optomotor behavior, may be caused by the lack of CSPs outside synaptic terminals.

Gating of sensory responses of descending brain neurones during walking in crickets

Single descending brain neurones were recorded and stained intracellularly in the neck connectives of crickets while they walked upon a styrofoam ball under open-loop conditions. The animal's translational and rotational velocities were measured simultaneously, and various stimuli were used to investigate the neuronal response characteristics. Stimulation with a moving grating or an artificial calling song of 5 kHz induced optomotor behaviour and positive phonotaxis. An acoustic stimulus of 20 kHz elicited negative phonotaxis. <P> We report the first clear evidence for behaviourally dependent gating of sensory responses of identified descending brain neurones. Most descending cells only responded to visual stimuli or to an artificial calling song of 5 kHz while the animal was walking, indicating that the responses to these stimuli were gated by the walking activity of the animal. In contrast to this, responses to stimuli that elicit negative phonotaxis, such as acoustic stimuli of 20 kHz, were not gated. This indicates that the gating of sensory responses in these cells depends on the behavioural context of the stimulus. <P> From these findings, we conclude that significant information about the properties of sensory processing in higher-order neurones can only be gained from tests in behaviourally relevant paradigms. Important characteristics might otherwise be missed, thus leading to misinterpretations regarding their function. <P>

Optomotor Behaviour in Xenopus Laevis Tadpoles as a Measure of the Effect of Gravity on Visual and Vestibular Neural Integration

The ability of aquatic vertebrates to maintain their position requires integration of visual and vestibular sensory information. To understand better how aquatic animals integrate such information, we measured the optomotor behaviour of Xenopus laevis tadpoles raised in growth chambers in microgravity (< 10(-3)g), normal gravity (1 g), hypergravity (3 g) and on a slowly rotating clinostat (simulated microgravity). The goal of this research was to determine how development in an altered gravitational force field affects the visual- and vestibular-dependent behaviour of tadpoles. This research represents the first time that the optomotor behaviour of an organism raised from fertilization in microgravity has been tested. Significant differences were observed in the optomotor behaviour among the four gravity treatments. When first exposed to normal gravity, the microgravity-raised tadpoles exhibited the strongest (or most positive) optomotor behaviour, while the 3 g centrifuge tadpoles showed no optomotor response. Some abnormal behaviours (such as erratic swimming, lying motionless and abnormal swimming posture) were observed in the tadpoles raised in altered gravity on the initial day of testing. One day later, the tadpoles raised in hypergravity did not differ significantly in their optomotor behaviour from control tadpoles raised in normal gravity. However, tadpoles raised in microgravity still displayed an exaggerated optomotor response. One week after the tadpoles had been introduced to normal gravity, there was no longer a significant difference in optomotor behaviour among the different gravity treatments. This convergence of optomotor behaviour by tadpoles from the different treatment reflects the acclimation of their vestibular systems to normal gravity.

BLIND MEXICAN CAVE FISH (ASTYANAX HUBBSI) RESPOND TO MOVING VISUAL STIMULI

In apparatus for measuring optomotor behaviour, blind Mexican cave fish, Astyanax hubbsi, increase their swimming velocity upon rotation of a striped cylinder, i.e. in response to a solely visual stimulus. The fish follow the movements of the stripes at (i) rotation velocities between 60 degrees s-1 and 80 degrees s-1, (ii) light intensities of less than 20 lx and, (iii) stimulus widths subtending an angle of less than 1 &deg;. Extirpation of the vestigial eye structures does not affect the response to the moving visual stimulus, which indicates that the response is mediated by extra-ocular photoreceptors. An optomotor response can be reliably evoked in a round test aquarium. Fish do not respond when the test aquarium contains environmental cues, such as bars on the wall or when a section of the round aquarium is divided off. This indicates that the fish obtain information about their environment from different sensory sources and that the visual stimulus is effective only when no other means of orientation are available. We suggest a modified theory of the optomotor response, which emphasizes the crucial role of the environment in eliciting the response and which permits behaviours more complex than just following the stimulus.

Tracking of small objects in front of a textured background by insects and vertebrates: phenomena and neuronal basis.

