Plasticity of Olfactory-Guided Behaviour and Its Neurobiological Basis: Lessons from Moths and Locusts

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DOI: 10.1111/j.1570-7458.2006.00516.x Blackwell Publishing Ltd MINI REVIEW Plasticity of olfactory-guided behaviour and its neurobiological basis: lessons from moths and locusts

Sylvia Anton1,2*, Marie-Cécile Dufour2 & Christophe Gadenne1,2 1INRA, UMR 1272 Physiologie de l’Insecte: Signalisation et Communication, Centre de Recherches de Versailles, route de Saint-Cyr, Bat A, 78026 Versailles cedex, France, 2INRA, UMR 1065 Santé Végétale, Centre de Recherche de Bordeaux, BP 81, F-33883 Villenave d’Ornon cedex, France Accepted: 24 November 2006

Key words: Lepidoptera, Orthoptera, olfaction, intracellular recordings, wind tunnel, juvenile hormone, mating, maturation, reproduction, sex pheromone, plant odour

Abstract The sense of smell plays an important role in guiding the behaviour of many animals including insects. The attractiveness of a volatile is not only dependent on the nature of the chemical, but might change with the physiological status (e.g., age/hormone or mating status) or environmental conditions (e.g., photoperiod or temperature) of the individual. Here we summarize our studies focused on the plasticity of olfactory-guided behaviour and its neurobiological basis linked with the physiological status in Lepidoptera and migratory locusts. In moths and locusts, age and juvenile hormone changed the behavioural responses to pheromones. In moths, mating had an effect on pheromone responses in males and plant odour responses in females. In all cases of behavioural plasticity studied, we found changes in the sensitivity of olfactory interneurons in the antennal lobe, whereas the peripheral system does not seem to show any plasticity in that context. Changes in the central nervous system were slow under the inﬂuence of juvenile hormone (days) or fast after mating (minutes). The olfactory system seems thus to adapt to the physiological or environmental situation of an animal to avoid a waste of energy. We discuss possible mechanisms underlying the observed plasticity.

physiologically ready to oviposit. Moreover, females of Introduction multivoltine moth species have to face a changing plant Plasticity of olfactory-guided behaviour odour pattern throughout the seasons: either they adapt Most animals, including insects, use odours in different their olfactory system to the changing host-plant odours behavioural contexts, e.g., to find a mating partner, food or they have developed a broadly tuned olfactory system sources, a habitat, or oviposition sites. In order to successfully that allows females of the different generations to detect reproduce, insects need to respond to biologically active and process plant odours that could be present throughout chemical stimuli at the right moment. For example, a male the year. Environmental factors, the physiological state, moth’s ability to detect sex pheromones should coincide and/or previous experience of the insect might therefore with the development of its reproductive organs and the influence its behaviour. Evidence is accumulating that presence of females in the field. Similarly, females should insects, through neuronal plasticity, have developed a variety be most sensitive to host-plant odours when they are of mechanisms that allow them to modulate their behaviour. In some insect species, larvae and adults use rather different olfactory cues and exhibit different behaviours in *Correspondence: Sylvia Anton, Institut National de la Recherche response to the same cues (Ignell et al., 2001a). For example, Agronomique (INRA), UMR 1272, Physiologie de l’Insecte: Signalisation et Communication, Centre de Recherches de Versailles, in the desert locust, Schistocerca gregaria, nymphs respond route de Saint-Cyr, Bat A, 78026 Versailles cedex, France. to a binary mixture of two aggregation pheromone com- E-mail: [email protected] pounds, phenol and guaiacol (Obeng-Ofori et al., 1993,

