Ability of the desert locust (Schistocerca gregaria) to compensate for visual deprivation during the final pre‐adult and adult stages

In the desert locust (Schistocerca gregaria Forsskål), vision is a seemingly indispensable prerequisite for many behaviour patterns. The question arises as to whether and to what extent other senses can compensate for the loss of vision, and whether this can take place in the adult stage. To answer this question, both of the compound eyes of nymphs in the final pre‐adult stage are blinded (but not the ocelli), resulting in permanent visual deprivation during adult life. The results are somewhat unexpected: under laboratory conditions, in comparison with sighted controls, the blinded locusts do not exhibit any noticeable change in overall agility relative to daily activity, nor any detriment in terms of the final moult, reproductive rate or longevity. In their search for a specific food source in an experimental arena with a narrow passage between the compartment where the animals are released and the compartment containing food, in the first trial, visually deprived females need significantly more time than the sighted controls. However with an increasing number of trials, each performed after 1 day of food deprivation, the food finding latency of blinded locusts (S. gregaria) approaches or even surpasses that of normally sighted locusts. The blinded locusts use their antennae, mouthparts and tarsi more extensively, suggesting a more frequent use of tactile and chemical cues, which they gradually learn to use more efficiently. The results indicate that pre‐adult and adult S. gregaria can respond to abrupt, permanent changes in their sensory inputs, and have a significant capacity for adaptation.     

Separating food and water deprivation in locusts: effects on the patterns of consumption, locomotion and growth

Abstract. In a factorial experiment, fifth-instar Locusta migratoria (L.) (Orthoptera: Acrididae) were given either dry food (lyophilized grass) and drinking water, food only, water only, or neither food nor water.Food consumption and insect weight were measured daily, and the behaviour of each locust was recorded for 5 h on each of four consecutive days and for 2.5 h on the fifth.Consumption declined progressively in locusts given food only, and those given water only were not observed to drink after the first day of food deprivation.The decline in food consumption on the first day was accounted for by a decrease in the average duration of feeds, which remained constant thereafter.The further decline in consumption over subsequent days was due to a progressive decline in the number of feeds.Although food availability did not slow weight loss relative to locusts given neither food nor water, the availability of water without food did.The proportion of time locomoting increased in all deprivation treatments, but the pattern of change across the five observation days differed markedly between treatments.Locusts given food but no water increased locomotion from 20% of the time budget (the value for controls) to 30% on the first day of deprivation, and by the second day had reached a plateau of approximately 65%.which was maintained until the experiment was terminated on day 5.In contrast, locusts given water but no food approached the 65% level of locomotion on the first day, which was stutistically greater than the 55% observed in those deprived of both food and water.This increase was due both to an increase in the number of locomotion bouts initiated and an increase in the average duration of locomotion bouts.On the second and third days, all deprivation treatments maintained locomotion at around 65%.By day 4, locomotion had decreased to approximately 15% in locusts deprived of both food and water, but not in those deprived of food only or water only.Unlike those given only food, locusts given only water showed a reduction in locomotion of c. 15% on the fifth day.     

Assembly of rhabdomeric membrane from smooth endoplasmic reticulum can be activated by light in chromophore-deprived photoreceptors of Manduca sexta

Summary Deficiency of the photopigment chromophore, resulting from carotenoid/retinoid (vitamin A) deprivation, that severely impairs the visual function of Manduca sexta also leads to the hypertrophy of smooth endoplasmic reticulum in the photoreceptors. The excess endomembrane accumulates in the stacked cisternae of myeloid bodies. Although 11-cis retinal promotes substantial recovery of function in the retinas of deprived moths maintained in darkness, the myeloid bodies remain. When such recovering photoreceptors were exposed to light of moderate intensities, the amount of endomembrane diminished to normal levels over a period of several hours, while rhabdomeres grew larger. Since there was no endocytolysis, the myeloid bodies must have provided the membrane for rhabdomere enlargement. Bright light similarly mobilized the myeloid bodies in deprived receptors. Thus the persistence of myeloid bodies in moderately illuminated chromophoredeficient receptors is a consequence of their insensitivity. However, the initial hypertrophy of endomembrane does not appear to result from the lack of adequate stimulation: normal, chromophore-replete photoreceptors maintained in darkness from before the period of retinal development had large rhabdomeres and no myeloid bodies. The development of myeloid bodies during the differentiation of vitamin A-deprived photoreceptors appears to entail an influence of the chromophore at another level of receptor cell function.     

