,JOURNAL OF NELJKORIOLOGY, VOI,. 8, NO. 6. PP. 537-548

Sensory Antenna1 Organization in an Ant and a Wasp CLAUDINE MASSON

and COLETTE STRAMBI

INTRODUCTION

The general anatomy of the brain of social Hymenoptera has been investigated by several authors (Viallanes, 1896; Jonescu, 1909; Sanchez, 1941; Vowles, 1955; Jawlowski, 1957; Goll, 1967; Bressac and Bitsch, 1969) but little attention has been devoted to the deutocerebrum (Pareto, 1972; Suzuki and Tateda, 1974; Suzuki, 1975a, 1975b; Masson, 1972,1973,1974). Data obtained on the cephalic ganglia of the wasp Polistes gallicus revealed histochemically different areas in the brain, especially the deutocerebrum (Strambi, 1974). Comparison with anatomical and electrophysiological data on the deutocerebrum of the ant Camponotus vagus (Masson, 1969,1972,1973, 1974), suggested the desirability of making a comparative histochemical study of the antenna1 lobe of these social insects. MATERIAL AND M E T H O D S Two social Hymenoptera were studied: the ant Camponotus vagus Scop. and the uasp Polistes gallicus L. Both species were reared in the laboratory under standard conditions (Stramhi, 1965). The central nervous structures were studied in the brains of workers which at least in the ant, represent the medial form (Masson, 1973). For histochemical purposes, the fresh tissues were dissected out, embedded in a medium for frozen tissues (OCT compound, Ames Laboratory), frozen in liquid nitrogen and then cut on a cryotome at -20°C in frontal or sagittal sections, 8-12 microns thick. Succinate dehydrogenase activity was detected by the method of Nachlas et al. using nitro-BT (in Gahe, 1968). Control sections were incubated in a solution without sodium succinate. Cytochrome oxidase activity was revealed by Burstone’s method (in Gabe, 1968); potassium cyacide was used as an inhibitor for control sections. The method of Arvy (in Gaht, 1968) was used to detect cholinesterase activity. Prefixation in cold neutral 10%formalin for 5 min was usually performed before incubation. The slides were incubated for 2.5 h a t 37°C in acetylthiocholine iodide or butyrylthiocholine iodide. Control sections were treated with eserine or tetraisopropylpyrophosphoramine (iso-OMPA).

537 0 1977 by John Wiley & Sons, Inc.

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For electron microscopy, small pieces of hrain were fixed for 40 min at 20°C in 2.5% glutaraldehyde in phosphate buffer, ph 7.4. They were then rinsed in the phosphate buffer and treated for 1.5 h a t 4°C in 2% OsO4 in the phosphate buffer. Thin sections were double stained with uranyl acetate and lead citrate. Electron micrographs were taken with a Siemens Elmiskop 1A. For electrophysiology, the stimulating equipment and recording systems were the same as those described by Masson (1973, 1974). A glass capillary microelectrode, generally filled with SM KCl solution, was used as recording electrode. After recordings, an electrical current of about lo-’ A was passed for 1 to I .5min though the electrode. The brain was then soaked with 204 ferrous chloride solution to mark the recording site; this point was locat,ed in serial paraffin sections hy light microscopy.

RESULTS

As in the proto and tritocerebrum, neuron somata and glial cells of the deutocerebrum were found mainly in peripheral locations. The deutocerebrum consists of two lobes: a mixed motorlsensory and a sensory one. In the ventral part a dense neuropile forms the dorsal lobe which usually has been considered a motor lobe controlling the antennal muscles. I t has however, been recently shown that some sensory afferent fibers together with motor fibers pass through this dorsal lobe (Pareto, 1972; Suzuki, 1975). The sensory lobe (also “lobus antennalis”, “antennal lobe”, “olfactory lobe” in literature) contains specific neuropile areas, the sensory glomeruli, in which primary sensory fibers from the two antennal sensory nerves terminate. Our data concern only the sensory lobe, but it should be noted that, in Polistes, some sensory afferent fibers seem t o run through the dorsal lobe which shows small neuropile spheres similar to the small glomeruli described by Pareto (1972) in Apis. Histochemistry In Hymenoptera, a characteristic of the sensory lobe is the peripheral arrangement of the glomeruli as seen in frontal section (Fig. 1). In serial sections, the sensory glomeruli were clustered in two groups (Figs. 1-7). A first curved group forms the anterior part of the deutocerebrum, this will be referred as sensory lobule 1. A second posterior one overlaps the distal part of the first group, referred to as sensory lobule 2. In parasagittal sections of the outer part of the deutocerebrum, the two groups of glomeruli appeared distinctly on 110th sides of the antennal sensori-motor nerve (Fig. 5). Although anatomical studies demonstrated the occurrence in both the a n t and the wasp of these two groups of sensory glomeruli, normal histological methods did not differentiate clearly the two clusters: The sensory glomeruli of both groups were of similar size and showed the same staining affinities (Fig. 1). However, using histoenzymological methods, important differences were revealed between the two groups. Succinate dehydrogenase activity was not uniform in the sensory lobe. The secondary sensory neurones enclosing the central neuropile reacted very weakly (Figs. 2, 4-6) and high magnification was necessary to reveal fine sparse granulations around the nuclei. The neuropile loosely surrounding the glomeruli was lightly colored. The glomeruli appeared as small distinct spheres in which succiriate

