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Termination profiles of photoreceptor cells in larval eye of the swallowtail butterfly
Abstract
Profiles of the axonal endings of seven retinular cells (R1-7) from each of six stemmata (I-VI) of the butterfly Papilio xuthus were examined. Their axons enter the brain anteroventrally and project dorsally along the brain's lateral surface before entering the optic neuropil. Larval optic neuropil has two distinct areas, a (distal) lamina and a (proximal) medulla, connected by a chiasma. Intracellular administration of cobalt shows that distal retinular cells (R1-3 of stemmata I-IV, R1-3 and R6 of stemmata V and VI) terminate as short axons with plug or toothbrush-like endings in the lamina. Proximal retinular cells (R4-7 of stemmata I-IV, R4, R5 and R7 of stemmata V and VI) terminate as long axons in the chiasma or in the medulla. The long axons have fine branches in the lamina, chiasma and medulla. The two proximal cells (R5 and R7) are distinguished by their deeper endings and longer branches. The terminals of photoreceptors correspond to their photoreceptive properties and provide further evidence for the functional specialization of the photoreceptors.
... The photoreceptor cells in each stemma are spectrally differentiated into two or three types (Ichikawa and Tateda, 1980). They project axons into the lamina and medulla (Ichikawa and Tateda, 1984;Toh and Iwasaki, 1982). The close similarity in basic structure of the visual systems between the larvae with stemmata and the adults with compound eyes makes the larval visual system a simple model for insect colour vision. ...
... A microelectrode filled with lmoll" 1 potassium acetate was inserted into the somata region of the medulla neurone between two imaginal disks (Ichikawa and Tateda, 1984). An indifferent electrode was placed in the saline bath. ...
... The other neurones were characterized by phasic excitatory responses evoked at both the onset and the offset (D) or only the offset (E) of the stimulus. Since the somata of the medulla neurones are distant from their dendrites and axons, which are located in the neuropile (a synaptic region) (Ichikawa and Tateda, 1984), these different features of the electrical activity recorded from somata may reflect different mechanisms of signal generation and different spatial properties for signal propagation from the generating sites, based on different morphology. Similar characteristic electrical activities found in another group of medulla neurones have been described previously (Ichikawa, 1986). ...
Spatial and chromatic properties of 25 types of medulla neurones which integrate input from different optical units (stemmata) of the larval eye in the swallowtail butterfly were examined by illuminating individual stemmata with chromatic stimuli. Eleven neurones received different types of colour (opponent) input from a few stemmata; thus, the receptive fields are spectrally heterogeneous. The stemmata dominating these complex neurones were usually located in the frontal (central) region of the eye. Seven neurones showed a relatively homo-geneous spectral profile over the receptive field by receiving similar spectral input from two or three stemmata which were usually located in the dorsolateral (peripheral) region of the eye. Three of these simple units showed tonic or phasic responses. The remaining seven were also spectrally simple neurones but with larger receptive fields covering four to all six stemmata. Some units showed a spatial summation of responses or a spatial antagonism between central and peripheral or dorsal and ventral regions of the eye.
... Butterfly larvae have an eye consisting of a small number of receptive units (six stemmata) with a large diameter, so we can stimulate individual units independently (Ichikawa, 1986). Although the number of optical units is greatly reduced, the larval visual system appears to be constructed according to the same architectural principles as the adult visual system with compound eyes (Ichikawa and Tateda, 1984;Toh and Iwasaki, 1982). These features make the larval visual system an interesting model for insect vision. ...
... The tip of a glass pipette containing 1 % Pronase was placed on the brain for 20-30 s to facilitate penetration by a glass pipette microelectrode. The microelectrode, filled with l m o l P 1 potassium acetate (30-50 MQ), was inserted into the somata region of the medulla neurones between two imaginal discs (Ichikawa and Tateda, 1984). An indifferent electrode was placed in the saline bath. ...
