Diverse populations of local interneurons integrate into the Drosophila adult olfactory circuit

Liou, Nan-Fu; Lin, Shih Han; Chen, Ying Jun; Tsai, Kuo Ting; Yang, Chi Jen; Lin, Tzi Yang; Wu, Ting Han; Lin, Hsin Ju; Chen, Yuh Tarng; Gohl, Daryl M.; Silies, Marion; Chou, Ya-Hui

doi:10.1038/s41467-018-04675-x

Cited by 30 publications

(44 citation statements)

References 68 publications

(68 reference statements)

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“…We show that serotonergic signals from CSD are used to shift the relative activity of an mPN pathway that mediates odor repulsion and an uPN pathway that mediates attraction. A small number of glutamatergic local interneurons also connects in different ways to these two sets of projection neurons (Olsen and Wilson, 2008;Liou et al, 2018). Using both this local glutamatergic inhibition as well as serotonergic modulation, CSD shifts the relative activation of the mPN and uPN pathways by state-dependent regulation.…”

Section: Introductionmentioning

confidence: 99%

Internal state configures olfactory behavior and early sensory processing inDrosophilalarvae

Vogt

Zimmerman

Schlichting

et al. 2020

Preprint

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Animals can respond differently to a sensory cue when in different states. Here, we show that certain odors repel well-fed Drosophila larvae but attract food-deprived larvae and how feeding state flexibly alters neural processing in an early olfactory circuit, the antennal lobe, to determine the behavioral valence of a sensory cue. Odor valence is assigned by a neuronal architecture that controls a switch between two separate projection neuron output pathways that mediate opposite behavioral responses. A uniglomerular projection neuron pathway mediates odor attraction whereas a multiglomerular projection neuron pathway mediates odor repulsion. The serotonergic CSD neuron in the antennal lobe is a critical regulator of this neuronal and behavioral switch. CSD selects an appropriate behavior by shifting patterns of serotonergic modulation and glutamatergic inhibition onto each output pathway. The antennal lobe is a decision-making circuit for innate behavioral responses that uses feeding state to determine an odor's valence.

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Section: Introductionmentioning

confidence: 99%

Internal state configures olfactory behavior and early sensory processing inDrosophilalarvae

Vogt

Zimmerman

Schlichting

et al. 2020

Preprint

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“…These animals have been studied for their inhibitory synaptic structure or function between bilateralized olfactory systems. The local interneurons of Drosophila are connected across the interbulbar glomeruli and modulate olfactory information between the left and right hemispheres using inhibitory neurotransmitters and neuropeptides [37–39]. The olfactory system of C. elegans has no structure like the glomerulus but has interneurons, such as AIA and AIB, with inhibitory synaptic connections that integrate signals from bilateral primary olfactory neurons [40,41].…”

Section: Discussionmentioning

confidence: 99%

Interhemispheric asymmetry of c‐Fos expression in glomeruli and the olfactory tubercle following repeated odor stimulation

et al. 2020

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Odor adaptation allows the olfactory system to regulate sensitivity to different stimulus intensities, which is essential for preventing saturation of the cell‐transducing machinery and maintaining high sensitivity to persistent and repetitive odor stimuli. Although many studies have investigated the structure and mechanisms of the mammalian olfactory system that responds to chemical sensation, few studies have considered differences in neuronal activation that depend on the manner in which the olfactory system is exposed to odorants, or examined activity patterns of olfactory‐related regions in the brain under different odor exposure conditions. To address these questions, we designed three different odor exposure conditions that mimicked diverse odor environments and analyzed c‐Fos‐expressing cells (c‐Fos+ cells) in the odor columns of the olfactory bulb (OB). We then measured differences in the proportions of c‐Fos‐expressing cell types depending on the odor exposure condition. Surprisingly, under the specific odor condition in which the olfactory system was repeatedly exposed to the odorant for 1 min at 5‐min intervals, one of the lateral odor columns and the ipsilateral hemisphere of the olfactory tubercle had more c‐Fos+ cells than the other three odor columns and the contralateral hemisphere of the olfactory tubercle. However, this interhemispheric asymmetry of c‐Fos expression was not observed in the anterior piriform cortex. To confirm whether the anterior olfactory nucleus pars externa (AONpE), which connects the left and right OB, contributes to this asymmetry, AONpE‐lesioned mice were analyzed under the specific odor exposure condition. Asymmetric c‐Fos expression was not observed in the OB or the olfactory tubercle. These data indicate that the c‐Fos expression patterns of the olfactory‐related regions in the brain are influenced by the odor exposure condition and that asymmetric c‐Fos expression in these regions was observed under a specific odor exposure condition due to synaptic linkage via the AONpE.

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“…These cells are likely to be LNs, based upon their expression of Elav ( Figure S3B) and presence of stained processes that innervate the antennal lobe but do not project to higher olfactory centers. Numerous LN subtypes exist, and these often have broad innervation patterns across many glomeruli 59,60 . To examine the specific contribution of OSNs to the Fmi immunoreactivity observed in the antennal lobe, we depleted Fmi in LNs by RNAi using a combination of Gal4 drivers (1081-Gal4 and 449-Gal4 60 ) that cover the vast majority of these interneurons ( Figure S3C).…”

Section: Pdm3 Acts As a Genetic Switch To Distinguish Ir75a And Ir75bmentioning

confidence: 99%

Targeted molecular profiling of rare cell populations identifies olfactory sensory neuron fate and wiring determinants

Arguello

Abuin

Armida

et al. 2020

Preprint

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AbstractDetermining the molecular properties of neurons is essential to understand their development, function and evolution. We used Targeted DamID (TaDa) to characterize RNA polymerase II occupancy and chromatin accessibility in selected Ionotropic Receptor (IR)-expressing sensory neurons in the Drosophila antenna. Although individual populations represent a minute fraction of cells, TaDa is sufficiently sensitive and specific to identify the expected receptor genes. Unique Ir expression is not linked to substantial differences in chromatin accessibility, but rather to distinct transcription factor profiles. Heterogeneously-expressed genes across populations are enriched for neurodevelopmental factors, and we identify functions for the POU-domain protein Pdm3 as a genetic switch of Ir neuron fate, and the atypical cadherin Flamingo in segregation of neurons into discrete glomeruli. Together this study reveals the effectiveness of TaDa in profiling rare neural populations, identifies new roles for a transcription factor and a neuronal guidance molecule, and provides valuable datasets for future exploration.

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Diverse populations of local interneurons integrate into the Drosophila adult olfactory circuit

Cited by 30 publications

References 68 publications

Internal state configures olfactory behavior and early sensory processing inDrosophilalarvae

Internal state configures olfactory behavior and early sensory processing inDrosophilalarvae

Interhemispheric asymmetry of c‐Fos expression in glomeruli and the olfactory tubercle following repeated odor stimulation

Targeted molecular profiling of rare cell populations identifies olfactory sensory neuron fate and wiring determinants

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