Microvillar components of light adaptation in blowflies

The process of light adaptation in blowfly photoreceptors was analyzed using intracellular recording techniques and double and triple flash stimuli. Adapting flashes of increasing intensity caused a progressive reduction in the excitability of the photoreceptors, which became temporarily suppressed when 3 x 10(6) quanta were absorbed by the cell. This suppression was confirmed by subsequently applying an intense test flash that photoactivated a considerable fraction of the 10(8) visual pigment molecules in the cell. The period of temporary desensitization is referred to as the refractory period. The stimulus intensity to render the receptor cell refractory was found to be independent of the extracellular calcium concentration over a range of 10(-4) and 10(-2) M. During the refractory period (30-40 ms after the adapting flash) the cell appears to be "protected" against further light adaptation since light absorption during this period did not affect the recovery of the cell's excitability. Calculations showed that the number of quantum absorptions necessary to induce receptor refractoriness is just sufficient to photoactivate every microvillus of the rhabdomere. This coincidence led to the hypothesis that the refractoriness of the receptor cells is due to the refractoriness of the individual microvilli. The sensitivity of the receptor cells after relatively weak adapting flashes was reduced considerably more than could be accounted for by the microvilli becoming refractory. A quantitative analysis of these results suggests that a photoactivated microvillus induces a local adaptation over a relatively small area of the rhabdomere around it, which includes several tens of microvilli. After light adaptation with an intense flash, photoactivation of every microvillus by the absorption of a few quanta produced only a small receptor response whereas photoactivation of every rhodopsin molecule in every microvillus produced the maximum response. The excitatory efficiency of the microvilli therefore increases with the number of quanta that are absorbed simultaneously.     

The fine structure of the compound eye of a damsel-fly

Summary The compound eyes of two species of damsel-flies, Ishunura senegalensis and Cersion calamorum, were examined by electron microscopy. Each ommatidium is composed of eight retinula cells which are semistratified in the receptor layer. The retinula cells are divided into four types from the difference of levels in the rhabdom formation; one distal large cell having the rhabdomere only in the distal layer, four middle cells forming the rhabdom in the middle layer, two proximal cells making up the rhabdom in the proximal layer and one distal small cell having no rhabdomere in any layers. In addition, the lamina ganglionaris was partly observed. Some retinula axons terminate at an different level from the other axons. The functional differentiation among these different types of cells is discussed with relation to the analysis of the polarized light and the discrimination of the diffraction images.This work is supported by a grant from the U.S. Army Research and Development Group (Far East), Department of the Army (DA-CRD-AG-S29-544-67-G61).The authors wish to express their gratitude to Drs. H. Morita and H. Tateda for their helpful discussions throughout this study.     

WASp is required for the correct temporal morphogenesis of rhabdomere microvilli

Microvilli are actin-based fingerlike membrane projections that form the basis of the brush border of enterocytes and the Drosophila melanogaster photoreceptor rhabdomere. Although many microvillar cytoskeletal components have been identified, the molecular basis of microvillus formation is largely undefined. Here, we report that the Wiskott-Aldrich syndrome protein (WASp) is necessary for rhabdomere microvillus morphogenesis. We show that WASp accumulates on the photoreceptor apical surface before microvillus formation, and at the time of microvillus initiation WASp colocalizes with amphiphysin and moesin. The loss of WASp delays the enrichment of F-actin on the apical photoreceptor surface, delays the appearance of the primordial microvillar projections, and subsequently leads to malformed rhabdomeres.     

Recovery from monocular deprivation in the monkey. III. Reversal of anatomical effects in the visual cortex

Transneuronal autoradiography was used to study the effects of visual deprivation on the ocular dominance stripes in layer IVc of the striated cortex of Erythrocebus patas (Old World) monkeys. The animals were studied after: (a) 21-28 days of monocular deprivation starting at, or within, a few days of birth; (b) the same treatment followed by a further 3, 6, 15 or 126 days of monocular vision through both eyes (reopening). One other monkey was monocularly deprived from birth to 1890 days. In most cases the behaviour of the ocular dominance stripes formed by the initially closed eye was studied. After 24 days of monocular deprivation from birth, the input from the normal eye was distributed uniformly within layer IVc, with no periodicity evident. After 21 days of deprivation, the deprived eye's input formed narrow stripes occupying about 38% of layer IVc in the operculum. Seven months of monocular deprivation reduced this to about 29%. Opening the closed eye after the deprivation produced no change in the area innervated: when periods of 15 or 96 days of binocular vision followed the deprivation, the areas innervated by the initially deprived eye were 26 and 30% respectively. However, in both cases the deprived eye's input formed blobs and spots, rather than uniformly narrow stripes. In contrast to reopening, reverse suturing increased the fraction of layer IVc occupied by input form the initially deprived eye. In the operculum, the effects of reverse suturing appeared to be fully developed after only 6 days of reversal: the initially deprived eye's stripes having expanded to occupy about 50% of layer IVc. A further 9 days' reversal produced little change in this. In the visual cortex in the calcarine fissure, the effect of the initial deprivation ws more severe, and the expansion induced by reverse suturing more pronounced. The initial deprivation caused the stripes to shrink to occupy 24% of layer IVc; after 6 days of reverse sulture the proportion increased to 52%, while after 15 days of reverse suture about 88% of IVc was occupied. These results show that reverse suturing can cause fresh growth of afferent axons in regions of layer IVc from which they had been at least partially removed, either by the normal process of segregation, or as a consequence of monocular deprivation. Taken in conjuction with the findings of the accompanying two papers (Blackemore et al...     