Summary The influence of interactions between the antagonistic centre and surround areas of receptive fields on the electrical activities of medulla neurones was examined in the larval swallowtail butterfly Papilio xuthus. Weak signals from the surround had a significant depressive effect on the maintained discharge, which increased for on-centre cells or decreased for off-centre cells in response to illumination of the centre. Moderation of the maintained discharge suppressed saturation of the response and extended the graded response range of the neurones. Surround illumination also reduced irregular fluctuations in the membrane potentials and variability in the discharge rate of impulses. The results indicate that the spatial inhibitory mechanism is important for the larval visual system in order to increase the efficiency of signal processing.
... This visual system, composed of 6 stemmata contains three spectrally distinct opsins (UV, blue and green). The output axons of photoreceptors project in a spectral specific manner to two different underlying optic neuropils (green receptors project to the lamina and blue/UV receptors project to the medulla) (Ichikawa and Tateda 1984). These different channels allows for color vision and promote color opponency in butterfly larvae (Ichikawa 1990). ...
Fireflies are bioluminescent beetles and members of the holometabolous clade. As holometabola, fireflies interact with their environment during two stages: larva and adult. I studied firefly stemmata, Photuris genus, with the aim of understanding their ecological utility by identifying structural and functional features of the eye. As a first step toward this goal, I used microscopy to characterize the architecture of firefly stemmata. I concluded that Photuris eyes were a type of fusion-stemmata, evidenced by a bi-lobed organization. Each eye contained 88 photoreceptors that contributed dense interlocking-microvilli forming a fused-rhabdom. In the next section, I tested whether stemmata regulated photo-dependent activity. I found that larvae were more active during nocturnal conditions, but unexpectedly, these behavioral patterns were not sufficiently explained by stemmata. Upon excision of the optic nerve, larvae maintained their activity preference to dark conditions, but this behavior was abolished upon removal of their head, suggesting an extraocular mechanism. In the final section, I demonstrated that stemmata were most sensitive to light in the blue/green part of the visible spectrum. Furthermore, using a chromatic adaptation assay, I showed that stemmata photoreceptors were consistent with having more than one spectrally distinct opsin. While a specific behavioral role for the larval eyes remain inconclusive, the macro- and ultrastructural results suggested the eyes have more sophisticated attributes than a simple light detector. This work has provided the framework upon which specific structure to function questions can be explored to advance our understanding of the Photuris firefly larval visual system.
... (b) Description of growth in individual brain structures(i) Optic lobesThe larval optic lobes anatomy showed a finger-like structure[16] (figure 4a). These larval optic lobes were still faintly Surface reconstructions of brain structures underlying subsequent volumetric measurements. ...
Diapause is an important escape mechanism from seasonal stress in many insects. A certain minimum amount of time in diapause is generally needed in order for it to terminate. The mechanisms of time-keeping in diapause are poorly understood, but it can be hypothesized that a well-developed neural system is required. However, since neural tissue is metabolically costly to maintain there might exist conflicting selective pressures on overall brain development during diapause, on one hand to save energy and on the other hand to provide reliable information processing during diapause. We performed the first ever investigation of neural development during diapause and non-diapause (direct) development in pupae of the butterfly Pieris napi from a population whose diapause duration is known. The brain grew in size similarly in pupae of both pathways up to three days after pupation, when development in the diapause brain was arrested. While development in the brain of direct pupae continued steadily after this point, no further development occurred during diapause until temperatures increased far after diapause termination. Interestingly, sensory structures related to vision were remarkably well developed in pupae from both pathways, in contrast to neuropils related to olfaction, which only developed in direct pupae. The results suggest that a well-developed visual system might be important for normal diapause development.
... Furthermore, there have been only a few studies on the projection of retinular axons to the brain and the spectral sensitivities of caterpillar eyes (Toh and Sagara 1982, Ichikawa and Tateda 1984). The aims of present study were to determine the structure and spectral sensitivity of the stemmata in the larva of the moth Trabala vishnou Lefebur. ...