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1994a,b; Torto et al., 1994), whereas adults respond speci- insects, most studies so far have investigated plasticity in the fically to a four-component pheromone blend (80% nervous system with physiological, anatomical, biochemical, phenylacetonitrile, benzaldehyde, guaiacol, and phenol) and molecular approaches. (Obeng-Ofori et al., 1993, 1994a,b; Torto et al., 1994). In the present paper, we review plasticity related to Moreover, numerous studies have shown that the same olfaction in moths and locusts as defined by the capacity of volatiles can also change their attractiveness for adult an insect to modulate its response to an odorant depend- insects depending on the physiological status or environ- ing on its physiological state in order to optimize its oppor- mental conditions of the individual. Among them, the tunities for reproduction. In this context, modulation of a effect of age has been shown on pheromone responses response to an odorant can occur as a function of age, hor- of male moths (Shorey et al., 1968; Turgeon et al., 1983; monal, or mating status and can include modulation of Gadenne et al., 1993) and on the search for a potential host peripheral and/or central nervous processing of chemical in the mosquito Aedes aegypti (Davis, 1984). Responses to stimuli leading to the appropriate behaviour. plant odours are also age dependent, e.g., in Drosophila melanogaster (Devaud et al., 2003, and references therein). The olfactory pathway Photoperiod, light, and temperature are known modula- The importance of the sense of smell is reflected by the size tors of sex pheromone responses of moths such as Ephestia and structure of olfactory organs and areas in the central kühniella (Traynier, 1970), Holomelina immaculata (Cardé nervous system dedicated to the processing of olfactory & Roelofs, 1973), Chilo suppressalis (Kanno, 1981), Tricho- information (Hansson & Anton, 2000). In insects, volatiles plusia ni (Linn et al., 1986; Linn & Roelofs, 1992), and are detected by olfactory receptor neurons (ORN), housed Pseudaletia unipuncta (Dumont & McNeil, 1992). Mating within cuticular sensilla mainly on the antennae or the has been shown to induce or enhance the female response mouthparts (review in Keil, 1999). The axons of ORNs to plant odours in many species such as Ameyelois transitella project via the antennal nerve into the primary olfactory (Phelan & Baker, 1987), T. ni (Landolt, 1989), and Manduca centre, the antennal lobe (AL). There they make synaptic sexta (Mechaber et al., 2002). However, certain virgin contact with intrinsic AL neurons, the local interneurons, females of the codling moth, Cydia pomonella, were also and with AL output neurons, the projection neurons, attracted by host-plant volatiles (Hern & Dorn, 1999; Yan which transfer information to higher brain centres, such as et al., 1999). In the fruit fly, Ceratitis capitata, the females the mushroom bodies and the lateral protocerebrum (de of which are attracted by a male-produced pheromone, Belle & Kanzaki, 1999). Modulatory neurons originating mating induces a switch in behavioural response: mated from different parts of the central nervous system, on the females stop responding to sex pheromone and start other hand, send their axons into the ALs (for review, see responding to plant odours (Jang, 1995). Anton & Homberg, 1999; Homberg & Müller, 1999). The In cases where environmental changes occur frequently AL consists of a species-specific number of globular neuropil, and immediate action is required, nervous systems, which the glomeruli (for review, see Rospars, 1988; Hansson & steer behaviour, can respond quickly through modulation Anton, 2000). In insect species that use sex pheromones, a or learning by means of neurophysiological, molecular, or sexual dimorphism is found at different levels of the olfactory anatomical changes. Two types of behavioural plasticity system. Male moths have large numbers of olfactory and their neuronal basis have mainly been studied so receptor neurons tuned to single compounds of the sex far, namely, plasticity induced by physiological changes (e.g., pheromone produced by conspecific females, and large hormone levels) and experience-induced plasticity (e.g., glomeruli at a specific position within the AL, called the different forms of learning). In this review, the second type macroglomerular complex (MGC), are entirely dedicated of plasticity will not be discussed. Adaptations to physio- to the processing of these sex pheromones (Hansson & logical and environmental changes are common in animals, Christensen, 1999). either as short-term modifications (e.g., via modulation) leading to changes in neural activity or as long-term modi- Mating-dependent plasticity fications (e.g., via life history traits) leading to changes in Many insects undergo significant changes in their general gene expression and neural structure. The development of physiology during mating. The more general physiological the nervous system has been well described in many animal effects are linked to drastic changes in olfactory-guided species including both vertebrates and invertebrates. behaviour in both males and females of a number of insect Although the study of brain maturation in adult animals species investigated. In particular, biologically active volatile has only recently begun, it is now clearly admitted that chemical stimuli that are necessary for sex recognition (sex developmental processes continue throughout adult life pheromones) and host-plant finding (host-plant odours), (Cayre et al., 2002; Huetteroth & Schachtner, 2005). In can be either attractive or without effect, depending on the