To follow visually a small object moving in front of a textured background, insects and vertebrates can employ a similar strategy: saccadic tracking. In the case of vertebrates, the neural components that generate this behavior are not known in detail. The neural substrate of optomotor behavior in Diptera is relatively well understood. Here a model developed from the dipteran data is found to be capable of saccadic tracking. It is characterized by the following components and functions: (1) Two subsystems contribute to the response, a small-field tracking system and a large-field compensatory optomotor system, as suggested previously (Egelhaaf et al. 1988). (2) Both systems need to be suppressed during saccadic rotation. In the small-field system, the suppression, close to the visual input, is mediated by the activity of the large-field system. In the large-field system, suppression, close to the motor output, is due to efferent signals from the saccade generator. A similar model could also apply to vertebrates. Two implications of the present model are that saccadic tracking does not require object identification, and under saccadic tracking it is the background rather than the object that is stabilized on the retina. If objects are identified under these conditions, this must occur even though their image is not stabilized on the retina.

Malathion induced changes in the optomotor behavior of an Indian carp, Labeo rohita.

Malathion induced changes in the optomotor behavior of an Indian carp, Labeo rohita.

Brain acetylcholinesterase activity and optomotor behavior in bluegills, Lepomis macrochirus exposed to different concentrations of diazinon.

Organophosphorus pesticides inhibit acetylcholinesterase (AChE) activity to varying degrees in different species of fish. Estimation of AChE activity is a useful tool for establishing the degree of pollution caused by these pesticides. Behavioral changes are very good and sensitive indicators of any chemical pollution. Changes in the optomotor behavior are easily quantifiable. Therefore estimation of AChE activity and changes in the optomotor response are taken as criteria to study the effects of different concentrations (15, 30, 45, 60 and 75 micrograms/l) of diazinon, an organophosphorus compound, in bluegill Sunfish, Lepomis macrochirus. The fish were exposed for a period of 24 hours. In this study, AChE activity showed a significant decline above an exposure concentration of 45 micrograms/l exposure concentration. In the case of optomotor behavior, a decline in the scores of the "following" responses of the fish was noticed from an exposure concentration of 30 micrograms/l. It seems that a behavioral bioassay is more sensitive than other types of testing.

Mutations in the proximal region of the optomotor-blind locus of Drosophila melanogaster reveal a gradient of neuroanatomical and behavioral phenotypes.

Mutations in the complex optomotor-blind (omb) gene locus (4C4-6) lead to a number of different phenotypes in various tissues of the adult Drosophila melanogaster fly. At the core of the locus lies a lethal complementation group, named l(1)omb, whose mutations cause larval and pupal lethality. Some 40% of all males hemizygous for lethal omb alleles develop to the pharate adult stage. These flies can be rescued from the pupal case and show a severe disturbance in optic lobe development. The recessive viable allele In(1)ombH31 reduces the optomotor response in walking flies and during stationary flight of tethered flies. At the neuroanatomical level, these animals lack a subset of lobula plate giant neurons (LPGNs), which are thought to mediate optomotor behavior. Chromosomal aberrations deleting the proximal, non transcribed part of the locus complement the lethality, but still cause neuroanatomical and optomotor defects. Analysis of different allelic combinations of such mutations, in which increasing amounts of DNA downstream of the transcribed region are removed, reveals a step gradient of increasing severity of the neuroanatomical defects and behavioral phenotypes. On this basis the 3'-regulatory region is divided into three domains each having specific effects on optic lobe development.

Genetic and molecular characterization of the optomotor-blind gene locus in Drosophila melanogaster.

The Drosophila gene optomotor-blind (omb) is involved in the development of a set of giant neurons in the optic lobes and possibly other structures in the imaginal brain. Adult flies have discrete defects in optomotor behavior. The gene has previously been mapped in chromomeres 4C5-6, together with three other genes, bifid, Quadroon and lacqueredgls. We have localized the gene in a genomic walk of 340 kb of DNA. By mapping seven chromosome breakpoints with omb phenotype we determined its minimum size to about 80 kb. From this region more than 20 RNAs of different size and temporal expression pattern are transcribed. Three of them (T3, T7 and T7') stem from primary transcripts of 40-80 kb in length. In its distal part the omb gene overlaps in at least 19 kb with four other complementation units, bifid, l(1)bifid, Quadroon and lacqueredgls. The three nonlethals affect the external appearance of the fly and seem to be unrelated to brain development.

