Fan-Shaped Body Neurons in the Drosophila Brain Regulate Both Innate and Conditioned Nociceptive Avoidance

Hu, Wantong; Peng, Yiqing; Sun, Jiameng; Zhang, Fang; Zhang, Xuchen; Wang, Lianzhang; Li, Qian; Zhong, Yi

doi:10.1016/j.celrep.2018.07.028

Cited by 43 publications

(62 citation statements)

References 56 publications

(93 reference statements)

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“…Here we have identified one such structure that is an anatomical candidate for pooling MB output activity to drive learned behaviors. Interestingly, although the FSB has an established role in arousal and sleep, more recent work has defined its role in innate and learned nociceptive avoidance further supporting its role in integrating MB output activity (Hu, Peng et al 2018). We hypothesize that output signals from the b2b`2a and a'2 neurons are integrated at the FSB to shift naïve response to cue-directed learned response.…”

Section: Discussionmentioning

confidence: 79%

“…We show that circuits required for formation of alcohol preference shift from population-level dopaminergic encoding to two microcircuits comprising of interconnected dopaminergic, glutamatergic, and cholinergic neurons. These circuits converge onto the fan-shaped body (FSB), a higherorder brain center implicated in arousal and modulating behavioral response (Liu, Seiler et al 2006, Weir, Schnell et al 2014, Weir and Dickinson 2015, Pimentel, Donlea et al 2016, Qian, Cao et al 2017, Donlea, Pimentel et al 2018, Hu, Peng et al 2018, Troup, Yap et al 2018. Our results, therefore, provide an in vivo circuit framework for how drugs of abuse temporally regulate acquisition and expression of sensory memories, which ultimately results in a shift in behavioral response from malleable to inflexible.…”

Section: Introductionmentioning

confidence: 72%

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Circuits that encode and predict alcohol associated preference

Scaplen

Talay

Salamon

et al. 2019

Preprint

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Substance use disorders are chronic relapsing disorders often impelled by enduring memories and persistent cravings. Alcohol, as well as other addictive substances, remolds neural circuits important for memory to establish obstinate preference despite aversive consequences. How pertinent circuits are selected and shaped to result in these unchanging, inflexible memories is unclear. Using neurogenetic tools available in Drosophila melanogaster we define how circuits required for alcohol associated preference shift from population level dopaminergic activation to select dopamine neurons that predict behavioral choice. During memory expression, these dopamine neurons directly, and indirectly via the mushroom body (MB), modulate the activity of interconnected glutamatergic and cholinergic output neurons. Transsynaptic tracing of these output neurons revealed at least two regions of convergence: 1) a center of memory consolidation within the MB implicated in arousal, and 2) a structure outside the MB implicated in integration of naïve and learned responses. These findings provide a circuit framework through which dopamine neuron activation shifts from reward delivery to cue onset, and provides insight into the inflexible, maladaptive nature of alcohol associated memories.

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Section: Discussionmentioning

confidence: 79%

Section: Introductionmentioning

confidence: 72%

Circuits that encode and predict alcohol associated preference

Scaplen

Talay

Salamon

et al. 2019

Preprint

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“…As part of the central complex, the FSB belongs to the main premotor center of the central brain, analogous to the basal ganglia in vertebrates 71 . The central complex itself serves as the main hub, integrating innate and conditioned multisensory information to relay behavioral decisions to the respective downstream effectors 71,72 .…”

Section: Discussionmentioning

confidence: 99%

Differential Role for a Defined Lateral Horn Neuron Subset in Naïve Odor Valence in Drosophila