The Caterpillar of the moth, Trabala vishnou Lefebur, has 6 stemmata on each side of its head. The diameter of the lens of each stemma varies. However, the basic structure of a stemma is similar to an ommatidium of a compound eye. Each stemma has a corneal lens, corneagenous cells, a crystalline cone, and retinular cells. The 7 retinular cells in each stemma are organized in 2 tiers, distal and proximal. Stemmata II and V both have 4 distal and 3 proximal retinular cells, while the other stemmata have 3 distal and 4 proximal cells in each stemma. The distal rhabdom is star-shaped radially around the central axis of the stemma, and the proximal one is irregular. The proximal part of each retinular cell narrows forming an axon. The 42 axons from the ipsilateral stemmata join together to form an optic nerve which directly enters into the brain. Axons I-IV project anterodorsally to the optic neuropile of the brain, while axons V and VI project posteroventrally. From the spectral sensitivities of stemmata, it is evident that stemmata I-IV have UV, blue, and green receptors, whereas stemmata V and VI have only blue and green units without UV receptors.
Through a system of neurons and ganglia, the nervous system coordinates physiological events by a sequence of electrical and chemical impulses. The central nervous system consists of the brain as a complex of ganglia, and the ventral nerve cord that primitively extends the length of the abdominal segments. Extending from the entire CNS are peripheral nerves that innervate other tissues and sensory receptors. A visceral nervous system innervates the gut, heart, and endocrine glands. Sensory transduction translates environmental stimuli into internal electrical energy, performed by sensory cells on the integument such as the compound eyes. The insect nervous system has been the main target of control measures.
Insects use both the endocrine and the nervous systems for information transfer between their cells, with each system having its own advantages and constraints. Biological information transmitted by the electrical signals of the nervous system provides a much more rapid means for coordinating cellular events than that transmitted by hormones or chemical messengers. This chapter examines aspects of nervous transmission in insects. Nerve cells, or neurons, are the cellular building blocks that make up the nervous system. They are capable of integrating information, undergoing excitation, and transmitting the information by electrical and short-range chemical signaling. Maintenance of electrical potential in dendrites of neurons help in neural transmission. A number of different neurotransmitters and neuromodulators are involved in nervous transmission at both invertebrate and vertebrate synapses. The synaptic connection of a single neuron with two or more neurons, or with a muscle cell innervated by multiple motor neurons that includes neurotransmitters capable of exciting or inhibiting at the synapse, allows the nervous system to integrate nervous transmission in a much more complex fashion. The insect central nervous system consists of the brain and ventral nerve cord. The system comprises the individual neurons that are associated in functional groupings that evolved together with a reorganization of the insect body from its primitive annelid-like ancestor. The peripheral nervous systeminvolves all the nerves that radiate from the central nervous system. These include the nerves that innervate muscles, stretch receptors that may serve as proprioreceptors, innervations of the reproductive system and spiracles, and the various sensory receptors. Another part of the insect nervous system, termed visceral nervous system, innervates the gut, heart, and endocrine glands and forms a network of peripheral ganglia that is associated with digestive processes.
Physiological Systems in Insects discusses the roles of molecular biology, neuroendocrinology, biochemistry, and genetics in our understanding of insects. All chapters in the new edition are updated, with major revisions to those covering swiftly evolving areas like endocrine, developmental, behavioral, and nervous systems. The new edition includes the latest details from the literature on hormone receptors, behavioral genetics, insect genomics, neural integration, and much more. Organized according to insect physiological functions, this book is fully updated with the latest and foundational research that has influenced understanding of the patterns and processes of insects and is a valuable addition to the collection of any researcher or student working with insects. There are about 10 quintillion insects in the world divided into more than one million known species, and some scientists believe there may be more than 30 million species. As the largest living group on earth, insects can provide us with insight into adaptation, evolution, and survival. The internationally respected third edition of Marc Klowden's standard reference for entomologists and researchers and textbook for insect physiology courses provides the most comprehensive analysis of the systems that make insects important contributors to our environment.