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state of the adult insect. Mated herbivorous females are were unable to mate more than once during the same more likely to search for their host plant in order to lay night, and wind tunnel experiments with newly mated their eggs. Indeed, many studies in moths have shown that males resulted in a complete inhibition of upwind ﬂight mated females are more attracted to host-plant volatiles behaviour (Gadenne et al., 2001) (see Figure 1). Electro- than virgin females (e.g., in Phelan & Baker, 1987; Landolt, antennogram (EAG) recordings revealed that the peripheral 1989; Tingle et al., 1989; Wiesenborn & Baker, 1990; Tingle olfactory system did not change in sensitivity to the sex & Mitchell, 1992; Mechaber et al., 2002). On the contrary, pheromone after mating. Intracellular recordings from AL mating inhibits host search in blood-fed mosquito females, projection neurons, however, demonstrated that the which are ready to oviposit (Fernandez & Klowden, 1995). proportion of highly sensitive neurons responding to the In most species these effects are reversible and after a sex pheromone dropped drastically after mating (Gadenne species-speciﬁc time interval, the original state is resumed. et al., 2001) (see Figure 1). All physiological parameters Neurobiological investigations were performed in male were restored during the following night: high sensitivity and female moths to determine at which level and in which of AL neurons allowed males to respond behaviourally to way the nervous system is involved in the behavioural changes the sex pheromone and, because the protein content of observed. Males were studied in the noctuid moth Agrotis their SAG was renewed, males were able to mate again ipsilon and females in the tortricid moth Lobesia botrana. (Duportets et al., 1998; Gadenne et al., 2001) (see Figure 1).

Mating inhibits sex pheromone response in Agrotis ipsilon males Mating triggers plant-odour response in Lobesia botrana females In A. ipsilon males, mating ‘switches off’ the olfactory In female moths, mating ‘switches on’ the olfactory system system leading to an inhibition of behavioural sex pheromone to allow them to respond to plant odours and oviposit. In responses in males. In this species, males become sexually female L. botrana, wind tunnel experiments using various mature a few days after adult emergence (Duportets et al., grapevine plant parts as odour sources, demonstrated that 1998). Juvenile hormone (JH) was shown to control sexual only mated females were attracted. Virgin females never maturation in general and the development of the sex showed any upwind ﬂight behaviour in response to any accessory glands (SAG) more speciﬁcally in this species. of the plant parts used (Masante-Roca et al., 2007). As in An elevated protein content of the SAGs allows the mature A. ipsilon males, EAG recordings did not reveal any dif- male to produce and transfer a spermatophore into the ferences in the response threshold to plant odour compounds female (Duportets et al., 1998). The SAG protein content between virgin and mated females (Masante-Roca et al., decreases to a low level directly following mating and 2007). However, intracellular recordings from AL neurons resumes during the next night without any measurable during stimulation with single plant compounds showed a changes in JH biosynthesis activity (Duportets et al., 1998) tendency towards lower thresholds in mated compared to (see Figure 1). Mating experiments showed that males virgin females (Masante-Roca et al., 2002).

Figure 1 Representation of age/juvenile hormone- and mating-dependent plasticity of olfaction in the studied noctuid moth Agrotis ipsilon. Black bars indicate the level of activity for the criteria during the maturation and postmating processes. Accumulated data from Gadenne et al. (1993, 2001), Duportets et al. (1998), Anton & Gadenne (1999).

