A comparative study of specific chromatic adaptation of the wildtype and trp mutant of Drosophila melanogaster

The trp mutant of Drosophila melanogaster was re-examined and compared with the wildtype using monochromatic blue and orange light to manipulate the bi-stable visual pigment states in the peripheral retinula cells R1-6 of white-eyed flies. Recovery of sensitivity by application of orange light either during or after blue-adaptation is different in w;trp flies from that in bw;cn flies and does not proceed as predicted from the trp genotype. Blue-adaptation by isolating the activity of the central retinula cells confirms that the trp lesion affects these receptors also.     

Blue adaptation: an experimental tool for the study of visual receptor mechanisms and behaviour of Drosophila

Physiological and behavioural studies with Drosophila to elucidate visual mechanisms have exploited the bi-stability of the visual pigment in the peripheral retinula cells R1-6, and the 'off-on switch' action of blue and orange light. Measurements of flicker fusion and response waveform from both receptor and lamina regions prior and subsequent to blue adaptation, which induces a prolonged depolarising afterpotential and loss of visual function in R1-6, show these retinula cells to have a high fusion frequency and R7/8, the central retinula cells, a lower fusion frequency. Such measurements also allow analysis of the extracellular response in terms of contributing cells, and its potential for studying the fly's ability to respond to various potential visual cues such as a rotating plane of polarised light. Blue adapted flies fail to fixate normally a black stripe, confirming a role for R1-6 in orientation behaviour requiring a competent degree of acuity.     

Expression of acetylcholinesterase during visual system development in Drosophila

As in other insects acetylcholine (ACh) and acetylcholinesterase (AChE) function in synaptic transmission in the central nervous system of Drosophila. Studies on flies mutant for AChE indicate that in addition to its synaptic function of inactivating acetylcholine, this neural enzyme is required for normal development of the nervous system (J.C. Hall, S.N. Alahiotis, D.A. Strumpf, and K. White, 1980, Genetics 96, 939-965; R.J. Greenspan, J.A. Finn, and J.C. Hall, 1980, J. Comp. Neurol. 189, 741-774). In order to understand what role AChE may play in neural development, it is necessary to know, in detail, where and when the enzyme appears. The use of monoclonal antibodies to localize AChE in the developing visual system of wild type Drosophila has yielded the novel observation that AChE appears in photoreceptor (retinula) cells 4-6 hr after they differentiate and 3 to 4 days before they are functional. Three days later the staining in the cell body of these cells is reduced. Because retinula cells have no functional connections at the time when AChE is first detected, AChE can not be performing its standard synaptic function. Subsequent to the reduction of AChE in the retinula cells, midway through the pupal stage, the enzyme accumulates rapidly in the neuropils of the optic lobes of the brain. Thus, there is a biphasic accumulation of AChE in the developing visual system with the enzyme initially being expressed in the retinula cells and accumulating later in the optic lobes.     

Task-specific association of photoreceptor systems and steering parameters in Drosophila

Visual motion processing enables moving fruit flies to stabilize their course and altitude and to approach selected objects. Earlier attempts to identify task-specific pathways between two photoreceptor systems (peripheral retinula cells 1-6, and central retinula cells 7 + 8) and three steering parameters (wingstroke asymmetry, abdomen deflection, hindleg deflection) attributed course control and object fixation to peripheral retinula cells 1-6-mediated simultaneous reactions of these parameters. The present investigation includes first results from fixed flying or freely walking ninaE17 mutants which cannot synthesize the peripheral retinula cells 1-6 photoreceptor-specific opsin. Retention of about 12% of the normal course control and about 58% of the object fixation in these flies suggests partial input sharing for both responses and, possibly, a specialization for large-field (peripheral retinula cells 1-6) and small-field (central retinula cells 7 + 8) motion. Such signals must be combined to perceive relative motion between an object and its background. The combining links found in larger species might explain a previously neglected interdependence of course control and object fixation in Drosophila. -Output decomposition revealed an unexpected orchestration of steering. Wingstroke asymmetry and abdomen deflection do not contribute in fixed proportions to the yaw torque of the flight system. Different steering modes seem to be selected according to their actual efficiency under closed-loop conditions and to the degree of intended turning. An easy experimental access to abdominal steering is introduced.     