There are about 10 quintillion insects in the world divided into more than 1 million known species, and some scientists believe there may be more than 30 million species. As the largest living group on earth, insects can provide us with insight into adaptation, evolution, and survival. The internationally respected 3e of Marc Klowden's standard reference for entomologists and researchers and textbook for insect physiology courses provides the most comprehensive analysis of the systems that make insects important contributors to our environment. Physiological Systems in Insects discusses the role of insect molecular biology, neuroendocrinology, biochemistry, and genetics in our understanding of insects. All chapters in the new edition are revised, and major revision in fast-moving areas includes the Endocrine, Developmental, Behavioral, and Nervous System chapters. This new edition includes the latest details from the literature on hormone receptors, behavioral genetics, insect genomics, neural integration, and much more. Organized according to insect physiological functions, this book is fully updated with the latest and foundational research that has influenced understanding of the patterns and processes of insects and is a valuable addition to the collection of any researcher or student working with insects. Third edition has been updated with new information in almost every chapter and new figures Includes an extensive up-to-date bibliography in each chapter for readers who need to pursue topics in more depth. Provides a glossary of common entomological and physiological terms.
As the largest living group on earth, insects can provide us with insight into adaptation, evolution, and survival. The 2nd edition of this standard text for insect physiology courses and entomologists provides the most comprehensive analysis of the systems that make insects important contributors to our environment. Physiological Systems in Insects discusses the role of insect molecular biology, nueroendocrinology, biochemistry, and genetics in our understanding of insects. Organized according to insect physiological functions, this book is fully updated with the latest and foundational research that has influenced understanding of the patterns and processes of insects. * Full update of a widely used text for students and researchers in entomology and zoology * Includes recent research that uses molecular techniques to uncover physiological mechanisms * Includes a glossary of physiological terms * New, extended section on locomotive systems * Provides abundant figures derived from scientific reports.
1. Temporal and spatial aspects of postembryonic optic lobe development in a Lepidopteran,Danaus plexippus plexippus L., were analyzed using serial section reconstructions and H(3)-thymidine radioautography to display loci of cell production and progressive movements of populations of cells. 2. Optic lobe development begins early in larval life and is continuous without perceptible fluctuations corresponding to molting. The production of new cells begins during the first larval stages and is completed within a few days after pupation. 3. Development of adult optic centers appears to be independent of the larval optic center and also of adult eye development which does not get underway until pupation. At pupation the larval stemmata migrate toward the brain along the stemmatal nerve which persists and later serves as the framework by which ommatidial neurones reach the brain. 4. Ganglion cells of the adult optic lobe are produced by two coiled rod-like aggregates of neuroblasts, the inner and outer optic lobe anlagen, which lie lateral to the protocerebrum and are already present in the brain of the newly hatched larva. Neuroblasts of the anlagen divide both symetrically to produce more neuroblasts and asymmetrically to yield one neuroblast and one smaller cell, the ganglion-mother cell. Subsequent ganglion-mother cell divisions produce the new ganglion cells which are continuously displaced from the anlage by additional cells. Following pupation mitotic activity in the anlagen diminishes and neuroblasts degenerate. By the fourth day after pupation the anlagen have disappeared. 5. Fiber differentiation begins within a few days of cell formation. Fibers travel in bundles usually toward the center of the coiled anlagen where they form the neuropile masses. With contributions from a growing population of ganglion cells, fibermasses grow rapidly in size and complexity. 6. The geometric arrangement of anlagen, cortices, and neuropile is dynamic and interdependent. Progressive changes in anlagen configuration result from the combined effects of an increasing neuroblast population, growing optic cortices, and expanding fibermasses between the arms of the anlagen. In turn, the cortices and fibermasses which follow anlagen contours also change form. The complex of these parts, initially small and coiled, gradually enlarges and uncoils until at the time of anlagen degeneration the three optic fibermasses and their cortices are in approximately their final arrangement. 