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Fig. 1. Frontal section of the sensory lobe of the deutocerebrum in Polistes gallieus. Although the two groups of glomeruli are anatomically distinct, their staining does not differ with the usual histological stainings. (Trichromic staining Gabe and Martoja Pierson) sl 1: sensory lobule 1; sl2: sensory lobule 2; f foregut (1OOX).

Fig. 2. Succinate dehydrogenase activity (frontal section; Polistes gallieus). In the sensory lobe, two groups of glomeruli are shown: the upper one (sl 1) has a stronger enzymic activity than the lower one (sl2); s.m.a.n. sensory-motor antenna1 nerve (1OOX).

dehydrogenase activity varied in intensity: Those of sensory lobule 1reacted strongly with Nachlas’s method, whereas the color was more discrete in those of sensory lobule 2. Sensory afferent coming from the antenna could be easily observed, especially in sensory lobule 1: sensory fibers surround the glomeruli’s periphery (Fig. 4). A comparison of Figures 2 and 6 shows that results for the wasp and ant were closely similar. It should be noted that succinate dehydrogenase and cytochrome oxidase activities have the same distribution. With cholinesterase, the enzyme activities are eserine sensitive. They seem to be related to acetylcholinesterase as demonstrated by controls using iso-OMPA as selective inhibitor and butyrylcholine as substrate. No activity could be de-

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Fig. 3. Acetylcholinesterase activity (frontal section; Polistes gallicus). The enzymic activity is more intense in the lower group of glomeruli (sl2) than in the upper one (loox).

Fig. 4. Succiriate dehydrogenase activity (parasagittal section; Polistes gallicus). Sensory antennal afferences (arrow) are running through sensory lobule 1and overlapping the sensory glomeruli. (1OOX).

Fig. 5. Succinate dehydrogenase activity (parasagittal section; Polistes gallicus). In parasagittal section of the outer part of the deutocerebrum, the sensory glomeruli appear clustered in two groups on both sides of the sensory motor antenna1 nerve (P: protocerebrum) (1OOX).

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Fig. 6. Succinate dehydrogenase activity (frontal section; Camporzotus uagus). In the sensory lobe of the ant, the glomeruli of sensory lobule 1appear more reactive than those of sensory lobule 2. C.P.: corpora pedunculata; D: deutocerebrum (lOOX).

Fig. 7. Acetycholinesterase activity (frontal section; C a m p m o t u s uagus). As in Fig. 3, the glomeruli of sensory lobule 2 are richer in acetylcholinesterase activity than those of sensory lobule l(160X).

tected in the cells. The neuropile surrounding the glomeruli stained weakly. The two groups of glomeruli reacted differently: in sensory lobule 1, acetylcholinesterase activity was weak in the glomeruli and stronger in sensory lobule 2, especially in the central area of the glomeruli (Figs. 3 and 7). I t should be stressed that a part of the afferents of the sensori-motor antenna1 nerve in wasp, was rich in acetylcholinesterase (Fig. 3 ) . As above, the data obtained for the wasp (Fig. 3) and the ant (Fig. 7) were similar.

Ultrastructure

At the ultrastructural level, the glomeruli of each sensory lobule were different. Numerous, large mitochondria appeared within the fibers a t the periphery of the glomeruli in sensory lobule 1 (Fig. 8). In addition to the considerable development of the chondriome, many lysosomes occurred in the same area. By contrast, in sensory lobule 2 the peripheral fibers of the glomeruli contained markedly fewer mitochondria and lysosomes (Fig. 9).

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Fig. 8. Photomicrograph of a small part of a glomerulus in sensory lobule 1. Numerous mitochondria and lysosomes are present in the fibers a t the periphery of the glomeruli Black line indicates the outer limit of the glomerulus. sl 1: sensory lobule 1; 1: lysosomes; m: mitochondria (4000X).

Fig. 9. Photomicrograph of an area of the glomerulus in sensory lobule 2. There are less mitochondria in the outer part of the glomerulus. Black line indicates the outer limit of the glomerulus. sl2: sensory lobule 2; m: mitochondria (4000X).