Visual signals in the courtship of Drosophila melanogaster

Drosophila melanogaster carrying either of the mutations sev or dipp⁶ show defective phototactic behaviour owing to deficiencies in the processing of visual information perceived by the central retinula cells (R7, R8). Mutant females show increased time to mating because the deficient visual input via this subsystem has an inhibitory effect on female receptivity. Similarly, deficient input through the peripheral retinula cells (R1–R6) also makes females sexually unreceptive. Thus females require appropriate visual stimulation through both subsystems to become maximally sexually receptive. One major source of this stimulation is the red eye of the male.     

Blue adaptation: An experimental tool for the study of visual receptor mechanisms and behaviour of Drosophila

Physiological and behavioural studies with Drosophila to elucidate visual mechanisms have exploited the bi-stability of the visual pigment in the peripheral retinula cells R1–6, and the off-on switch action of blue and orange light. Measurements of flicker fusion and response waveform from both receptor and lamina regions prior and subsequent to blue adaptation, which induces a prolonged depolarising afterpotential and loss of visual function in R1–6, show these retinula cells to have a high fusion frequency and R7/8, the central retinula cells, a lower fusion frequency. Such measurements also allow analysis of the extracellular response in terms of contributing cells, and its potential for studying the fly's ability to respond to various potential visual cues such as a rotating plane of polarised light. Blue adapted flies fail to fixate normally a black stripe, confirming a role for R1–6 in orientation behaviour requiring a competent degree of acuity.Based on material presented at the European Neurosciences Meeting, Florence, September 1978     

Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster.

Flies display a sophisticated suite of aerial behaviours that require rapid sensory-motor processing. Like all insects, flight control in flies is mediated in part by motion-sensitive visual interneurons that project to steering motor circuitry within the thorax. Flies, however, possess a unique flight control equilibrium sense that is encoded by mechanoreceptors at the base of the halteres, small dumb-bell-shaped organs derived through evolutionary transformation of the hind wings. To study the input of the haltere system onto the flight control system, I constructed a mechanically oscillating flight arena consisting of a cylindrical array of light-emitting diodes that generated the moving image of a 30 degrees vertical stripe. The arena provided closed-loop visual feedback to elicit fixation behaviour, an orientation response in which flies maintain the position of the stripe in the front portion of their visual field by actively adjusting their wing kinematics. While flies orientate towards the stripe, the entire arena was swung back and forth while an optoelectronic device recorded the compensatory changes in wing stroke amplitude and frequency. In order to reduce the background changes in stroke kinematics resulting from the animal's closed-loop visual fixation behaviour, the responses to eight identical mechanical rotations were averaged in each trial. The results indicate that flies possess a robust equilibrium reflex in which angular rotations of the body elicit compensatory changes in both the amplitude and stroke frequency of the wings. The results of uni- and bilateral ablation experiments demonstrate that the halteres are required for these stability reflexes. The results also confirm that halteres encode angular velocity of the body by detecting the Coriolis forces that result from the linear motion of the haltere within the rotating frame of reference of the fly's thorax. By rotating the flight arena at different orientations, it was possible to construct a complete directional tuning map of the haltere-mediated reflexes. The directional tuning of the reflex is quite linear such that the kinematic responses vary as simple trigonometric functions of stimulus orientation. The reflexes function primarily to stabilize pitch and yaw within the horizontal plane.     

Photoreceptor structures. III. Drosophila melanogaster

The eyes of three eye mutants of Drosophila melanogaster were fixed and thin sections studied for its structural detail in the electron microscope. Each ommatidium was found to have seven retinula cells with an equal number of rhabdomeres (visual units). The rhabdomeres average 1.2 micro in diameter and 60 micro in length. Each rhabdomere consists of osmium-fixed dense bands averaging 120 A in thickness, and with less dense interspaces 200 to 400 A. There is an average of 23 dense bands or 46 interfaces per micron within the rhabdomere. The rhabdomere as we have presented it is a single structure of packed rods or tubes. The "fine structure" within the rhabdomere is similar to that observed by electron microscopy for the retinula of the house fly, and to the retinal rods of the vertebrate eye, and to the chloroplasts of plant cells in a variety of animal and plant photoreceptor structures. In addition, the radial arrangements within the ommatidium of radially unsymmetrical units, the rhabdomeres, is probably related to the analysis of polarized light in the insect eye.     

