The role of the Drosophila lateral horn in olfactory information processing and behavioral response

Schultzhaus, Janna N.; Saleem, Sehresh; Iftikhar, Hina; Carney, Ginger E.

doi:10.1016/j.jinsphys.2016.11.007

Cited by 49 publications

(39 citation statements)

References 92 publications

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“…Although we have not tested an exhaustive panel of odorants, our work to date suggests that visual valence reversal is mediated by appetitive but not aversive odors, a result that provides key insight into the putative organization of olfactory inputs to OA neuromodulation. In the Drosophila olfactory system, diverse lines of evidence suggest that attractive and aversive odorants are encoded by anatomically segregated pathways that reside within subdomains of hierarchical olfactory neuropils (Grabe and Sachse, 2018;Masse et al, 2009;Sachse and Beshel, 2016;Schultzhaus et al, 2017) . Our finding that the observed odor-induced visual valence reversal takes place only in the presence of attractive odorants (ACV and EtOH, Figure 1F & 2B) and not aversive odorants (BA, Figure 2C) specifically implicates the attractive olfactory pathway (Masse et al, 2009;Sachse and Beshel, 2016;Strutz et al, 2014) .…”

Section: Odor-activated Visual Valence Reversal Is Rapid and Odor-valmentioning

confidence: 99%

Section: Odor-activated Visual Valence Reversal Is Rapid and Odor-valmentioning

confidence: 99%

“…Another third-order olfactory neuropil, the lateral horn (LH), mediates olfactory behaviors in a rapid, experience-independent manner (Fişek and Wilson, 2014;Grabe and Sachse, 2018;Sachse and Beshel, 2016;Schultzhaus et al, 2017) . This neuropil houses neurons that encode odor features such as hedonic valence and odor intensity (Grabe and Sachse, 2018;Sachse and Beshel, 2016;Schultzhaus et al, 2017) . LH projection neurons innervate the superior medial protocerebrum (SMP), superior lateral protocerebrum (SLP), and the ventral nerve cord (VNC) (Dolan et al, 2018;Fişek and Wilson, 2014;Jefferis et al, 2007;Sachse et al, 2007;Tanaka et al, 2012Tanaka et al, , 2004 .…”

Section: Odor-activated Visual Valence Reversal Is Rapid and Odor-valmentioning

confidence: 99%

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Olfactory and neuromodulatory signals reverse visual object avoidance to approach in Drosophila

Cheng

Frye

2018

Preprint

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Innate behavioral reactions to sensory stimuli may be subject to modulation by contextual conditions including signals from other modalities. Whereas sensory processing by individual modalities has been well-studied, the cell circuit mechanisms by which signals from different sensory systems are integrated to control behavior remains poorly understood. Here, we provide a new behavioral model to study the mechanisms of multisensory integration. This behavior, which we termed odor-induced visual valence reversal, occurs when the innate avoidance response to a small moving object by flying Drosophila melanogaster is reversed by the presence of an appetitive odor. Instead of steering away from the small object representing an approaching threat, flies begin to steer towards the object in the presence of odor. Odor-induced visual valence reversal occurs rapidly without associative learning and occurs for attractive odors including apple cider vinegar and ethanol, but not for innately aversive benzaldehyde. Optogenetic activation of octopaminergic neurons robustly induces visual valence reversal in the absence of odor, as does optogenetic activation of directional columnar motion detecting neurons that express octopamine receptors. Optogenetic activation of octopamine neurons drives calcium responses in the motion detectors. Taken together, our results implicate a multisensory processing cascade in which appetitive odor activates octopaminergic neuromodulation of visual pathways, which leads to increased visual saliency and the switch from avoidance to approach toward a small visual object.

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Section: Odor-activated Visual Valence Reversal Is Rapid and Odor-valmentioning

confidence: 99%

Section: Odor-activated Visual Valence Reversal Is Rapid and Odor-valmentioning

confidence: 99%

Section: Odor-activated Visual Valence Reversal Is Rapid and Odor-valmentioning

confidence: 99%

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Olfactory and neuromodulatory signals reverse visual object avoidance to approach in Drosophila

Cheng

Frye

2018

Preprint

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“…After training, flies showed significantly stronger avoidance to OCT in the subsequent single-odor test (2-way ANOVA, F (1, 28) = 0.21, P > .05, n = 8 for all groups; Bonferroni post-tests, P < .001) (Figure 5B), suggesting that they had learned to associate OCT with electric shock. The odor avoidance after training represented the comprehensive result of the interaction between innate odor avoidance and learned odor avoidance [49][50][51]. When background 60 V ES was delivered to both sides of the T-maze, the odor avoidance of the trained flies was significantly diminished (Bonferroni post-tests, P < .001, n = 8) (Figure 5B).…”

