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Do fruit flies have emotions?

Two hormones and a neurotransmitter play a crucial role in male fruit fly's courtship or lack thereof....

Using the common fruit fly for their model animal system, UC Riverside scientists identified two hormones and a neurotransmitter that play a crucial role in early fly adulthood. They found how unsuccessful courtship attempts by male fruitflies can create memories that reduce enthusiasm for more attempts. Scientists at the University of California Riverside want to understand this behavior at the molecular level.

In the fruit fly (Drosophila melanogaster), if a courting male is rejected by a mated female, he courts less enthusiastically when with a virgin female. Further exploration revealed the fruit fly's hormonal state is critical to maintenance of "courtship memories."

Their report in Current Biology identified two hormones required for the brain to maintain courtship memories: ecdysis triggering hormone (ETH) and juvenile hormone (JH). Furthermore, researchers noted how dopamine — a neurotransmitter that helps control the brain's reward and pleasure centers — is also crucial. ETH is essential for courtship memory through regulation of JH levels in adult males.
"Memories of prior experiences have an important influence on future behaviors. Our study underscores the underappreciated role of hormonal states in the ability of animals to learn and remember experiences. This hormonal state is maintained by a signaling cascade - a multistep pathway that involves ETH, JH, and dopamine neurons.

The ETH-JH-dopamine signaling cascade operates within the first three days — a critical period during early adulthood which regulates social-context-dependent memories."

Michael Adams PhD, Professor, Department of Cell Biology; Department of Entomology; Neuroscience Graduate Program, University of California, Riverside, Riverside, CA, USA, and research project leader.

In their lab experiments, researchers found that a male fruit fly spurned by a female fruit fly will approach another female only if the JH level is reduced by silencing ETH signaling genes. This interruption causes loss of short-term memory of the previously unsuccessful courtship.
"In the absence of a hormonal signaling cascade, the animal doesn't maintain memory of courtship failure. It rapidly forgets an unsuccessful courtship, and courts at a level it would have in the absence of that failure.

"In the lab, we are able to rescue this memory by applying methoprene, a chemical that mimics JH. Following methoprene treatment, male flies rejected by mated females show normal levels of courtship suppression. This indicates that JH plays a crucial role in maintaining memory."

Sang Soo Lee, Graduate Student, Adams lab, and first author of the paper.

Hormones are organic substances that circulate in the blood stream and are needed for maintaining homeostasis. In insects, ETH stimulates a gland to secrete JH. JH, in turn, acts on dopamine neurons - nerve cells that synthesize and release dopamine - in the brain. During early development, JH is one of the most well studied hormones in insects as it maintains the juvenile state. Present in all insects, male and female, it disappears during metamorphosis only to return when the insect becomes an adult. At that time, JH activates reproductive functions.

JH was discovered in the 1930s. "Although strictly an insect hormone directing JH signaling, it is conserved across a wide range of insect species, and may have signaling functions similar to thyroid hormone in mammals," explains Adams.
"This work raises the question 'what is emotion?' We have male fruit flies experiencing failure in courtship, failure in mating, with negatively modified behavior affecting their subsequent enthusiasm for courtship. This could be viewed as an emotional or stress response to failure."

Michael Adams PhD

Sang Soo Lee explains that in the field of learning and memory, most studies focus on neural circuitry. Only a few successfully show hormones as good modulators of neural circuitry.

"Why would it be adaptive for these hormones to promote maintenance of unpleasant memories?" he asks. "Perhaps as such memories may enhance the male's ability to mate successfully by shifting attention to receptive females — where successful mating is much more likely. In other words, there is no point in wasting valuable time pursuing unreceptive females. In those situations, the hormonal cascade is a good upstream regulator of neural circuitry," he adds. "The cascade operates in females, but its function is different. It influences learning and memory, but also reproductive physiology - egg development and ovulation."

Researchers will next study what role ETH and JH play in the development of long-term memory.
"Evidence is emerging that the same hormones [in males and females] operating through different signaling pathways are involved in long-term memory."

Michael Adams PhD

• ETH-JH cascade in adult males regulates short-term courtship memory retention
• JH is required for retention of memory from pheromone-independent experiences
• The action of JH on memory has an early-adult-specific critical period
• JH targets DA neurons to regulate male courtship memory

Formation and expression of memories are critical for context-dependent decision making. In Drosophila, a courting male rejected by a mated female subsequently courts less avidly when paired with a virgin female, a behavioral modification attributed to “courtship memory.” Here we show the critical role of hormonal state for maintenance of courtship memory. Ecdysis-triggering hormone (ETH) is essential for courtship memory through regulation of juvenile hormone (JH) levels in adult males. Reduction of JH levels via silencing of ETH signaling genes impairs short-term courtship memory, a phenotype rescuable by the JH analog methoprene. JH-deficit-induced memory impairment involves rapid decay rather than failure of memory acquisition. A critical period governs memory performance during the first 3 days of adulthood. Using sex-peptide-expressing “pseudo-mated” trainers, we find that robust courtship memory elicited in the absence of aversive chemical mating cues also is dependent on ETH-JH signaling. Finally, we find that JH acts through dopaminergic neurons and conclude that an ETH-JH-dopamine signaling cascade is required during a critical period for promotion of social-context-dependent memory.

All authors: Sang Soo Lee, Yike Ding, Natalie Karapetians, Crisalejandra Rivera-Perez, Fernando Gabriel Noriega, Michael E. Adams

Keywords: ecdysis triggering hormone, juvenile hormone, dopamine, courtship conditioning, learning.

Adams, Director of the UCR Graduate Neuroscience Program, and Lee were joined in the study by Yike Ding and Natalie Karapetians at UCR; and Crisalejandra Rivera-Perez and Fernando Gabriel Noriega at Florida International University, Miami.

The research was funded by a grant to Adams from the National Institutes of Health. The Agricultural Experiment Station, the Office of Research and Economic Development, and the Graduate Division, all at UC Riverside, provided additional funding.

The University of California, Riverside is a doctoral research university, a living laboratory for groundbreaking exploration of issues critical to Inland Southern California, the state and communities around the world. Reflecting California's diverse culture, UCR's enrollment is now nearly 23,000 students. The campus opened a medical school in 2013 and has reached the heart of the Coachella Valley by way of the UCR Palm Desert Center. The campus has an annual statewide economic impact of more than $1 billion.

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Sep 20, 2017   Fetal Timeline   Maternal Timeline   News   News Archive

A courting male fruit fly (right) rejected by a female subsequently courts less avidly.
Image Credit: Adams lab, UC Riverside

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