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Mechanisms underlying fast and transient plasticity ing the release of the pheromone biosynthesis activating Our studies in males of A. ipsilon and in females of neurohormone (PBAN), thus inhibiting the production L. botrana revealed that both the behavioural response and and release of sex pheromone by the mated female (review the sensitivity of the AL neurons to odours (sex pheromones in Rafaeli, 2005, and references therein). and plant odours) changed soon after mating had actually Work is now in progress to understand the mechanisms occurred. The data collected so far indicate that the clear-cut underlying the rapid neuronal plasticity in mated males of behavioural changes might be due to changes in sensitivity A. ipsilon and females of L. botrana. As an analogy to what of central olfactory neurons rather than of the peripheral is known for pheromone production in females, it will be system. The results of EAG recordings do not, however, interesting to test the hypothesis that there could be either exclude changes in the sensitivity of individual ORNs. an inhibitory factor present or a stimulatory factor lacking In females of the yellow fever mosquito, A. aegypti, a in the SAG or in some part of the brain in newly mated reversible modulation of the sensitivity of ORNs to a host A. ipsilon males or vice versa in L. botrana females. odour component, lactic acid, has been shown (Davis, 1984). Another possible mechanism to explain the rapid change In this case, modulation was dependent on a haemolymph- in neuron sensitivity could be the involvement of neuro- borne factor present in blood-fed females, but it is not modulators, such as biogenic amines. Indeed, both known if mating has the same effect on the neuronal level octopamine and serotonin have been shown to act on sex (Davis, 1984). On the other hand, a peptide present in pheromone response and on the sensitivity of ORNs and accessory glands of male A. aegypti has been shown to AL neurons (see reviews in Blenau & Baumann, 2001; inhibit host-seeking behaviour after mating (Fernandez & Roeder, 2005). Octopamine was shown to play a role in the Klowden, 1995; Lee & Klowden, 1999). In both studies of sexual behaviour of male moths by improving pheromone behaviour and receptor neuron sensitivity in mosquitoes, blend discrimination and orientation towards pheromone effects were investigated 2–3 days after ‘treatment’, much sources (Linn & Roelofs, 1986, 1992; Linn et al., 1992, 1996). longer delays as the fast mating effects we observed in moths. It has also been shown to have an effect on peripheral In addition, female mosquito behaviour is influenced by olfactory neurons by enhancing the antennal response to many interacting factors such as blood ingestion, mating, pheromone through the transepithelial potential of olfac- and oocyte development (for review, see Klowden, 1996) tory sensilla (Pophof, 2000; Dolzer et al., 2001; Grosmaître and the situation is therefore much more complex than et al., 2001), but not to plant odours (Pophof, 2002). At the in moths. central level, octopamine has been shown to be the respon- In A. ipsilon, as males are physiologically unable to mate sible transmitter within the reinforcement pathway during a second time during one single night, the significant associative learning of the honeybee (Hammer, 1993; decrease in sensitivity of the central olfactory system avoids Farooqui et al., 2003). Serotonin was shown to enhance the a waste of energy. Here, mating induces a transient inhibi- responses of individual AL neurons, and of neuron ensem- tion of pheromone responsiveness and AL neuron sensitivity. bles as measured by calcium imaging within the central In L. botrana, virgin females do not respond to plant olfactory system in different moth species (Kloppenburg & odours, they stay stationary and emit their sex pheromone. Hildebrand, 1995; Kloppenburg & Heinbockel, 2000; We hypothesize that females first need to attract a male for Kloppenburg et al., 1999; Hill et al., 2003). mating and only when they have mated does their priority In the case of A. ipsilon, mating could trigger a release of change towards egg laying and they start to search for an biogenic amines that could act at the antennal and/or the oviposition site. In both cases, a signal is presumably sent central nervous level. We plan to study the possible involve- to the brain from the reproductive system to momentarily ment of octopamine and serotonin in the fast transient ‘switch off/on’ the olfactory system. This signal is so far inhibition of AL neuron sensitivity in males of A. ipsilon. unknown and could be neural (through the ventral nerve cord) or physiological (via a humoral factor). In female Age- and hormone-dependent plasticity moths, mating induces a transient inhibitory period cha- Age- and hormone-dependent changes in olfactory-guided racterized by a temporal arrest of pheromone production, behaviour have been found in a few insect species. Male which lasts until the next night (Raina, 1988). This tempo- migratory locusts change their sexual behaviour under ral inhibition of pheromone production is caused by a hormonal control (Greenfield & Pener, 1992; Ignell et al., factor present in the haemolymph (Raina, 1989). This factor, 2001b). Male moths change their responsiveness to sex originating from the SAGs of the male and transferred pheromones with age and endocrine situation in migratory into the female during copulation, has been isolated and species (Cusson et al., 1991; Gadenne et al., 1993), whereas sequenced as the pheromonostatic peptide (Kingan et al., males in non-migratory species respond to the female sex 1993). It was further shown that this peptide was inhibit- pheromone directly after hatching (Anderson et al., 2003).

