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Dopamine and Mushroom Bodies in Drosophila: Experience-Dependent and -Independent Aspects of Sexual Behavior Wendi S

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Dopamine and Mushroom Bodies in Drosophila: Experience-Dependent and -Independent Aspects of Sexual Behavior Wendi S Downloaded from learnmem.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Dopamine and Mushroom Bodies in Drosophila: Experience-Dependent and -Independent Aspects of Sexual Behavior Wendi S. Neckameyer Department of Pharmacological and Physiological Science Saint Louis University School of Medicine St. Louis, Missouri 63104 USA Abstract Introduction Catecholamines act as transmitters in the ner- Depletion of dopamine in Drosophila vous systems of both vertebrates and invertebrates; melanogaster adult males, accomplished several pharmacological studies in mammalian sys- through systemic introduction of the tems have implicated catecholamines in synaptic tyrosine hydroxylase inhibitor modulation and behavioral plasticity (Civelli et al. 3-iodo-tyrosine, severely impaired the ability 1993; Sawaguchi and Goldman-Rakic 1994). Pertur- of these flies to modify their courtship bation of catecholaminergic systems has also been responses to immature males. Mature males, implicated in the etiology of schizophrenia and when first exposed to immature males, will depression (Hornykiewicz 1966; Goldstein and perform courtship rituals; the intensity and Deutch 1992; Seeman et al. 1993), suggesting that duration of this behavior rapidly diminshes catecholamines play a role in the modulation of with time. Dopamine is also required for cognitive function. normal female sexual receptivity; Tyrosine hydroxylase, the first and rate-limit- dopamine-depleted females show increased ing enzyme in the synthesis of catecholamines, is latency to copulation. One kilobase of 5* highly conserved among evolutionarily diverged upstream information from the Drosophila species. Drosophila tyrosine hydroxylase (DTH) tyrosine hydroxylase (DTH) gene, when shares 50% amino acid identity with its mammalian fused to the Escherichia coli b-galactosidase counterparts, and its biochemical and regulatory reporter and transduced into the genome of mechanisms are also highly conserved (Neckam- Drosophila melanogaster, is capable of eyer and Quinn 1989; W. Neckameyer, unpubl.). directing expression of the reporter gene in Depletion of dopamine levels in larval and adult the mushroom bodies, which are believed to stages by systemic administration of tyrosine hy- mediate learning acquisition and memory droxylase inhibitors has proven to be a useful phar- retention in flies. Ablation of mushroom macological approach to elucidate the physiologi- bodies by treatment of newly hatched larva cal requirements for dopamine. with hydroxyurea resulted in the inability of Recently, we have demonstrated that dopa- treated mature adult males to cease mine modulates female sexual receptivity in Dro- courtship when placed with untreated sophila melanogaster (Neckameyer 1998). This immature males. However, functional role for dopamine also appears to be utilized in mushroom bodies were not required for the mammalian systems (Mani et al. 1994). Exposure to dopaminergic modulation of an innate male courtship stimulates a suitable female to ac- behavior, female sexual receptivity. These cept the male’s overtures (Tompkins et al. 1982); data suggest that dopamine acts as a however, this is not considered a learned behavior. signaling molecule within the mushroom One study has suggested that in Drosophila, as bodies to mediate a simple form of learning. in mammals, biogenic monoamines may play a role LEARNING & MEMORY 5:157–165 © 1998 by Cold Spring Harbor Laboratory Press ISSN1072-0502/98 $5.00 LEARNING& MEMORY 157 Downloaded from learnmem.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press Neckameyer in learning (Tempel et al. 1984), but this work has of transgenic lines will be presented elsewhere (W. not yet been replicated. Using a pharmacological Neckameyer, A. Mayer, and M. Van Kanegan, in approach to deplete dopamine levels in adult prep.). Cesium chloride-banded plasmid DNA (500 males, it has been demonstrated here that dopa- µg/ml) was injected into a w− strain (Rubin and mine is required for normal habituation in an ex- Spradling 1982) with the pp25.7wc turbo plasmid perience-dependent courtship paradigm and that (100 µg/ml) as the source of transposase (Robert- the focus for this dopaminergic modulation of one son et al. 1988). type of learning likely resides within the mush- Single transformant lines for both the 38 to 58 room bodies. Female sexual receptivity, which (p1.28DTHlacZ) and the 58 to 38 (p1.2DTHlacZ) does not require learning, also does not require orientations of the DTH promoter sequence were functional mushroom bodies. generated; the p1.28DTHlacZ stock, when homo- zygous, exhibited a strong red eye color. The Materials and Methods p1.2DTHlacZ stock, when homozygous, exhibited