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Electrophysiology Olfactory and mechanical sensilla of the ipsilateral antenna were stimulated, while responding single units were localized by recording in the sensory lobe of deutocerebrum. The results corresponded well with the structural analysis (Masson, 1973). Odorous substances used were monitored by an air-flow olfactometer (Masson, 1973; Masson and Friggi, 1974). The antennae were stimulated with several odorous air current without considering the relative quantitative values of the stimuli. Our purpose was to explore the olfactory sensory projections, not to study the coding of the olfactory information in the central nervous system. Mechanical stimuli consisted either by touching the long tactile antennal sensilla with a hair or lightly displacing hair plates of the main antennal joints (Masson, 1973) with the aid of a micromanipulator. The results show that the different projection sites of each stimulus modality determine two well-delimited areas in the sensory antennal lobe (Fig. 10) corroborating the morphological and histochemical observations (Fig. 11). DISCUSSION

Our combined anatomical, histochemical, and electrophysiological studies provide evidence for subdivision of centers within the sensory lobe of the deutocerebrum in both wasp and ant. Several authors have dealt with deutocerebral anatomy and deutocerebral pathways in insects (Viallanes, 1887; Kenyon, 1896; Jonescu, 1909; Jawlowski, 1958; Prigent, 1966; Goll, 1967; Boeckh et al., 1974; Roeckh, 1974,1975; Pareto, 1972; Masson, 1972,1973; Weiss, 1974; Suzuki, 1975), but arrangement of the sensory glomeruli in distinct clusters has seldom been reported. In the ant such a differentiation has been previously suggested by anatomical and electrophysiological studies (Masson, 1973,1974);histochemical results have also indicated this in the wasp (Strambi, 1974). In other insects Prigent (1966) established that sensory glomeruli within the sensory lobe of Periplaneta americana are arranged in two distinct groups, one anterior and one posterior, with which our observations agree. Studies on the localization of cholinesterases in the central nervous system of insects have been carried out by several authors (Iyatomi and Kaneshina, 1958; Wigglesworth, 1958; Ramade, 1965; Smith and Treherne, 1965; Landolt and Sandri, 1966; Frontali, Piazza, and Scopelliti, 1971; Hess, 1972). Using different methods and different inhibitors Wigglesworth (1958) demonstrated in the brain and in the thoracic and abdominal ganglia of Rhodnius prolixus the presence of a specific acetylcholinesterase localized in the neuropile and of an ali-esterase localized in the perineurium and between ganglion cells. In the terminal ganglion of Periplaneta americana, Smith and Treherne (1965) distinguished a specific acetylcholinesterase localized mainly on the membranes of certain axons and axon terminals within the neuropile. Landolt and Sandri (1966) found acetylcholinesterase associated with synaptic areas of axonal membranes in the corpora pedunculata of Formica lugubris'; they did not mention the presence of ali-esterase.

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Fig. 10. Map of the projections to the sensory deutocerebrum for chemical and mechanical stimulations of the antenna of Camponotus uagus.

Our histochemical preparations failed to reveal other esterases than acetylcholinesterase and this result is in agreement with those obtained in other insects, indicating that the brain undoubtedly contains less ali-esterase than the nerve cord (Frontali, Piazza, and Scopelliti, 1971; Hess, 1972). It is still uncertain whether histochemical staining of acetylcholinesterase does, indeed, sites of cholinergic transmission (Gerschenfeld, 1973). As regards localization of acetylcholinesterase in the deutocerebrum of the insects, different results have been reported: thus Frontali, Piazza, and Scopelliti (1971) and Hess (1972) noted a weak reaction in the glomeruli of the antennal lobe of Periplaneta americana, whereas Ramade (1965) found strong reactivity in the glomeruli of Musca domestica. In Polistes gallicus and Camponotus uagus, two different groups of glomeruli have been revealed: the glomeruli clustering within sensory lobule 1were poor in acetylcholinesterase while those of sensory lobule 2 had a strong enzymic activi ty. Besides acetylcholine, using the fluorescence histochemical method of Falck and Hillarp, insect brains have been also shown to contain biogenic amines which possibly act as neurotransmitters (Frontali and Norberg, 1966; Frontali, 1968; Plotnikova and Govyrin, 1966; Ramade and L’Hermite, 1971; Klemm and Axelsson, 1973; Musko, Nagy, and Deak, 1973; Schurmann and Klemm, 1973; Klemm and Schneider, 1975). Usually the antennal lobe did not exhibit a strong fluorescence. Nevertheless, in Periplaneta americana the glomeruli appeared

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supant $ens nerve

\

545

inf.ant,sens.nerve

neuroni Fig. 11. Drawing of the sensory lobe of the deutocerebrum to show the general organization in Cumponotus uugus. Abbreviations are as follows: mot. nerve, SC.~.:motor nerve, scapus-pedicellus; mot. nerve, h-sc: motor nerve, head-scapus; sup. ant. sens. nerve: superior antennal sensory nerve; inf. ant. sens. nerve: inferior antennal sensory nerve; primary sens. fibers: primary sensory fibers.