The role of the glandular lobes of the corpora cardiaca during flight in Locusta

ABSTRACT. Flight performance in Locusta is reduced following severance of the major afferent nerves to the corpora cardiaca or removal of the glandular lobes of the corpora cardiaca. These operations prevent the release of adipokinetic hormone and the consequent mobilization of stored lipid. However, locusts deprived of about 90% of their glandular lobe tissue, while flying poorly, did mobilize lipid. It is suggested that the remaining glandular parenchyma cells are capable of secreting enough hormone to stimulate lipid mobilization, but that the concentration may be inadequate to encourage lipid utilization. After removal of all the glandular lobe parenchyma, the blood carbohydrate concentration was temporarily depressed. Nevertheless flight performance was equally poor, both when haemolymph carbohydrate levels were low and when they had returned to normal. After the injection of trehalose into operated control locusts and locusts deprived of their glandular lobes, flight was still markedly poorer in the operated insects, even though the injection of trehalose prevented adipokinetic hormone release in the intact locust. It seems that the poor flight performance of locusts deprived of their glandular lobes cannot be fully explained by the simple absence of adipokinetic hormone.     

Experience-driven axon retraction without binocular imbalance in developing visual cortex

Refinement of the neural circuit during brain maturation is regulated by experience-driven neural activity. In the mammalian visual cortex, monocular visual deprivation (MD) in the early postnatal life causes a significant loss of cortical responses to a deprived eye and the retraction of input axons serving the deprived eye. A competitive interaction between inputs serving both eyes has been supposed to underlie the effects of MD because the loss of cortical response is much weaker when both eyes are deprived of vision. Also, the input axons do not retract after binocular deprivation. Here, we report that uncorrelated activity between presynaptic and postsynaptic neurons can solely lead to the retraction of geniculocortical axons in the absence of activity imbalance between two inputs. We analyzed the morphology of geniculocortical axons in a pharmacologically inhibited visual cortex of animals with normal vision and of binocularly deprived animals. In the normal vision animals, the axonal arbors in the inhibited cortex showed robust retraction. On the other hand, the arbors in binocularly deprived animals remained mostly intact. These results suggest that a homosynaptic associative mechanism, rather than a heterosynaptic competition between inputs, may play an important role in experience-driven axon retraction.     

Cofilin/ADF is required for retinal elongation and morphogenesis of the Drosophila rhabdomere

Drosophila photoreceptors undergo marked changes in their morphology during pupal development. These changes include a five-fold elongation of the retinal cell body and the morphogenesis of the rhabdomere, the light sensing structure of the cell. Here we show that twinstar (tsr), which encodes Drosophila cofilin/ADF (actin-depolymerizing factor), is required for both of these processes. In tsr mutants, the retina is shorter than normal, the result of a lack of retinal elongation. In addition, in a strong tsr mutant, the rhabdomere structure is disorganized and the microvilli are short and occasionally unraveled. In an intermediate tsr mutant, the rhabdomeres are not disorganized but have a wider than normal structure. The adherens junctions connecting photoreceptor cells to each other are also found to be wider than normal. We propose, and provide data supporting, that these wide rhabdomeres and adherens junctions are secondary events caused by the inhibition of retinal elongation. These results provide insight into the functions of the actin cytoskeleton during morphogenesis of the Drosophila eye.     

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 µ in diameter and 60 µ 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.     