Morphological and functional characteristics of arpa (receptor potential absent) visual mutant of the blowfly (Calliphora erythrocephala)

1. We have discovered a previously unreported visual mutant of the blowfly,Calliphora erythrocephala. It shows a reduced or absent visual performance, e.g., in escape and optomotor behavior. The effects of this mutation on the ultrastructure were studied by electron microscopy (Figs. 3–8) and on electrophysiological function, by intracellular recordings (Figs. 1 and 2). 2. The genetic basis of this spontaneous mutation was studied by test crosses of mutant and wild-type flies. The defect appears to be in an autosomal recessive gene (Table 1). 3. Of the mutant stock studied soon after eclosion (n = 18) 35% shows optomotor reactions, whereas only 6% studied in later life (n = 240) shows any optomotor behavior. 4. The absence of the receptor potentials in photoreceptor cells is not directly associated with structural disorders in the early life of these mutant flies, but several types of degenerative changes are manifested in the retinular cells later on. The optomotorically blind specimens have normal (about −60 mV) resting membrane voltages but no detectable receptor cell voltage response to light, indicating a block in phototransduction. The spectral and polarization sensitivities of optomotor-positive flies are normal (Fig. 2). 5. At the beginning of degeneration the number of lysosomes in the receptor cells is increased compared with normal flies, but their number as well as that of other components of the cell interior decrease later on. During the progression of the degeneration, the rhabdomeres shrink while the mitochondria swell and disintegrate (Figs. 6–8). 6. The blocking of phototransduction is proposed to lead to disturbance of the turnover of the rhabdomeres and finally to degeneration of the receptor cells.

Behavioral Correlates of Cerebellar Ablations in the Teleost, &lt;em&gt;Aquidens Latifrons&lt;/em&gt;

The effects of ablation of the corpus, eminentia granularis and valvula of the cerebellum on the performance of optomotor tasks, and the appearance of atypical behavior patterns were studied in the teleost fish Aquidens latifrons. The subjects were observed in their home tanks before and after surgery, and were tested in a modified optomotor apparatus where the drum changed direction of rotation at regular intervals. The corpus cerebellum was ablated totally or partially, bilaterally or unilaterally. In other subjects the eminentia granularis was ablated on the right side or in conjunction with ipsilateral corpus lesions. The valvula was completely ablated in still other subjects with only slight damage to adjacent brain tissue.When experimentally naive intact fish were given a series of optomotor tests they gradually improved their optomotor performance. After cerebellar operations this improvement was reversed in most of the optomotor measurements as the fish followed the moving stripes much less efficiently. However swimming speed, which we considered a good indicator of motor performance, was unchanged except in 2 out of 13 groups. We concluded that the less efficient optomotor behavior could not be attributed to a direct effect of the lesions on motor processes. The home-tank observations clearly revealed four postoperative motor abnormalities. Oscillatory movements, wobbling and tilting persisted through the tests, but the fourth, lying on the side, a more profound disability, disappeared in all but one subject in a few hours to a few days. The first three abnormal behavior patterns, especially the oscillatory movements, suggest a deficiency in fme motor tasks and support the interpretation that the major function of the cerebellum is described best as the modulation of movement. High levels of tilting and lying on the side in subjects with unilateral lesions maybe caused by an inbalance in motor function. Several alternative or additional functions of the cerebellum suggested by these experiments are evaluated.

Drosophila mutants disturbed in visual orientation

With the Y-maze selection technique de- scribed in Part 1 2 strains of probably central nervous system (CNS) mutants have been isolated. These mu- tants show defects in the computation of both position and movement. One of these mutants (nofg B12) shows strong avoidance of small patterns moving with high velocity. This inversion of the object-induced orien- tation response can be mainly attributed to a "modifi- cation of responses to fast progressive (front-to-back) movement. It is thus possible that overall optomotor behaviour may be decomposed into a set of genetically independent modules.