Exploratory activity in Drosophila requires the kurtz nonvisual arrestin

When Drosophila adults are placed into an open field arena, they initially exhibit an elevated level of activity followed by a reduced stable level of spontaneous activity. We have found that the initial elevated component arises from the fly's interaction with the novel arena since: (1) the increased activity is independent of handling prior to placement within the arena, (2) the fly's elevated activity is proportional to the size of the arena, and (3) the decay in activity to spontaneous levels requires both visual and olfactory input. These data indicate that active exploration is the major component of elevated initial activity. There is a specific requirement for the kurtz nonvisual arrestin in the nervous system for both the exploration stimulated by the novel arena and the mechanically stimulated activity. kurtz is not required for spontaneous activity; kurtz mutants display normal levels of spontaneous activity and average the same velocities as wild-type controls. Inhibition of dopamine signaling has no effect on the elevated initial activity phase in either wild-type or krz(1) mutants. Therefore, the exploratory phase of open field activity requires kurtz in the nervous system, but is independent of dopamine's stimulation of activity.     

Graded illumination potentials from retinula cell axons in the bug Lethocerus

Summary Intracellular responses to illumination have been recorded separately from the retinula cells and from their axons in the compound eyes of the giant water bug Lethocerus. The basic response in both places consists of an initial transient depolarisation followed by a plateau (Fig. 2). No action potentials were seen in either axons or retinula cells.The responses are graded according to the intensity of the stimulus, to its position within the visual field of the cells and to the plane of polarization of the light (Figs. 3, 4). The angle of acceptance (dark-adapted eyes) measured in either retinula cells or axons is 9°. Similarly, the average value of the sensitivity ratio to light polarised at orthogonal planes is 31 in both places.Experiments designed to reveal a presumed spike initiation region of the cells by reducing damage to the eye failed to reveal impulses. It is concluded that the receptor potential spreads electrotonically in the axon to the first synaptic region which lies up to 2 mm away. The values of membrane constants which would be required for conduction without severe decrement over such a distance are within the range measured in other systems.     

Visual behaviors of the migratory grasshopper,Melanoplus sanguinipes F. (Orthoptera: Acrididae)

The visual behavior of adult Melanoplus sanguinipesF. (Orthoptera: Acrididae) was investigated by placing individuals in the center of an arena and recording their orientation responses to visual targets at the perimeter of the arena. Targets that reflected more 540- to 570-nm light were approached more frequently; however, when reflectance in the 540 -to 570-nm region was combined with reflectance in the 400- to 520-nm region, orientation responses were reduced significantly. This suggests that spectral discrimination in M. sanguinipesinvolves at least two classes of photoreceptors, which respond to different regions of the wavelength spectrum. In addition, grasshoppers oriented to vertical, but not horizontal, contrasting stripes. However, when vertical stripes were added to targets reflecting 520- to 650-nm light, responses to verticals on these targets were not enhanced relative to verticals presented against a target background of 400- to 520-nm + 520- to 650-nm light. Thus, spectral discrimination and vertical stripe fixation appear to be two distinct visual behaviors, controlled by outputs from two classes of photoreceptors and a single class of photoreceptors, respectively, and may be used in different physiological or ecological contexts.     

The electrical responses of the retinal receptors and the lamina in the visual system of the fly musca

Slow electrical responses were recorded from receptors and from the lamina of the visual pathway of the fly Musca.

1. Receptors 1 to 6 in the retinal ommatidia are identified by their response dichroic sensitivity planes. The half-width of their angular sensitivity distributions is estimated 2.5° in dark adaptation, and found not to vary with ambient illumination. The retinula cells are only excited by light that enters the eye through their overlying corneal facets.
2. The responses of the lamina show no detectable dichroic sensitivity, though in favourable cases their angular sensitivity distributions may be as narrow as those of the receptors. It is shown that these responses are excited by light that enters the six facets of the corneal projection of the single lamina cartridge synapse. The retinula fibres of passage through the lamina, originating from ommatidial cells 7 and 8, evidently do not contribute excitation to the responses.
3. It is shown that the separate responses contributed by the individual receptors of the projection are added linearly at the lamina response compartment over a wide range of light intensities.