Partial compensatory growth in hybrid tilapia Oreochromis mossambicus × O. niloticus following food deprivation

The capacity of hybrid tilapia Oreochromis mossambicus × O. niloticus [23.2 ± 0.2 g (mean ± SE)] to show compensatory growth was assessed in an 8‐week experiment. Fish were deprived of feed for 1, 2 and 4 weeks, and then fed to satiation for 4 weeks; fish fed to satiation during the experiment served as control. Water temperature gradually declined from 28.1 to 25.5°C throughout the experiment. Specific growth rate (SGR) decreased with progressive food deprivation. At the end of deprivation, body weight was lower in the deprived fish than in the control. Fish deprived for 4 weeks exhibited lower contents of lipids and energy in whole body, and higher moisture content and ratio of protein to energy (P/E) than those of the control; they also consumed feed faster than the control when normal feeding was resumed. All deprived fish showed higher food intake (FI) than that of the control during re‐alimentation; however, enhanced SGR was only observed in the fish deprived for 4 weeks. There were no significant differences in digestibility of protein and energy, food efficiency (FE) or energy retention efficiency between the control and deprived fish. At the end of re‐alimentation, deprived fish failed to catch up in body weight with the control, while content of moisture, lipids and energy, and P/E in whole body of the deprived fish did not significantly differ from that of the control. The results of the experiment revealed that the hybrid tilapia reared in freshwater showed partial capacity for compensatory growth following food deprivation of 4 weeks, and that growth compensation was due mainly to increased FI, rather than to improved FE.     

THE MICROSTRUCTURE OF THE COMPOUND EYES OF INSECTS

The apposition eyes of two diurnal insects, Sarcophaga bullata (Diptera) and Anax junius (Odonata), have been examined with the electron microscope. In the latter case only the rhabdom is described. The rhabdom of the fly consists of a central matrix and seven rhabdomeres, one for each retinula cell. The rhabdomeres show an ordered internal structure built up of transverse tubes, hexagonal in cross-section. These slender compartments running the width of the rhabdomere are 370 A in diameter. After fixation with osmium tetroxide the walls of the compartments are more electron dense than the interiors. The retinula cells contain mitochondria, and pigment granules smaller than those found in the pigment cells. These granules tend to cluster close behind the membranes which separate the retinula cells from their rhabdomeres. The rhabdom of the dragonfly is a single structure which appears to be composed of three fused "rhabdomeres," each similar to a rhabdomere of Sarcophaga. Reasons are given for believing that the rhabdom may be the site of photoreception, as well as the organ for analyzing plane-polarized light, as suggested by other workers.     

Ultrastructural changes of the microvillar cytoskeleton in the photoreceptor of the crayfish Orconectes limosus related to different adaptation conditions

In the retina of crayfish microvilli of seven of the eight photoreceptor cells build highly organized structures, the rhabdoms. Cytoskeletal elements inside the microvilli were investigated in conventional and slightly extracted electron microscopical preparations. In conventional preparations the ultrastructure of these cytoskeletal elements depended on the adaptational state of the animal. They appeared as central filament-like structures inside each microvillus when dark-adapted retinae were prepared and fixed at night in the absence of calcium. Changes of these conditions (light, daytime, or calcium concentration) impaired the detectability of these central filaments; in light-adapted eyes prepared at midday they were rarely seen. Nevertheless, single microvillar filaments were present in light-adapted retinae after mild cell permeabilization with the saponin beta-escin. They appeared as a regular structure in each microvillus, often attached to the membrane. Their fine structure was consistent with the ultrastructure of single actin filaments as indicated by fast-Fourier-analysis and further supported by the presence of anti-actin immunoreactivity in electron microscopical and immunocytochemical preparations. These results indicate that microvillar filaments are not necessarily destroyed by light as previously described; we suggest that their appearance inside the microvillus might be altered by the properties of associated, maybe sidearm-like proteins.     

Angular and spectral sensitivity of fly photoreceptors. III. Dependence on the pupil mechanism in the blowfly<Emphasis Type="Italic"> Calliphora</Emphasis>

A wave optics model for the facet lens-rhabdomere system of fly eyes is used to analyze the dependence of the angular and spectral sensitivity of R1–6 photoreceptors on the pupil mechanism. This assembly of light-absorbing pigment granules in the soma interacts with the waveguide modes propagating in the rhabdomere. A fly rhabdomere carries two modes in the middle wavelength range and four modes at short wavelengths, depending on the rhabdomere diameter and the angle of the incident light flux. The extension of the mode to outside the rhabdomere strongly depends on wavelength, and this dependence plays a determinant role in the light control function of the pupil. The absorbance spectrum of the pigment in the pupil granules is severely depressed at short wavelengths by waveguide effects, resulting in a distinct blue peak. Accordingly, pupil closure suppresses the photoreceptors spectral sensitivity much more in the blue-green than in the UV. The pupil only narrows the angular sensitivity at short wavelengths. The geometrical size of the rhabdomere governs the angular sensitivity of fly photoreceptors in the dark-adapted state, but diffraction takes over in the fully light-adapted state.     