7. The outer anlage forms cells of the lamina cortex at its lateral rim and cells of the medulla at its medial rim. Cells of the lobula cortex are produced by strands of inner anlage neuroblasts extending laterally between the arms of the coiled outer anlage. 8. Cells of the medulla cortex are first seen during the second larval instar and several days later the medulla fibermass is discernible. Cortex and fibermass lie medial to the outer anlage which is moved progressively more laterally as more cells are produced. Cells labelled with H(3)-Td R at the beginning of the third instar become the tangential cells of the adult optic lobe. Those labelled at the fourth and fith stages occupy positions near the tangential cells, and those labelled at pupation ultimately lie at the lateral edge of the cortex. 9. Production of the lamina cortex begins later and procedes more slowly. Cells here are first apparent during the fourth instar and form a cellular cap covering the lateral part of the optic lobe. Labelling studies show that the earliest formed cells finally occupy the most posterior region of the lamina cortex. The lamina fibermass is first seen in the mid-fifth instar brain. 10. For most of larval life the lobula cortex forms a plug of cells just inside the lamina. While the anlage remains coiled, the first-formed cells are at the center of the plug, but ultimately they lie at the most medial part of the cortex. Production of lobula cells begins during the third instar and by the mid-fourth instar the lobula neuropile can be seen medial to them. 11. As a result of these studies with H(3)-Td R injection and fixation after varying intervals it has been possible to estimate the age of cells at a particular developmental stage. Because this material offers an organized arrangement of cells of a wide range of identifiable ages and levels of maturation within a single individual, it provides an excellent model for the study of progressive neurone differentiation.
Passage of cobalt or nickel ions through axons to nerve cell branches can be achieved by introducing the salt solutions (such as acetate, chloride, nitrate, or bromide) into cut ganglia or their connectives (see Chap. 19). Distal portions of nerve cells are resolved after silver intensification. Appropriate conditions, such as low temperature, low salt concentrations (in Diptera), or high concentrations (in Orthoptera), reveal contiguous interneurons that impinge on primary-filled elements. In Dipterous insects, this method has been used to resolve the entire population of horizontal and vertical motion-sensitive neurons whose terminals are presynaptic onto a set of descending interneurons that happen to be particularly receptive to cobalt ion influx (Strausfeld and Obermayer, 1976). Comparisons between the shapes of such “trans-synaptically” filled elements, and identical neurons resolved by Procion yellow iontophoresis (Hausen, 1976a) have shown that cobalt ions pass to all parts of the neuron. Extended periods of Co2+ uptake may even resolve up to three consecutive sets of nerve cells (Fig. 18–1D).
1. Cellular morphogenesis during postembryonic brain development in Danaus plexippus plexippus L. was examined using histological techniques including radioautography. 2. The production of new neurones is continuous throughout larval and pupal stages and shows no fluctuations corresponding to ecdysis. Glial cell production, on the other hand, occurs at the time of molting. 3. New ganglion cells are formed by the division of neuroblasts found in aggregates or isolated among larval ganglion cells. Asymmetrical neuroblast divisions yield one neuroblast and one ganglion-mother cell which then divides at least once to form the new ganglion cells. Such divisions begin earlier in Danaus than in other investigated Lepidoptera. Symmetrical divisions yielding two neuroblasts also occur, but only among aggregated neuroblasts. 4. Radioautographs of brains fixed at progressive intervals after Tritiated Thymidine (H3TdR) injection have permitted description of the basic pattern by which cells of the adult brain cortex are laid out and progressive changes in the relationship of new ganglion cells derived from a single neuroblast. Ganglion-mother cells are deposited between the neuroblast and the neuropile, thus forming a row of cells which move the neuroblast progressively farther from the neuropile. New ganglion cells produced by ganglion-mother cell mitoses, which usually are oriented at 45° angles to the neuropile, expand the cell cluster. Differentiating fibers of these cells are apparent within a few days of their production and seem to enter the neuropile in one bundle. Later with increased neuropile volume and further cell differentiation the cells are no longer clumped and thus are not recognizable as offspring of a single neuroblast. 