Behavioral functions of the insect mushroom bodies

Zars, Troy

doi:10.1016/s0959-4388(00)00147-1

Cited by 174 publications

(151 citation statements)

References 47 publications

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“…The MB appears to mediate taste-based attraction to AA for egg-laying purposes. Given the role of the MB in olfactory learning and memory (29,30), it was surprising that it regulates taste-based behavior in our paradigm. However, a neural connection between the suboesophageal ganglion, which receives gustatory input, and the MB has been described recently in honey bees (31), providing a possible neuroanatomical link.…”

Section: Discussionmentioning

confidence: 99%

Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila

Joseph¹,

Devineni²,

King

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

193

235

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Selection of appropriate oviposition sites is essential for progeny survival and fitness in generalist insect species, such as Drosphila melanogaster, yet little is known about the mechanisms regulating how environmental conditions and innate adult preferences are evaluated and balanced to yield the final substrate choice for eggdeposition. Female D. melanogaster are attracted to food containing acetic acid (AA) as an oviposition substrate. However, our observations reveal that this egg-laying preference is a complex process, as it directly opposes an otherwise strong, default behavior of positional avoidance for the same food. We show that 2 distinct sensory modalities detect AA. Attraction to AA-containing food for the purpose of egg-laying relies on the gustatory system, while positional repulsion depends primarily on the olfactory system. Similarly, distinct central brain regions are involved in AA attraction and repulsion. Given this unique situation, in which a single environmental stimulus yields 2 opposing behavioral outputs, we propose that the interaction of egg-laying attraction and positional aversion for AA provides a powerful model for studying how organisms balance competing behavioral drives and integrate signals involved in choice-like processes.choice behavior ͉ gustatory system ͉ olfactory system ͉ mushroom body ͉ ellipsoid body O viposition provides a powerful yet simple means for monitoring preference behavior in Drosophila melanogaster, since a laid egg represents a marker for female position. Past studies have used egg laying as a readout for conditions advantageous to progeny development (1, 2), in which oviposition preference effectively separates larvae of different sibling species of Drosophila. Egg laying has also been used to detect aversion toward compounds toxic to both larvae and adults (3, 4). Furthermore, numerous studies have used patterns of oviposition to distinguish subtle differences in host plant preferences, which have provided insights into resource requirements and ecological behaviors of different Drosophila species (5, 6).Despite numerous studies using oviposition-site selection as a behavioral readout, direct study of the relevant sensory circuits and the oviposition program itself have been initiated only recently in D. melanogaster (7,8). To investigate the genetic mechanisms and neural circuits regulating this important behavioral choice in D. melanogaster, we developed a simple yet robust 2-choice assay that utilizes acetic acid (AA), a naturally occurring product of fruit fermentation, as an egg-laying attractant (9, 10). However, in addition to verifying a strong egg-laying preference for AA, we surprisingly observed D. melanogaster show a strong positional aversion to the same AA-containing food. We demonstrate that when sampling for oviposition sites, females integrate input from distinct sensory modalities to choose a particular behavioral output from 2 competing options: ovipositional attraction for and positional repulsion to AA. Egg-laying preference is p...

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Section: Discussionmentioning

confidence: 99%

Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila

Joseph¹,

Devineni²,

King

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

193

235

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“…If so, for may play a role in higher-order reward pathways that mediate these individual behaviors. Interestingly, the mushroom bodies play a role in such complex behaviors, including courtship, courtship conditioning, spatial learning, aggression, and sleep (Zars 2000;Baier et al 2002;Joiner et al 2006;Pitman et al 2006). Accordingly, the role of the mushroom bodies in for-dependent larval reward learning hints at a role of for in more complex behaviors involving higher-order reward pathways.…”

Section: Discussionmentioning

confidence: 99%

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Kaun

Hendel²,

Gerber³

et al. 2007

Learn. Mem.