Lerner

Rozenfeld

Rozenman

et al. 2020

Sci Rep

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Value coding of external stimuli in general, and odor valence in particular, is crucial for survival. In flies, odor valence is thought to be coded by two types of neurons: mushroom body output neurons (MBONs) and lateral horn (LH) neurons. MBONs are classified as neurons that promote either attraction or aversion, but not both, and they are dynamically activated by upstream neurons. This dynamic activation updates the valence values. In contrast, LH neurons receive scaled, but non-dynamic, input from their upstream neurons. It remains unclear how such a non-dynamic system generates differential valence values. Recently, PD2a1/b1 LH neurons were demonstrated to promote approach behavior at low odor concentration in starved flies. Here, we demonstrate that at high odor concentrations, these same neurons contribute to avoidance in satiated flies. The contribution of PD2a1/b1 LH neurons to aversion is context dependent. It is diminished in starved flies, although PD2a1/b1 neural activity remains unchanged, and at lower odor concentration. In addition, PD2a1/b1 aversive effect develops over time. Thus, our results indicate that, even though PD2a1/b1 LH neurons transmit hardwired output, their effect on valence can change. Taken together, we suggest that the valence model described for MBONs does not hold for LH neurons.In order to survive, animals must attach value to external stimuli, be it due to innate or learned behavior. In particular, the ability to accurately evaluate potential food resources is a critical trait for survival. To make such an assessment, animals use many senses, with olfaction often serving as a primary cue. The Drosophila olfactory system resembles that of mammals, including our own, and uses similar principles to decode olfactory information 1,2 . Odors bind to olfactory receptor neurons (ORNs), which are located in the antennae and maxillary palps, where each ORN expresses a single type of odorant receptor (OR) 3-5 . All ORNs expressing the same OR converge onto the same region in the antennal lobe termed the glomerulus 6-8 . Second-order excitatory cholinergic projection neurons (ePNs) have dendrites that are restricted to a single glomerulus, whereas inhibitory GABAergic projection neurons (iPNs) are mostly multiglomerular 9 . Both PN types project to the lateral horn (LH), whereas only ePNs project to the calyx of the mushroom body (MB) 9 . Until recently, associative learning and memory processes were generally believed to occur in the MB, with innate behavior driven by the LH 10,11 . However, although the LH is still believed to contribute greatly to innate behavior, it has become apparent that the rigid functional distinction between the two neuropils cannot be upheld. There is now evidence that the MB also plays a role in some innate olfactory behaviors, mostly attractive 12-14 , while the LH is involved in some forms of associative memory 15 .The LH compartment contains over 1300 cells that are categorized into over 150 types, each with individual morphology 16 . Cells that share mor...

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“…Just as mammalian nociceptors send information to the brain via dorsal horn neurons in the spinal cord (Purves et al 2012), insect nociceptors synapse onto neurons that reach the brain (e.g., larval D. melanogaster; Gerhard et al 2017). Although the entire nociceptive pathway has not yet been delineated in any insect, it is known that nociceptive information is processed in two higher-order integratory areas, the mushroom bodies (Waddell 2013;Konig et al 2018) and the central complex (Hu et al 2018). These two areas are among the most complex in the insect brain, and are key for navigation, learning, memory, and other complex cognitive tasks (Barron and Klein 2016; Kinoshita and Homberg 2017).…”

Section: Neurobiology Of Nociception and Painmentioning

confidence: 99%

“…Not only do mushroom bodies and the fanshaped body have few output neurons, there are no direct connections between them (Pfeiffer and Homberg 2014; Collett and Collett 2018;Hu et al 2018), and they are not in the same hub of interconnected neuropils (Chiang et al 2011;Shih et al 2015). The lack of direct connections between these two important information integration centres in the insect brain raises question about how insects perform cognitive tasks (Collett and Collett 2018).…”

Section: Neurobiology Of Nociception and Painmentioning

confidence: 99%

Is it pain if it does not hurt? On the unlikelihood of insect pain

Adamo

2019

Can Entomol

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Whether insects (Insecta) have the subjective experience of pain is difficult to answer. Recent work in humans demonstrated that the experience of pain occurs due to the activation of a “pain network” that integrates nociceptive sensory information, memory, emotion, cognition, and self-awareness. In humans, the processing of nociceptive sensory information alone does not produce the subjective experience of pain. Insect nociception is processed largely in parallel in two higher-order areas in the brain: the mushroom bodies and the central complex. There is little evidence of a coordinated pain network that would integrate these two areas with each other along with other traits thought to be important for a pain experience in humans. However, it is difficult to exclude the possibility that insects could have a modest pain experience using a less integrated neural circuit. This possibility seems unlikely, however, because even a modest experience would require some neuronal investment. It is unclear whether insects would benefit from such an investment. Recent work in artificial intelligence suggests that relatively simple, cost-efficient circuits can produce adaptive behaviours without subjective experience. Given our current understanding of insect behaviour, neurobiology, and evolution, the likelihood that insects experience pain is low.

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Fan-Shaped Body Neurons in the Drosophila Brain Regulate Both Innate and Conditioned Nociceptive Avoidance

Cited by 43 publications

References 56 publications

Circuits that encode and predict alcohol associated preference

Circuits that encode and predict alcohol associated preference

Differential Role for a Defined Lateral Horn Neuron Subset in Naïve Odor Valence in Drosophila

Is it pain if it does not hurt? On the unlikelihood of insect pain

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