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The role of dopamine in Drosophila larval classical olfactory conditioning.

Selcho M, Pauls D, Han KA, Stocker RF, Thum AS - PLoS ONE (2009)

Bottom Line: Single cell analysis suggests that dopaminergic neurons do not directly connect gustatory input in the larval suboesophageal ganglion to olfactory information in the mushroom bodies.We found that dopamine receptors are highly enriched in the mushroom bodies and that aversive and appetitive olfactory learning is strongly impaired in dopamine receptor mutants.Genetically interfering with dopaminergic signaling supports this finding, although our data do not exclude on naïve odor and sugar preferences of the larvae.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Fribourg, Fribourg, Switzerland.

ABSTRACT
Learning and memory is not an attribute of higher animals. Even Drosophila larvae are able to form and recall an association of a given odor with an aversive or appetitive gustatory reinforcer. As the Drosophila larva has turned into a particularly simple model for studying odor processing, a detailed neuronal and functional map of the olfactory pathway is available up to the third order neurons in the mushroom bodies. At this point, a convergence of olfactory processing and gustatory reinforcement is suggested to underlie associative memory formation. The dopaminergic system was shown to be involved in mammalian and insect olfactory conditioning. To analyze the anatomy and function of the larval dopaminergic system, we first characterize dopaminergic neurons immunohistochemically up to the single cell level and subsequent test for the effects of distortions in the dopamine system upon aversive (odor-salt) as well as appetitive (odor-sugar) associative learning. Single cell analysis suggests that dopaminergic neurons do not directly connect gustatory input in the larval suboesophageal ganglion to olfactory information in the mushroom bodies. However, a number of dopaminergic neurons innervate different regions of the brain, including protocerebra, mushroom bodies and suboesophageal ganglion. We found that dopamine receptors are highly enriched in the mushroom bodies and that aversive and appetitive olfactory learning is strongly impaired in dopamine receptor mutants. Genetically interfering with dopaminergic signaling supports this finding, although our data do not exclude on naïve odor and sugar preferences of the larvae. Our data suggest that dopaminergic neurons provide input to different brain regions including protocerebra, suboesophageal ganglion and mushroom bodies by more than one route. We therefore propose that different types of dopaminergic neurons might be involved in different types of signaling necessary for aversive and appetitive olfactory memory formation respectively, or for the retrieval of these memory traces. Future studies of the dopaminergic system need to take into account such cellular dissociations in function in order to be meaningful.

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DA is Involved in Olfactory Learning, Naïve Odor and Naïve Taste Responses.Olfactory stimuli are detected by the dorsal organ and transmitted via the antennal lobe to the mb and lateral horn. The mb is postulated as a site of coincidence detection of odor signals from the antennal lobe and salt or sugar signals from the sog. The lateral horn and the sog might be involved in mediating naïve odor responses and naïve gustatory preferences, respectively (A–C). (A) We postulate a role of DA in aversive and appetitive olfactory learning, interfering either with aversive and appetitive reinforcement signaling, or with memory retrieval. DA neurons innervating the lateral horn (B) may be involved in naïve odor responses whereas DA neurons innervating the sog (C) may control naïve gustatory responses.
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pone-0005897-g008: DA is Involved in Olfactory Learning, Naïve Odor and Naïve Taste Responses.Olfactory stimuli are detected by the dorsal organ and transmitted via the antennal lobe to the mb and lateral horn. The mb is postulated as a site of coincidence detection of odor signals from the antennal lobe and salt or sugar signals from the sog. The lateral horn and the sog might be involved in mediating naïve odor responses and naïve gustatory preferences, respectively (A–C). (A) We postulate a role of DA in aversive and appetitive olfactory learning, interfering either with aversive and appetitive reinforcement signaling, or with memory retrieval. DA neurons innervating the lateral horn (B) may be involved in naïve odor responses whereas DA neurons innervating the sog (C) may control naïve gustatory responses.

Mentions: We found that blocking output from TH-GAL4 positive neurons impairs associative aversive scores (Figure 3H), but leaves responsiveness to the to-be-associated stimuli (1-octanol: Figure 3L; salt: Figure 3N) intact. The same defect in associative aversive scores is seen in the DA receptor mutants dumb1, dumb2 and DAMB (Figure 4A and 4C). Thus, together with the previous reports of Tempel et al. [102], Schwaerzel et al. [30], Kim et al. [35] and Honjo and Furukubo-Tokunaga [33], the requirement of dopaminergic signaling for associative aversive conditioning seems well substantiated (Figure 8A).