Horizontal movement detectors of honeybees: Directionally-selective visual neurons in the lobula and brain

1. Intracellular recordings have been made from both input (ipsilateral) and output (contralateral) ends of directionally-selective optomotor neurons in the left lobulae of worker honeybees. Optical stimuli were two, monocular, horizontally-moving vertical gratings placed on opposite sides of the bee's head. The eyes could be stimulated separately or together. 2. Horizontal regressive motion-sensitive (HR) cells are strongly excited (and depolarized) by ipsilateral regressive motion. They are moderately excited by contralateral progressive motion but are inhibited by contralateral regressive motion. Ipsilateral progressive motion has little effect (Figs. 1 and 2). The HR cells (HRLeft and HRRight cells) are bilateral, reciprocal neurons which run from one lobula to the other via the anterior optic tracts, the optic tubercles, and the intertubicular tract. They have co-extensive dendrites and terminals in the distal lamellae of the lobulae (Figs. 4–6). HR cells are the bees' optomotor neurons, known hitherto from extracellular recordings. 3. Horizontal progressive-motion sensitive (HP) cells (HPRight and HPLeft cells) are excited and depolarized by ipsilateral progressive motion but are inhibited and hyperpolarized by ipsilateral regressive motion. It is uncertain if there are bilateral influences on HP cells (Figs. 7 and 8). No stained HP cells have been recovered. 4. Other directionally-selective cells with and without spikes have also been stained and reconstructed (Figs. 9 and 10). 5. A model network is proposed between HR and HP cells in which a) HR cells mutually inhibit each other; b) the ipsilateral, input end of each HR cell inhibits the HP cell originating in the same lobula; and c) the contralateral, output terminals of each HP cell excite the HR cell originating in the opposite lobula (Fig. 11 A). It is discussed how the model could explain the observed directional selectivities of cells (Figs. 11B, C and 12). Additionally, the possible role of such a model network in optomotor behavior is considered.

Effects of experience on optomotor performance in the cichlid fish Aequidens latifrons

Laboratory-bred cichlid fishes, Aequidens latifrons, were tested individually in a modified optomotor apparatus in which the rotation of the vertically striped drum changed direction every 56 sec. Over a period of five consecutive daily tests, quantitative changes in optomotor behavior that are characterized as more efficient responding occurred. That is, the fish followed the moving stripes more accurately in all the measures that we used to define it. Retesting some subjects on Days 11–15, 43–47, and 89–93 showed that these changes in behavior persisted and are therefore characterized as a learning phenomenon. A hypothesis is presented concerning the ontogeny of optomotor behavior based on the experience gained by juveniles in viewing the conspicuous vertical stripes of other members of the school when following them.

Acetylcholinesterase mutants in Drosophila and their effects on the structure and function of the central nervous system.

Mutations that eliminate acetylcholinesterase (AChE) activity were used to study the effects of disrupted acetylcholine metabolism on the form and function of the central nervous system in Drosophila melanogaster. Mutants in the Ace gene, which have no AChE activity, usually die in early development, but the postembryonic effects of this lesion can be studied in genetic mosaics, or with conditional mutants. Adult mosaics, which expressed Ace mutations in part of their CNS, exhibited morphological defects in any ganglionic neuropile whose cells were mutant. The defects included reduction in ganglionic volume, a condensed appearance, and for a very large clone, degeneration. Examination of many such mosaics indicated that small clones restricted to one side of the CNS were not usually lethal. However, mosaics with large clones, with clones on either side of the posterior slope of the protocerebrum, or with clones encompassing symmetrical structures on both sides of the CNS rarely survived to adulthood. Mosaics with AChE-null tissue on either side of the optic lobes or the posterior-inferior protocerebrum had marked deficits in optomotor behavior, although they were outwardly normal in their movement and posture. Mosaics with Ace mutant tissue in the first-order optic lobe, the lamina, lacked a synaptic component of the electroretinogram, the "off" transient. Tests of courtship behavior revealed that AChE mosaics with mutant clones in the superior protocerebrum were often capable of demonstrating male courtship. However, their behavior was quantitatively and perhaps qualitatively deficient. In order to study critical periods for the effects of mutant AChE, temperature-sensitive mutations of the Ace gene were isolated. Flies bearing certain of these new mutations produced AchE activity that was thermolabile in vivo and in vitro. The critical period during which the mutants were most susceptible to conditional lethality was late in embryogenesis.