The Actomyosin Machinery Is Required for Drosophila Retinal Lumen Formation

Multicellular tubes consist of polarized cells wrapped around a central lumen and are essential structures underlying many developmental and physiological functions. In Drosophila compound eyes, each ommatidium forms a luminal matrix, the inter-rhabdomeral space, to shape and separate the key phototransduction organelles, the rhabdomeres, for proper visual perception. In an enhancer screen to define mechanisms of retina lumen formation, we identified Actin5C as a key molecule. Our results demonstrate that the disruption of lumen formation upon the reduction of Actin5C is not linked to any discernible defect in microvillus formation, the rhabdomere terminal web (RTW), or the overall morphogenesis and basal extension of the rhabdomere. Second, the failure of proper lumen formation is not the result of previously identified processes of retinal lumen formation: Prominin localization, expansion of the apical membrane, or secretion of the luminal matrix. Rather, the phenotype observed with Actin5C is phenocopied upon the decrease of the individual components of non-muscle myosin II (MyoII) and its upstream activators. In photoreceptor cells MyoII localizes to the base of the rhabdomeres, overlapping with the actin filaments of the RTW. Consistent with the well-established roll of actomyosin-mediated cellular contraction, reduction of MyoII results in reduced distance between apical membranes as measured by a decrease in lumen diameter. Together, our results indicate the actomyosin machinery coordinates with the localization of apical membrane components and the secretion of an extracellular matrix to overcome apical membrane adhesion to initiate and expand the retinal lumen.     

Evolutionary significance of fine structure of archiannelid eyes

Summary The structure of the ocelli of representatives of four of the five families of archiannelids (Polychaeta: Annelida) was studied by light and electron microscopy. The apparent photoreceptoral organelle in each species is an array of microvilli (rhabdomere). Cilia were observed in the eyes of only a couple of specimens in one species of archiannelid (Nerilla antennata). They were unassociated with the rhabdomeres; we regard them as adventitious. Support is given by this study to the theory that the photoreceptoral organelle of the ancestral annelid was a rhabdomere. Other features of the ocelli are described and illustrated.We acknowledge the support of a grant-in-aid of research (GM 10292) from the United States Public Health Service; the skillful transformation of our sketches into finished drawings by Phyllis Thompson; the assistance of Jean Brandenburger in the electron microscopy of villar particles; and the critical reading of the paper by Mrs. Brandenburger and Drs. Colin O. Hermans and Ralph I. Smith     

Regulation of water ingestion by the locust, Chortoicetes terminifera: the effect of injections into the haemolymph

Adults of the locust Chortoicetes terminifera which had been deprived of water for 24 h took larger 'meals' of water than insects which had been deprived for 2 h. Water or dilute solutions of NaCl injected into the kaemcoel reduced the amount of water ingested by 24-h, deprived locusts. Injections of more concentrated solutions of NaCl (0.5 m) or glycerol (1.0m) increased the water intake of 2-h deprived locusts. Water injections into 24-h deprived locusts did not reduce their responsiveness to sucrose and it is concluded that haemolymph osmotic pressure plays an important role in determining the specific responsiveness of C. terminifera to water. The time course of the effects of injection indicates that the effects of haemolymph osmotic pressure on water responsiveness are mediated neurally. Injections of water into 24-h deprived insects caused a marked reduction in the sizes of their meals of seedling wheat. It is suggested that the mechanisms responsible for the regulation of water intake might limit total intake when locusts have access only to fresh vegetation of high water content.     

Effect of short-term food deprivation on reproduction in female mice

CF-1 female mice were subjected to 24 or 48 h of food deprivation beginning when they were in estrus or diestrus, or when they were 2 or 12 days pregnant, or on Days 2 or 12 of lactation. Ovulation was delayed by a week or more when 48 h of food deprivation was initiated when the female was in diestrus; lesser delays occurred when food deprivation began in estrus. There was little effect of acute food deprivation on pregnancy. Most females deprived of food beginning on Day 2 of lactation ate their young, but females deprived on Day 12 of lactation rarely did so. These results are discussed in terms of the complexity of interacting factors that determine the degree to which each stage of the female's reproductive cycle is susceptible to disruption by acute food deprivation.     

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.