5. Neuroblasts found scattered among the larval ganglion cells arise from cells near the neuropile. These cells, at first indistinguishable from their neighbors, gradually assume the size and ready stainability of neuroblasts and subsequently divide according to the pattern described above. 6. Scattered neuroblasts degenerate beginning shortly after pupation and have completely disappeared by the end of the fourth day. 7. Except in the developing optic lobe, glial cell numbers increase through the proliferation of already existing glial cells. All glial cells show H3TdR uptake during a 12 hour period surrounding each larval-larval molt and for a somewhat longer period after pupation. However, in the larval stages mitotic figures were seen only among glial I, II, and IV. Glial I cells divide through the entire last larval stage and for two days following pupation. Large irregular mitoses seen among glial III cells at pupation indicate that these cells are probably polyploid. 8. In the newly forming adult optic lobe glial II, III, and IV cells appear to develop from preganglion cells or cells indistinguishable from them. These cells gradually stain more and more darkly, segregate into the normal glial positions, and subsequently divide in accord with other glial cells. 9. At the end of the fifth instar the perineurium (glial I cells), which begins to thicken during the third larval instar, is multilayered and contains many vacuolar cells. Just prior to pupation the neurilemma begins to disintegrate and during the next five days all but the cells closest to the brain disappear. Hemocytes are seen to engulf portions of the disintegrating neurilemma and already degenerating perineurial cells, but do not seem to engulf live cells. The glial I cells remaining adjacent to the brain secrete a new neurilemma. 10. There is no evidence for mass destruction of larval ganglion cells by either autolysis or phagocytosis, and only in the antennal center is there evidence of degeneration of larval cells (Nordlander and Edwards, in press).
The structure of optic cartridges in the frontal part of the lamina ganglionaris (the outermost synaptic region of the visual system of insects) has been analysed from selective and reduced silver stained preparations. The results, obtained from studies on five different species of Diptera, confirm that six retinula cells, together situated in a single ommatidium, project to six optic cartridges in a manner no different from that described by Braitenberg (1967) from Musca domestica. Each optic cartridge contains five first order interneurons (monopolar cells) which project together to a single column in the second synaptic region, the medulla. The dendritic arrangement of two of these neurons (L1 and L2) indicates that they must make contact with all six retinula cell terminals of a cartridge (R1-R6). Two others (L3 and L5) have processes that reach to only some of the retinula cell endings. A fifth form of monopolar cell (L4) sometimes has an arrangement of processes which could establish contact with all six retinula cells: other cells of the same type may contact only a proportion of them. This neuron (L4) also has an arrangement of collaterals such as to allow lateral interaction between neigbouring optic cartridges. The processes of the other four monopolar cells (L1, L2, L3 and L5) are usually contained within a single cartridge. In addition to these elements there is a pair of receptor prolongations (the long visual fibres, R7 and R8) that bypasses all other elements of a cartridge, including the receptor terminals R1-R6, and finally terminates in the medulla. Four types of neurons, which are derived from perikarya lying just beneath or just above the second synaptic region, send fibres across the first optic chiasma to the lamina. Like all the other interneuronal elements of cartridges the terminals of these so-called "centrifugal" cells have characteristic topographical relationships with the cyclic arrangement of retinula cell terminals. Apart from the above mentioned neurons there is also a system of tangential fibres whose processes invade single cartridges but which together could provide a substrate for relaying information to the medulla derived from aggregates of cartridges. Optic cartridges contain at least 15 neural elements other than retinula cells. This complex structure is discussed with respect to the receptor physiology, as it is known from electrophysiological and behavioural experiments. The arrangements of neurons in cartridges is tentatively interpreted as a means of providing at least 6 separate channels of information to the medulla, four of which may serve special functions such as relaying color coded information or information about the angle of polarised light at high light intensities.