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In honeybees, odour-guided behaviour changes with age quantity of JH acids instead of JH in their corpora allata and hormonal status during the change of tasks within the (CA) (Peter et al., 1981; Bhaskaran et al., 1988; Cusson community (Robinson, 1987). et al., 1993; Ho et al., 1995). This high titre of JH has been In various insects, the degree of reproductive develop- shown to be mainly involved in the control of SAG deve- ment and activity at adult emergence varies greatly (review lopment in Orthoptera and Lepidoptera (Gillot, 2003). in Wyatt & Davey, 1996). In some insects such as the silk- However, in the true armyworm, P. unipuncta, male response moth, Bombyx mori, or the gypsy moth, Lymantria dispar, to sex pheromone also shows a correlation with rates of gametogenesis is complete at the time of eclosion, and adults JH biosynthesis that suggests dependence on JH action of these species do not feed and are ready for immediate (McNeil et al., 1994). In locusts, an increase in JH titre has mating and oviposition, with no need for hormonal regu- been associated with a decrease in response to aggregation lation. In other insects, such as cockroaches, locusts, and pheromones in locusts (Ignell et al., 2001b; for a review on mosquitoes, oogenesis is completed at eclosion, but the JH and locust phase polymorphism, see Pener, 1991). timing for reproduction is regulated by food intake and Below we describe the results of studies on the role of JH other stimuli, which act through JH. In still other insects, in the maturation of reproduction-related behaviour and as in Lepidoptera, development and egg production are its neurobiological basis both in the locust S. gregaria and sequential and non-overlapping: hormones regulate egg in the moth A. ipsilon. development during the adult stage. Here, reproduction can be delayed or repressed in response to environmental Age- and juvenile hormone-dependent response to aggregation signals (e.g., photoperiod and temperature) in order to pheromones in Schistocerca gregaria adapt to an unfavourable season. This is the case in the Migratory locusts exist in two different phases: the solitary monarch butterﬂy, Danaus plexippus (Herman, 1973), and and the gregarious phase. Individuals can change from one in the noctuid moths P. unipuncta (Fields & McNeil, 1984) phase to the other, and the mechanisms that elicit a phase and A. ipsilon (Kaster & Showers, 1982), which undergo shift are relatively complex (Pener, 1991). One prerequisite seasonal migrations characterizing a state of reproductive for gregarization is an aggregation behaviour, which has diapause. For these species and also for many insect species been shown to be regulated by aggregation pheromones from other orders, JH contributes to variations in migra- (Obeng-Ofori et al., 1993). Male adult desert locusts, tory life histories (Dingle & Winchell, 1997). Moreover, S. gregaria, produce an aggregation pheromone, which is using radiochemichal assays for JH biosynthetic activity or attractive for young adult males and females (Torto direct radioimmunoassay of JH haemolymphatic titres, JH et al., 1994). The response to the aggregation pheromones deprivation and/or applications of JH mimics, JH has been changes, however, with adult age, and adults are indifferent shown to control both vitellogenesis and oogenesis in females to aggregation pheromones from 3- to 4 weeks of age and SAG activity in males (review in Wyatt & Davey, 1996). (Ignell et al., 2001b). These differences had not been found The role of JH in the sexual behaviours associated with in an earlier study (Torto et al., 1994). Differences in rearing reproduction has been studied in various insect orders conditions and the pheromone doses tested might account such as Orthoptera, Dictyoptera, Coleoptera, Diptera, for differences between the two studies. The behavioural and Lepidoptera (review in Wyatt & Davey, 1996) and responses to aggregation pheromones were altered when Hymenoptera (Robinson et al., 1992; Robinson & Vargo, the JH level in the insects, which increases naturally with 1997). The previously described long-lived moth species, age, was manipulated: allatectomized 4-week-old males and which