The role of dopamine in Drosophila larval classical olfactory conditioning.

Selcho M, Pauls D, Han KA, Stocker RF, Thum AS - PLoS ONE (2009)

DA is Involved in Olfactory Learning, Naïve Odor and Naïve Taste Responses.Olfactory stimuli are detected by the dorsal organ and transmitted via the antennal lobe to the mb and lateral horn. The mb is postulated as a site of coincidence detection of odor signals from the antennal lobe and salt or sugar signals from the sog. The lateral horn and the sog might be involved in mediating naïve odor responses and naïve gustatory preferences, respectively (A–C). (A) We postulate a role of DA in aversive and appetitive olfactory learning, interfering either with aversive and appetitive reinforcement signaling, or with memory retrieval. DA neurons innervating the lateral horn (B) may be involved in naïve odor responses whereas DA neurons innervating the sog (C) may control naïve gustatory responses.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2690826&req=5

pone-0005897-g008: DA is Involved in Olfactory Learning, Naïve Odor and Naïve Taste Responses.Olfactory stimuli are detected by the dorsal organ and transmitted via the antennal lobe to the mb and lateral horn. The mb is postulated as a site of coincidence detection of odor signals from the antennal lobe and salt or sugar signals from the sog. The lateral horn and the sog might be involved in mediating naïve odor responses and naïve gustatory preferences, respectively (A–C). (A) We postulate a role of DA in aversive and appetitive olfactory learning, interfering either with aversive and appetitive reinforcement signaling, or with memory retrieval. DA neurons innervating the lateral horn (B) may be involved in naïve odor responses whereas DA neurons innervating the sog (C) may control naïve gustatory responses.
Mentions: We found that blocking output from TH-GAL4 positive neurons impairs associative aversive scores (Figure 3H), but leaves responsiveness to the to-be-associated stimuli (1-octanol: Figure 3L; salt: Figure 3N) intact. The same defect in associative aversive scores is seen in the DA receptor mutants dumb1, dumb2 and DAMB (Figure 4A and 4C). Thus, together with the previous reports of Tempel et al. [102], Schwaerzel et al. [30], Kim et al. [35] and Honjo and Furukubo-Tokunaga [33], the requirement of dopaminergic signaling for associative aversive conditioning seems well substantiated (Figure 8A).

Bottom Line: Single cell analysis suggests that dopaminergic neurons do not directly connect gustatory input in the larval suboesophageal ganglion to olfactory information in the mushroom bodies.We found that dopamine receptors are highly enriched in the mushroom bodies and that aversive and appetitive olfactory learning is strongly impaired in dopamine receptor mutants.Genetically interfering with dopaminergic signaling supports this finding, although our data do not exclude on naïve odor and sugar preferences of the larvae.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Fribourg, Fribourg, Switzerland.

ABSTRACT
Learning and memory is not an attribute of higher animals. Even Drosophila larvae are able to form and recall an association of a given odor with an aversive or appetitive gustatory reinforcer. As the Drosophila larva has turned into a particularly simple model for studying odor processing, a detailed neuronal and functional map of the olfactory pathway is available up to the third order neurons in the mushroom bodies. At this point, a convergence of olfactory processing and gustatory reinforcement is suggested to underlie associative memory formation. The dopaminergic system was shown to be involved in mammalian and insect olfactory conditioning. To analyze the anatomy and function of the larval dopaminergic system, we first characterize dopaminergic neurons immunohistochemically up to the single cell level and subsequent test for the effects of distortions in the dopamine system upon aversive (odor-salt) as well as appetitive (odor-sugar) associative learning. Single cell analysis suggests that dopaminergic neurons do not directly connect gustatory input in the larval suboesophageal ganglion to olfactory information in the mushroom bodies. However, a number of dopaminergic neurons innervate different regions of the brain, including protocerebra, mushroom bodies and suboesophageal ganglion. We found that dopamine receptors are highly enriched in the mushroom bodies and that aversive and appetitive olfactory learning is strongly impaired in dopamine receptor mutants. Genetically interfering with dopaminergic signaling supports this finding, although our data do not exclude on naïve odor and sugar preferences of the larvae. Our data suggest that dopaminergic neurons provide input to different brain regions including protocerebra, suboesophageal ganglion and mushroom bodies by more than one route. We therefore propose that different types of dopaminergic neurons might be involved in different types of signaling necessary for aversive and appetitive olfactory memory formation respectively, or for the retrieval of these memory traces. Future studies of the dopaminergic system need to take into account such cellular dissociations in function in order to be meaningful.

Show MeSH
Related in: MedlinePlus