to be surrounded and crossed by a network of fluorescent fibers (Frontali, 1968). In the antennal lobe of Schistocerca gregaria, fibers which normally did not contain fluorogenic amines selectively take up 6-HT; these fibers belong exclusively to an intradeutocerebral system of interneurons (Klemm and Schneider, 1975). Nevertheless, none of these last authors mentioned the presence of two types of glomeruli in the antennal lobe. The distribution of biogenic amines in the brains of wasps and ants is not yet known, and it is thus difficult to formulate an hypothesis concerning neurotransmitters in the two groups of glomeruli occurring in the deutocerebrum of Polistes gallicus and of Camponotus vagus. With regard to the enzymes catalyzing the transfer of hydrogen, succinate dehydrogenase and cytochrome oxidase, histochemical data on insect brains are, to our knowledge, not yet available. A t the cellular level, these enzymic activities seemed to be related to the mitochondria (Arvy, 1958). As seen above, a strong correlation existed between succinate dehydrogenase and cytochrome oxidase activities and the abundance of mitochondria in the glomeruli of sensory lobule 1. Such a correlation had been previously established in the lamina ganglionaris and in the medulla of Polistes (Strambi, 1974). Some authors have noted that the area around the glomeruli is very rich in fiber agglomerations and synaptic regions (Schurmann and Wechsler, 1970; Pareto, 1972; Masson 1972,1973). Furthermore, after removal

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of the antennal flagellum, degenerating nervous processes were found in the glomeruli of the deutocerebrum; these processes were more numerous in the outer part of the glomeruli (Boeckh, Sandri, and Akert, 1970). Thus, the preferential distribution of mitochondria a t the periphery of the glomeruli emphasizes the physiological importance of this area. Our findings in the wasp and the ant show an inverse relationship between the distribution of acetylcholinesterase and succinate dehydrogenase (or cytochrome oxidase) in the two groups of sensory glomeruli of the deutocerebrum. This result suggested at least some differences in the metabolic activity of the two sensory lobules. It should be stressed that Campa and Engel (1971), in a study of the anterior horn neurones of the cat spinal cord, have found some histochemical and functional correlations. Anterior horn neurones capable of higher firing frequencies are richer in mitochondria oxidative enzymic activity as shown by succinate dehydrogenase activity; those firing a t lower frequencies are richer in phosphorylase activity and glycogen content and are apparently better equipped for anaerobic glycolysis. The electrophysiological data obtained in the ant suggest that the projections from chemical and mechanical stimulation of the antenna had specific regional localization in the sensory lobe of the deutocerebrum. This implies the coexistence, more or less overlapping, of a “chemical sensory center” and of a “mechanical sensory center” within the sensory lobe (Masson, 1973, 1974), an hypothesis supported by our histochemical and ultrastructural observation. Electrophysiological studies in Periplaneta americana, have provided evidence for the occurrence of different levels in the coding of sensory input (Boeckh et al. 1974,1975; Waldow, 1975). In vertebrates, degeneration studies of olfactory receptor projections in the rabbit (Land 1970, 1973) shows that they are localized projection of olfactory nerves to olfactory bulb, and that the differing glomerular patterns indicate different levels of functional organization in the olfactory pathway, these work also suggest the presence of inter- and intraglomerular patterns of synaptic input. In a recent paper, Land (1974), using an autoradiographic analysis of olfactory receptor projections in the rabbit, provide additional support for the concept that the olfactory receptor input to the glomerular layer of the olfactory bulb is organized a t several anatomical and functional levels (Shepherd, 1972). In insects, the antennal sensory lobe appears to be the first level for the integration of sensory information, whereas the corpora pedunculata are probably the main second-order antennal processing center (Horridge, 1965; Weiss, 1974). Although we are not yet able to ascertain the functional significance of our observations, they do provide evidence for a subdivision of centers within the antennal lobe. REFERENCES ARVY,L. (1958). Les techniques actuelles d’histoenzymologie. Biol. M e d . 46,47 p. 477. BOECKH,J., ERNST,K., SASS, H., and WALDOW,U. (1974). Coding of odor quality in the insect olfactory pathway. Proceedings of the Fifth Olfaction and Taste, D. A. Denton and J. P. Coghlan (Eds.) Academic Press, New York.

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Sensory antennal organization in an ant and a wasp.

,JOURNAL OF NELJKORIOLOGY, VOI,. 8, NO. 6. PP. 537-548 Sensory Antenna1 Organization in an Ant and a Wasp CLAUDINE MASSON and COLETTE STRAMBI INTRO...
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