have an extended period of adult maturation, are females were attracted by the aggregation pheromones, speciﬁcally suited to study changes in behaviour and its whereas 1-week-old locusts, which had been injected with neurobiological basis linked with these maturation pro- JH 2 days after the last moult, were indifferent to the cesses. Juvenile hormone was found to be involved in the pheromone (Ignell et al., 2001b). Electroantennogram female sexual behaviour associated with reproduction in recordings revealed no differences in the sensitivity of two migrant moth species, P. unipuncta and A. ipsilon, in the antennal system to aggregation pheromones between which JH is involved in the control of pheromone produc- the different experimental groups (Ignell et al., 2001b). tion and release in females (Cusson & McNeil, 1989; Intracellular recordings from AL output neurons showed a Gadenne, 1993). In both species, JH was found to act through shift from a large percentage of pheromone-responding the release of PBAN in the brain (Cusson et al., 1994; neurons in young adults and allatectomized 4-week-old Picimbon et al., 1995). individuals, to a large percentage of non-responding neurons In male insects, very little is known about the reproduc- in 4-week-old adults and young individuals injected tive events leading to mating and their eventual hormonal with JH (Ignell et al., 2001b). These results indicate that control. It has been known that males produce a high apparently aggregation behaviour is especially important in

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young adult locusts, which are in search of a mating partner neurons in sexually mature control males and in young and susceptible for gregarization (Ignell et al., 2001b). males injected with JH were highly sensitive (Anton & Gadenne, 1999). The JH injection had, however, its full Age- and juvenile hormone-dependent response to sex pheromone in effect only 2 days after injection, even if some changes Agrotis ipsilon occurred already after 1 day (Gadenne & Anton, 2000). A The noctuid moth A. ipsilon is a migratory species that is differential effect of age and JH was observed in the not sexually mature at emergence (Swier et al., 1976, 1977). response of AL neurons to the blend and single pheromone Maturation processes take place during adult life in both compounds: the strongest effect was seen when the sexes. In females, photoperiod acts, via the JH levels, on the complete blend or the major component (Z)-7-dodecen- developmental rate of oogenesis and behaviours associated 1-yl acetate, was used for stimulation (Gadenne & Anton, with reproduction (calling, pheromone release, and egg 2000). A smaller change in neuron sensitivity was observed laying): newly emerged females have low JH biosynthetic in response to (Z)-9-tetradecen-1-yl acetate, and no signi- activity, undeveloped ovaries, do not produce pheromone, ficant effect was observed for the minor compound (Z)- and therefore cannot mate (Gadenne, 1993). In males, newly 11-hexadecen-1-yl acetate, which might either be due to emerged adults have low JH biosynthetic activity and missing plasticity or might simply be difficult to detect, as the protein content of their SAGs is very low (Duportets there are so few neurons responding to that component in et al., 1998) (see Figure 1). If they would mate at this early general. Moreover, the observed changes in the sensitivity stage of adult life, they would be unable to produce a of central neurons were restricted to pheromone-responding spermatophore. Experiments with JH deprivation, using neurons within the MGC. Neurons arborizing in the so- a JH antagonist, showed that JH actually controls the called ordinary glomeruli and responding to plant odours development of the SAG in males of A. ipsilon (Duportets did not change their sensitivity with age or JH level (Greiner et al., 1998). After a few days of maturation, the reproductive et al., 2002). The sensitivity of AL neurons involved in cen- system is fully functional and males can mate and are able tral plant volatile processing is therefore age independent to produce and transfer a spermatophore into the female. and the action of JH is specific for central sex pheromone When testing the