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confidence: 99%

The interruptive effect of electric shock on odor response requires mushroom bodies in Drosophila melanogaster

Song

Zhao

Tao

et al. 2018

Genes Brain and Behavior

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Nociceptive stimulus involuntarily interrupts concurrent activities. This interruptive effect is related to the protective function of nociception that is believed to be under stringent evolutionary pressure. To determine whether such interruptive effect is conserved in invertebrate and potentially uncover underlying neural circuits, we examined Drosophila melanogaster. Electric shock (ES) is a commonly used nociceptive stimulus for nociception related research in Drosophila. Here, we showed that background noxious ES dramatically interrupted odor response behaviors in a T-maze, which is termed blocking odor response by electric shock (BOBE). The interruptive effect is not odor specific. ES could interrupt both odor avoidance and odor approach. To identify involved brain areas, we focused on the odor avoidance to 3-OCT. By spatially abolishing neurotransmission with temperature sensitive Shibire , we found that mushroom bodies (MBs) are necessary for BOBE. Among the 3 major MB Kenyon cell (KCs) subtypes, α/β neurons and γ neurons but not α'/β' neurons are required for normal BOBE. Specifically, abolishing the neurotransmission of either α/β surface (α/β ), α/β core (α/β ) or γ dorsal (γ ) neurons alone is sufficient to abrogate BOBE. This pattern of MB subset requirement is distinct from that of aversive olfactory learning, indicating a specialized BOBE pathway. Consistent with this idea, BOBE was not diminished in several associative memory mutants and noxious ES interrupted both innate and learned odor avoidance. Overall, our results suggest that MB α/β and γ neurons are parts of a previously unappreciated central neural circuit that processes the interruptive effect of nociception.

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“…The innate attraction to these specific olfactory cues is potentially mediated by neurons in the lateral horn. In fruit flies, these cells are known to encode odour valence (Schultzhaus, Saleem, Iftikhar, & Carney, 2017;Strutz et al, 2014) and specifically underly innate attraction or aversion to behaviourally highly relevant odours (Jefferis et al, 2007). The Bogong moth lateral horn is therefore an interesting target region for physiological and genetic studies that aim at understanding the mechanisms underlying the final segment of their migration -the short distance search for their aestivation caves.…”

Section: Mushroom Bodiesmentioning

confidence: 99%

The brain of a nocturnal migratory insect, the Australian Bogong moth

Adden

Wibrand

Pfeiffer

et al. 2019

Preprint

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Every year, millions of Australian Bogong moths (Agrotis infusa) complete an astonishing journey: in spring, they migrate from their breeding grounds to the alpine regions of the Snowy Mountains, where they endure the hot summer in the cool climate of alpine caves. In autumn, the moths return to their breeding grounds, where they mate, lay eggs and die. Each journey can be over 1000 km long and each moth generation completes the entire roundtrip. Without being able to learn any aspect of this journey from experienced individuals, these moths can use visual cues in combination with the geomagnetic field to guide their flight. How these cues are processed and integrated in the brain to drive migratory behaviour is as yet unknown. Equally unanswered is the question of how these insects identify their targets, i.e. specific alpine caves used as aestivation sites over many generations. To generate an access point for functional studies aiming at understanding the neural basis of these insect's nocturnal migrations, we provide a detailed description of the Bogong moth's brain. Based on immunohistochemical stainings against synapsin and serotonin (5HT), we describe the overall layout as well as the fine structure of all major neuropils, including all regions that have previously been implicated in compass-based navigation. The resulting average brain atlas consists of 3D reconstructions of 25 separate neuropils, comprising the most detailed account of a moth brain to date. Our results show that the Bogong moth brain follows the typical lepidopteran ground pattern, with no major specializations that can be attributed to their spectacular migratory lifestyle. Comparison to the brain of the migratory Monarch butterfly revealed nocturnal versus diurnal lifestyle and phylogenetic identity as the dominant parameters determining large-scale neuroarchitecture. These findings suggest that migratory behaviour does not require widespread modifications of brain structure, but might be achievable via small adjustments of neural circuitry in key brain areas. Locating these subtle changes will be a challenging task for the future, for which our study provides an essential anatomical framework.

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The role of the Drosophila lateral horn in olfactory information processing and behavioral response

Cited by 49 publications

References 92 publications

Olfactory and neuromodulatory signals reverse visual object avoidance to approach in Drosophila

Olfactory and neuromodulatory signals reverse visual object avoidance to approach in Drosophila

The interruptive effect of electric shock on odor response requires mushroom bodies in Drosophila melanogaster

The brain of a nocturnal migratory insect, the Australian Bogong moth

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