a light apricot eye color. Two other independent lines were isolated from the latter stock by use of FLY CULTURE AND COURTSHIP ANALYSIS a genetic strain carrying a source of transposase to Unless otherwise specified, wild-type Canton-S jump the transgene, 1F-4 and 2M-1, which exhib- flies were maintained in individual pint bottles con- ited orange and red eye colors, respectively. taining standard agar–cornmeal–molasses food at 25°C on a 12-hr light–dark cycle. Newly eclosed STAINING FOR b-GALACTOSIDASE males were placed singly in vials containing filter discs saturated with 2% yeast–5% sucrose or yeast– Third instar larval and 1-day-old adult brain tis- sucrose plus 10 mg/ml 3-iodo-tyrosine (3IY), or sues were dissected from control (Df[1]w and yeast–sucrose plus 10 mg/ml 3IY and 10 mg/ml p1.28DTHlacZ) and experimental (p1.2DTHlacZ L-3,4-dihydroxyphenylalanine (LDOPA). Treatment series) lines. The staining protocol was as follows: with this concentration of inhibitor has previously Tissues were dissected in PBS and immediately been shown to substantially deplete dopamine lev- fixed for 5 min in 5% formaldehyde/1× PBS. Tis- els in adult flies (Neckameyer 1996). After 4–6 sues were washed 4× for 5 min in 1× PBS, and days, each male was placed with a newly eclosed incubated overnight at 37°C in a moist chamber in (0–3-hr-old) male fly and observed in a 10-position assay buffer [3.1 mM K3Fe(CN)6/3.1 mM K4Fe mating chamber wheel for 30 min. The courtship (CN)6/0.15 M NaCl/1 mM MgCl2/10% DMSO/10 paradigm has been described previously (Gailey et mM NaPi (pH 6.8)/0.1% 5-bromo-4-chloro-3-indolyl- al. 1986; for review, see Greenspan 1995), as has b-D-galactoside]. Samples were postfixed by wash- the conditioned response to immature males (Gai- ing 4× for 5 min in 1× PBS, fixing in 5% formalde- ley et al. 1982). Courtship indices (CIs) were col- hyde, 1× PBS for 2 hr, followed by four 5-min lected as described in Gailey et al. (1986; see also washes in 1× PBS. Tissues were prepared for Siegel and Hall 1979) for the first and last 10 min- mounting by incubation for at least 20 min in a utes of the 30-min observation period. 30%–50%–90% glycerol series in 1× PBS and were mounted in 90% glycerol/1× PBS on glass slides. GENERATION OF TRANSGENIC LINES ABLATION OF MUSHROOM BODIES A 1-kb genomic fragment from the DTH gene WITH HYDROXYUREA (Neckameyer and White 1993), consisting of ∼800 bp of promoter sequences adjacent to the first 200 Several hundred Canton-S adult flies were bp of DTH 58-untranslated sequences was ligated maintained for 1 week in a population cage kept at into the the unique BamHI site of the pJY505 25°C on a 12-hr light–dark cycle. Flies were al- CaSpeR transformation vector (gift of Dr. Jerry Yin) lowed to lay eggs for 1–1.5 hr on apple juice–agar in both the 58 to 38 (p1.2DTHlacZ) and 38 to 58 plates, and any larvae that had hatched were re- (p1.28DTHlacZ) orientations. pJY505 is a deriva- moved after 20 hr. Newly hatched larvae were tive of CaSpeRhs43bgal, which includes a trun- then collected within a 45-min period and placed cated hs43 promoter and the E. coli b-galactosidase on 60-mm petri dishes containing apple juice–agar gene downstream of a multiple cloning region (Yin and either a small amount of yeast paste (0.5 grams et al. 1994). Details of the cloning and generation of baker’s yeast in 1 ml of H2O), or yeast paste with LEARNING& MEMORY 158 Downloaded from learnmem.cshlp.org on September 23, 2021 - Published by Cold Spring Harbor Laboratory Press DOPAMINE AND MUSHROOM BODIES 50 mg/ml hydroxyurea (de Belle and Heisenberg 1994) for 4 hr at 25°C. The larvae were harvested and placed in vials containing 5 ml of 2% baker’s yeast, 5% yeast extract, 5% sucrose, 0.8% agar, and 0.5% 9:1 propionic acid/phosphoric acid. The vials were maintained at 25°C on a 12-hr light–dark cycle until eclosion, when male flies were placed singly in vials containing standard agar–cornmeal– molasses food, and maintained under these condi- tions for 4–6 days before behavioral analysis. A smaller cage containing the p1.2DTHlacZ trans- genic strain 2M-1 was run in parallel; larval brains were dissected from the wandering third instar stage and stained as described above. Figure 1: Dopamine-depleted males do not learn in a COURTSHIP ANALYSIS FOR FEMALE RECEPTIVITY conditioned courtship assay. Canton-S males were col- One to five newly eclosed females, treated lected within 1 hr of eclosion and maintained singly in with yeast paste or yeast paste plus hydroxyurea, vials. All animals were 4–5 days old when tested. (con) as described above, were maintained in vials con- Control animals fed 2% yeast–5% sucrose (n = 15); (3IY) taining standard fly food medium for 4–6 days. A animals fed yeast–sucrose containing 10 mg/ml 3IY (n = 18); (LDOPA) animals fed yeast–sucrose containing single female was placed with a 4- to 6-day-old vir- 10 mg/ml 3IY plus 10 mg/ml L-3,4-dihydroxyphenylala- gin untreated Canton-S male fly and observed in a nine (n = 15).
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