     

Light-initiated responses of retinula and eccentric cells in the Limulus lateral eye

The relationship between retinula and eccentric cells in the lateral eye of Limulus polyphemus was studied using a double electrode technique which permitted simultaneous recording of light-initiated responses in two sense cells and the labeling of the cells for subsequent histological examination and identification. The following results were obtained: (a) light-initiated slow responses with and without superimposed spike potentials were recorded from retinula cells and from eccentric cells (only one eccentric cell yielded responses without superimposed spike potentials); (b) spike potentials recorded in different cells within the same ommatidium were always synchronous; (c) a complete absence of spike potentials was observed in two experiments in which no eccentric cells could be found in the ommatidia containing the labeled retinula cells; (d) the greatest differences in the characteristics of responses recorded simultaneously occurred in those recorded from retinula-eccentric combinations. The results indicate that there is only one source of spike potential activity within an ommatidium (presumably the eccentric cell) and that the light-initiated response of retinula cells may be independent of the eccentric cell response. The suggestion is advanced that the response of the retinula cell may "trigger" the eccentric cell response.     

Response properties of motion-sensitive visual interneurons in the lobula plate of Drosophila melanogaster

The crystalline-like structure of the optic lobes of the fruit fly Drosophila melanogaster has made them a model system for the study of neuronal cell-fate determination, axonal path finding, and target selection. For functional studies, however, the small size of the constituting visual interneurons has so far presented a formidable barrier. We have overcome this problem by establishing in vivo whole-cell recordings from genetically targeted visual interneurons of Drosophila. Here, we describe the response properties of six motion-sensitive large-field neurons in the lobula plate that form a network consisting of individually identifiable, directionally selective cells most sensitive to vertical image motion (VS cells). Individual VS cell responses to visual motion stimuli exhibit all the characteristics that are indicative of presynaptic input from elementary motion detectors of the correlation type. Different VS cells possess distinct receptive fields that are arranged sequentially along the eye's azimuth, corresponding to their characteristic cellular morphology and position within the retinotopically organized lobula plate. In addition, lateral connections between individual VS cells cause strongly overlapping receptive fields that are wider than expected from their dendritic input. Our results suggest that motion vision in different dipteran fly species is accomplished in similar circuitries and according to common algorithmic rules. The underlying neural mechanisms of population coding within the VS cell network and of elementary motion detection, respectively, can now be analyzed by the combination of electrophysiology and genetic intervention in Drosophila.     

The superposition eye of Cloeon dipterum: The organization of the lamina ganglionaris

Summary The lamina ganglionaris of the superposition eye of Cloeon dipterum is composed of separate optic cartridges arranged in a hexagonal pattern. Each optic cartridge consists of one central, radially branched monopolar cell (Li) surrounded by a crown of seven retinula cell terminals and two more unilaterally branched monopolar cells (La1/La2) situated close together outside the cartridge. Projections to neighbouring cartridges have not been observed.In most cases, synaptic contacts could be seen between a presynaptic retinula cell and more than two other postsynaptic profiles, which belong to monopolar cells or sometimes to glial cells.Seven retinula cell fibers of one ommatidium pass in a bundle through the basement membrane, run into their respective cartridges without changing orientation and terminate at approximately equal levels in the lamina. Long visual fibers with endings in the medulla are not visible in the superposition eye lamina, but are present in the lateral apposition eye. The relationship between the behaviour of the animal, optic mechanisms of the superposition eye and the structure of the lamina is discussed.     

Height control by free-flying Drosophila

ABSTRACT. In a horizontal wind tunnel, Drosophila flew at almost constant height along tracks up to 2 m long. The flies rose or sank only slowly when it was so dark that they no longer responded to movements of the tunnel floor, suggesting that their height control is mediated, at least partly, by responses to their movement relative to the air. In the light, the flies maintained height better than in the dark and were very responsive to movements around them. They faithfully followed the up and down movements of horizon screens at their sides whether they were flying in still air or against a wind, even in the presence of many other stationary visual cues. The flies did not respond by compensatory height changes to real vertical movements of a patterned horizontal disc beneath them, nor to changes in the size of the floor pattern. They did respond to horizontal acceleration of the floor pattern in the direction opposite to their flight (optically simulating a descent by the fly), by an apparently compensatory increase in height, but they also rose (instead of sinking) in response to floor acceleration in the direction of their flight. When the floor was accelerated in either direction they showed compensatory groundspeed-controlling responses. The increases in height might be alarm responses to sudden movements in the visual field beneath them. Both speed and height changing responses to floor movement were reduced when the number of stationary visual cues was increased. Drosophila thus control their height mainly by responses to the apparent movement of nearby visual cues at round about their own height.     