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Animals must be able to find and evaluate food to ensure survival. The ability to associate a cue with the presence of food is advantageous because it allows an animal to quickly identify a situation associated with a good, bad, or even harmful food. Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we investigate whether natural variation in the foraging (for) gene in Drosophila melanogaster larvae is important in mediating associations between either an odor or a light stimulus and food reward. We found that for influences olfactory conditioning and that the mushroom bodies play a role in this for-mediated olfactory learning. Genotypes associated with high activity of the product of for, cGMP-dependent protein kinase (PKG), showed greater memory acquisition and retention compared with genotypes associated with low activity of PKG when trained with three conditioning trials. Interestingly, increasing the number of training trials resulted in decreased memory retention only in genotypes associated with high PKG activity. The difference in the dynamics of memory acquisition and retention between variants of for suggests that the ability to learn and retain an association may be linked to the foraging strategies of the two variants.Learned associations such as identifying odors as indicators of food, or showing preferences for food-related odors, are conserved across diverse taxa from humans and mice to slugs, honeybees, and fruit flies (Ache and Young 2005). The fruit fly Drosophila melanogaster can use odors as cues for the presence of both a food reward and an aversive stimulus (Tempel et al. 1983;Scherer et al. 2003;Schwaerzel et al. 2003;Margulies et al. 2005;McGuire et al. 2005;Kim et al. 2007). Identifying genes underlying these natural learned responses is essential to understanding this ability. Here, we use classical reward conditioning to investigate how natural variation in the foraging (for) gene affects acquisition and decay of memory in D. melanogaster larvae.for encodes a cGMP-dependent protein kinase (PKG) (Osborne et al. 1997). In mammals, PKG is important for proper induction of long-term potentiation (LTP) and long-term depression (LTD) (Hartell 1994;Zhuo et al. 1994;Lev-Ram et al. 1997;Arancio et al. 2001;Fiel et al. 2003Fiel et al. , 2005Kleppisch et al. 2003;Hofmann et al. 2006). Although LTP and LTD are thought to be important mechanisms underlying learning and memory (Whitlock et al. 2006), few studies have shown a direct role for PKG in learning and memory. This study aims to do this by investigating how learning differs between allelic variants of for in Drosophila larvae.for is an ideal candidate to study how natural genetic variation can affect learning and memory, since natural for variants exist that have subtle but significant variations in PKG activity (Osborne et al. 1997). The rover variants of for (for R ) have higher for transcript levels and higher PKG activities compared with the sitter variants of for (for s ) (Osb...

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“…The only neurons for which both axonal and dendritic morphologies have been examined in dfmr1 mutants are those of the mushroom bodies, a brain region well known for its role in many forms of associative learning and memory [Zars, 2000;Roman and Davis, 2001;Heisenberg, 2003]. Carlos Michel and Robert Kraft in my lab found a specific developmental defect during the metamorphic transition [Michel et al, 2004], when hundreds of mushroom body ␣/␤ neurons are born and differentiate .…”

Section: Case In Point: Drosophila Fragile X Mental Retardation 1 (Dfmentioning

confidence: 99%

Mental retardation genes in drosophila: New approaches to understanding and treating developmental brain disorders

Restifo

2005

Ment. Retard. Dev. Disabil. Res. Rev.

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Drosophila melanogaster is emerging as a valuable genetic model system for the study of mental retardation (MR). MR genes are remarkably similar between humans and fruit flies. Cognitive behavioral assays can detect reductions in learning and memory in flies with mutations in MR genes. Neuroanatomical methods, including some at single-neuron resolution, are helping to reveal the cellular bases of faulty brain development caused by MR gene mutations. Drosophila fragile X mental retardation 1 (dfmr1) is the fly counterpart of the human gene whose malfunction causes fragile X syndrome. Research on the fly gene is leading the field in molecular mechanisms of the gene product's biological function and in pharmacological rescue of brain and behavioral phenotypes. Future work holds the promise of using genetic pathway analysis and primary neuronal culture methods in Drosophila as tools for drug discovery for a wide range of MR and related disorders.

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Behavioral functions of the insect mushroom bodies

Cited by 174 publications

References 47 publications

Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila

Oviposition preference for and positional avoidance of acetic acid provide a model for competing behavioral drives in Drosophila

Natural variation in Drosophila larval reward learning and memory due to a cGMP-dependent protein kinase

Mental retardation genes in drosophila: New approaches to understanding and treating developmental brain disorders

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