behavioural responsiveness of males to processing in A. ipsilon males. sex pheromone, clear changes were found with age: freshly hatched males did not react to the conspecific female’s Mechanisms underlying slow developmental plasticity pheromone, but after a few days some males did respond Our results with locusts and moths indicate that sensitivity and the best responses were obtained within about 5 days changes in response to pheromones occur primarily within (at 21 °C) (Gadenne et al., 1993) (see Figure 1). A similar the central nervous system whereas the sensitivity of the age-dependent response to sex pheromone was found in peripheral system remains stable. In female blowflies, however, another migratory moth, P. unipuncta (Turgeon et al., 1983). EAG amplitudes were found to increase as a function of age This increase in behavioural responsiveness was paralleled in response to oviposition cues (Crnjar et al., 1990). To explain by an increase in JH biosynthesis in the CA, as measured by the neuronal plasticity characterized by age-dependent radiochemical assay (Duportets et al., 1998) (see Figure 1). changes in behaviour and central processing of chemical Using manipulations of the JH level, it was shown that the stimuli, one could expect structural and physiological changes age-dependent changes in behaviour could be altered under to occur within the olfactory brain centres. Indeed, morpho- the influence of JH. Sexually mature males, deprived of JH logical changes in olfactory brain structures have been by allatectomy, did not respond to the sex pheromone, associated with maturation and caste specificity in bees whereas freshly hatched males injected with JH responded (Withers et al., 1993; Fahrbach et al., 1995, 2003; Winnington better to the sex pheromone than control males of the same et al., 1996; Farris et al., 2001; Brown et al., 2002; Wang et al., age (Gadenne et al., 1993). To determine the level in the 2005), ants (Gronenberg et al., 1996; Julian & Gronenberg, olfactory pathway, where JH (and age) has an effect, various 2002), and Drosophila (Technau, 1984; Devaud et al., 2003). physiological techniques have been used. EAG recordings In the described cases of neuronal plasticity (in A. ipsilon showed no difference between the responses to sex phe- males and S. gregaria) linked with the maturation of the romone for males at different ages and JH levels (Gadenne olfactory system, the cascade of events leading to full sexual et al., 1993) (see Figure 1). Intracellular recordings from maturation (SAG and ovarian maturation, JH biosynthesis, AL neurons revealed a large proportion of pheromone AL neuron sensitivity, sexual, and aggregation behaviour) responding neurons with very high thresholds in freshly occurs within several days. The relatively slow effect of JH hatched males and in sexually mature, allatectomized on AL neurons and behaviour could be referred to as ‘a males (Anton & Gadenne, 1999) (see Figure 1). On the long-latency activational effect’ (Elekonich & Robinson, other hand, the vast majority of pheromone-responding 2000). The age- and JH-dependent plasticity of the central

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olfactory system could be caused by structural, physio- levels in the pathway. The changes in the observed behavioural logical, or molecular changes or a combination of parts or output are probably due to a combinatorial effect on all of these aspects. different levels of the sensory-motor pathway. So far we Regarding the structural changes that might be involved have mainly investigated parts of the pathway close to, or in the maturation of A. ipsilon males, we have tested the identical to the sensory input (antennae, AL neurons). In hypothesis that adult neurogenesis could occur in some future, we will need to analyse this in more detail (single parts of the brain, and that newly produced neurons could receptor neuron level, plasticity of local circuits, and output participate in the higher sensitivity of neurons in mature pathways), but we should also investigate the part of the males. Our results show that adult neurogenesis does occur nervous system more closely linked with the effectors in brains of both male and female adults of A. ipsilon (protocerebral