Response properties of dipteran giant visual interneurones involved in control of optomotor behaviour.

Response properties of dipteran giant visual interneurones involved in control of optomotor behaviour

The participation of all three colour receptors in the phototactic behaviour of fixed walking honeybees

1. The phototactic behaviour of tethered bees which walked on a y-maze globe was investigated under open-loop conditions. The monochromatic stimulus was always presented monocularly; the nonstimulated eye remained in complete darkness. The bees' heads were adjusted so that we always stimulated the same part of the eye (Fig. 1). 2. Twenty-eight ommatidia in the centrolateral region of the eye were stimulated. We determined their coordinates in anx-y-z system (Figs. 6, 7, and Table 1). 3. The bees usually tried spontaneously to turn towards the light (positive phototaxis). Only one animal showed negative phototaxis (Figs. 2 and 8). 4. The phototactic reaction (R) is a function of light intensity (I) and wavelength (λ): R=R (I, λ) (Fig. 2). 5. The slopes of theR(I)-curves are dependent on wavelength. TheR(I)-curves for 410 nm and 492 nm have significantly larger gradients than those for all other wavelengths (Figs. 2–4). 6. We calculated spectral sensitivity curves [S(λ)-functions] for different reaction levels. Near threshold, the curves have 3 peaks; at higher intensities additional peaks appear (Fig. 5A and B). The subjective brightness values of the colours for the bees are reflected only by theS(λ)-function at the threshold intensity. Colour-specific effects come into play at higher intensities. 7. All three visual cell types of the bee-ultraviolet, blue and green receptors-participate in the control of phototactic behaviour. We have been able to demonstrate, for the first time, the participation of the blue receptor. In addition, this proves that all three colour receptors occur in the centrolateral region of the compound eye. 8. The bee exhibits differentS(λ)-functions for different behavioural patterns: theS(λ)-function in phototactic behaviour is very different from that in optomotor behaviour, even if thesame region of the eye is stimulated. Thus the circuitry at the receptor level and/or the central nervous evaluation of the information coming from the receptors is different for each of the two behavioural patterns. 9. Physiological mechanisms are discussed which could explain the discrepancies between our results and those of previous phototaxis investigations.

Effects of continuous light and darkness on the eyes of the troglobitic salamander Typhlotriton spelaeus

Larval Typhlotriton spelaeus collected from five caves in Pulaski Co., Missouri, were kept as larvae or induced to transform in darkness or continuous fluorescent illumination. Larvae maintained in darkness for 215 and 279 days had smaller eyes, smaller rod inner and outer segments, and fewer metaphase figures in the germinative zone of the neural retina than comparable larvae maintained in light (258 lux). Except for visual cell size, differences were small and for each characteristic exceptions were observed. One larva kept in light showed early retinal degeneration comparable to that in transformed adults to T. spelaeus. All larvae exhibited optomotor behavior both before and after the experiment. Among animals induced to transform by L-thyroxin and maintained in darkness 111 to 366 days, visual cell and pigment epithelium degeneration was more extensive and more frequent than in animals kept for the same length of time in light (237-298 lux). In darkness the frequency of animals with retinal degeneration increased between 111 and 366 days. In light some animals exhibited pigment epithelium reduction with normal visual cells, and others had free, pigmented cells in the subretinal space. These effects were not comparable to degeneration in darkness. Eyelids covered the eyes of only a few animals in both light and dark treatments. The extent of eyelid encroachment over the eye greater in darkness than in light. Most animals exhibited optomotor responses after experiments, but responses of animals kept in darkness were impaired in comparison to those of animals kept in light.