The first optic ganglion of the bee

Each visual unit (ommatidium) of the compound eye of the honey bee contains nine retinula cells, six of which end as axons in the first synaptic ganglion, the lamina, and three in the second optic ganglion, the medulla. A technique allowing light- and electron microscopy to be performed on the same silver-impregnated sections has made it possible to follow all types of retinula axons of one ommatidium to their terminals in order to study the shape of the terminal branches with their position in the cartridge. 1. The axons of retinula cells 1-6 (numbered according to Menzel and Snyder, 1974) end as three different types of short visual fibres (svf) in the lamina; the axons of retinula cells 7-9 run through the lamina to terminate in the medulla and are known as long visual fibres (lvf). Retinula cells of each type are identified by the location of their cell bodies and by the direction of their microvilli. The retinula cells 1 and 4 (group I according to Gribakin, 1967) end as svf type 1 with three tassel-like branches in stratum B of the first synaptic region. The pair of cells 3, 6 and the pair 2, 5 (group II) end in the first synaptic region in stratum A. Cells 3 and 6 have forked endings, svf type 2, whereas cells 2 and 5 have tapered endings, svf type 3. The remaining retinula cells 7, 8 and 9 have long fibres. Nos. 7 and 8 (group III) have tapered endings and are termed lvf types 1 and 2, respectively. The 9th cell is the lvf type 3 with a highly branched ending. 2. The nine axons in the bundle from one ommatidium have relative positions which do not change from the proximal retina to the monopolar cell body layer. 3. By following silver-stained retinula cells and their corresponding axons, it is possible to describe mirror-image arrangements of fibres in the axon bundles in different parts of the eye. This correlation of numbered retinula cells with specific axon types, together with the highly organized pattern in an axon bundle, allows the correlation between histological and physiological findings on polarization and colour perception.     

Afferent growth cone interactions control synaptic specificity in the Drosophila visual system

In the Drosophila compound eye, photoreceptors (R cells) that respond to light from the same point in space are distributed across the retina and connect to the same target neurons. This complex connectivity pattern reconstructs visual space in the first optic ganglion, the lamina. We have used mutations that delete specific R cell subtypes or alter their retinal organization to define the cellular mechanisms that generate this pattern. R cell axons are programmed to search for targets within a local region in the lamina but their selection of appropriate postsynaptic targets requires specific interactions among R cell growth cones. The orientation of the projections is controlled both by the spatial arrangement of R cells in the retina and by cues in the target.     

Eye color pigment granules in Drosophila mauritiana: mosaics produced by excision of a transposable element

Compound eyes of the white-peach (wpch) mutant strain of Drosophila mauritiana have some pigment and receptor cells with wild-type eye color pigmentation. These eyes are mosaic, because excision of a transposable element reverts wpch to wild type during the development of somatic cells. Wild-type patches have three types of pigment granule residing in three respective cell types: primary pigment cells, secondary pigment cells, and retinula (visual receptor) cells. Most aspects of these granules, as well as all other aspects of compound eye ultrastructure, are exactly as in the better studied sibling species D. melanogaster. In the wpch parts of the eye, small and giant unpigmented "pigment granules" reside in secondary pigment cells. These white granules are just like the corresponding granules of w mutant D. melanogaster. Small vs. large patches of pigmented cells likely represent excision events occurring late vs. early respectively during development. Mosaics of eye color markers have been important in developmental analyses; the ease of constructing mosaics of D. mauritiana gives this preparation advantages for mosaic analyses.     

Polarotaxis and scototaxis in the supratidal amphipod Platorchestia platensis

Talitrid amphipods use many cues for orientation during forays between temporary burrows and feeding areas, and for locating beaches when submerged, with visual cues being particularly important. Little evidence exists for polarized light among these visual cues despite extensive orientation by celestial and underwater polarized light in other crustaceans and in insects. We used electroretinography to assess spectral sensitivity in the eye of the beach flea Platorchestia platensis, and behavioral studies to test whether linearly polarized light serves as an orientation cue. Two spectral classes were present in the P. platensis eye with maxima at 431 and 520 nm. Non-uniform orientation of amphipods in the laboratory arena required either light/dark or polarized cues. Scototactic movements depended on arena conditions (day/night, wet/dry), while orientation under linearly polarized light was wavelength-dependent and parallel to the e-vector. Subsequent tests presented conflicting and additive scototactic and polarotactic cues to differentiate among these responses. In dry conditions, orientation parallel to the polarization e-vector overcame a dominant negative scototaxis, confirming that polarotaxis and scototaxis are separate orientation responses in this species. These behavioral results demonstrate talitrid amphipods can perceive and orient to linearly polarized light, and may use it to orient toward preferred zones on beaches.