plasticity and effects on descending pathways). (Dufour & Gadenne, 2006). Persistent dividing neuro- To explain modulation at the different levels within the blasts are localized in the mushroom bodies and give rise olfactory pathway, we plan to investigate (i) the role of to a few new Kenyon cells. Neurogenesis was observed in neuromodulators such as biogenic amines, neuropeptides, both newly emerged and sexually mature males (Dufour & and nitric oxide, (ii) the role of specific modulatory Gadenne, 2006). Adult neurogenesis has also been described neuronal circuits, and (iii) potential changes in synaptic in the house cricket and a few other insects (Cayre et al., connectivities and/or synaptic weight. 1994, 1996). In the house cricket, newly born neurons were The process of mating probably triggers a cascade of shown to play a role in olfactory learning and memory gene expression leading to the production of specific (Scotto-Lomassese et al., 2003). The recent findings on proteins involved in the detection and processing of the neurogenesis in A. ipsilon suggest that the increase in odorants both at the antennal level and far up into the behavioural sex pheromone response of mature males brain, finally leading to the characteristic behaviours of the might result from effects at different levels in the olfactory mated moths. Recent studies have shown that gene expres- pathway. It is clearly correlated with an increase in the sen- sion profiles change in individual adult insects, e.g., during sitivity of AL neurons, but higher brain centres (such as the the caste determination of honeybees when nurses change mushroom bodies) might additionally participate in into foragers (Whitfield et al., 2003), and in migratory maturation. In addition, we will have to re-evaluate possible locusts when they change between the solitarious and the effects on the peripheral olfactory system by studying gregarious phase (Kang et al., 2004). One of our future responses of individual ORNs. As described above, biogenic goals will be to study the gene expression profiles of mated amines and octopamine in particular have been shown moths vs. virgin moths (at the brain level) in order to to be involved in many aspects of insect life including be- unveil possible genes involved in the observed plasticity. haviour and locomotion (for review, see Roeder, 2005). In honeybees, octopamine has been shown to act on Acknowledgements nestmate recognition (Robinson et al., 1999), division of labour (Schulz et al., 2002a; Barron & Robinson, 2005; We thank Prof. F. Marion-Poll and three anonymous Lehman et al., 2006), responsiveness to foraging stimuli referees for valuable comments on the manuscript and (Barron et al., 2002), memory consolidation (Farooqui Prof. Monika Hilker for the invitation to write this review. et al., 2003), and pollen hoarding (Schulz et al., 2004). Although octopamine and JH can independently induce References foraging behaviour in bees, some evidence on interactions between the effects of JH and octopamine is emerging Anderson P, Sadek MM & Hansson BS (2003) Pre-exposure (Schulz et al., 2002a,b). Increasing JH levels leads to modulates attraction to sex pheromone in a moth. Chemical increasing octopamine levels in the brain, and more spe- Senses 28: 285–291. cifically in the ALs, inducing foraging behaviour (Schulz Anton S & Gadenne C (1999) Effect of juvenile hormone on the et al., 2002a,b). We hypothesize that biogenic amines could central nervous processing of sex pheromone in an insect. act as mediators between hormones, behavioural, and cen- Proceedings of the National Academy of Sciences USA 96: 5764–5767. tral nervous effects also in the observed developmental Anton S & Homberg U (1999) Antennal lobe structure. Insect plasticity of the olfactory system in locusts and moths. Olfaction (ed. by BS Hansson), pp. 98–125. Springer, Berlin, Germany. Conclusion Barron AB & Robinson GE (2005) Selective modulation of task performance by octopamine in honey bee (Apis mellifera) Altogether, the results described above indicate that the division of labour. Journal of Comparative Physiology A 191: plasticity of the olfactory system probably acts at different 659–668.

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