Convergence of monosynaptic and polysynaptic sensory paths onto common motor outputs in a Drosophila feeding connectome

Miroschnikow, Anton; Schlegel, Philipp; Schoofs, Andreas; Hueckesfeld, Sebastian; Li, Feng; Schneider-Mizell, Casey M; Fetter, Richard D.; Truman, James W.; Cardona, Albert; Pankratz, Michael J.

doi:10.7554/elife.40247

Cited by 69 publications

(87 citation statements)

References 69 publications

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“…The emerging Drosophila larval connectome of about 10.000 neurons illustrates that sensory networks fan out extensively, adding numerous partners at each subsequent level (14,23,53). As a result, an unambiguous output path of any given sensory input is often difficult to identify, indicating that physical connection is not a sufficient predictor for function (17,54).…”

Section: Discussionmentioning

confidence: 99%

Discrete escape responses are generated by neuropeptide-mediated circuit logic

Imambocus

Wittich

Tenedini

et al. 2020

Preprint

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Animals display a plethora of escape behaviors when faced with environmental threats. Selection of the appropriate response by the underlying neuronal network is key to maximize chances of survival. We uncovered a somatosensory network in Drosophila larvae that encodes two escape behaviors through input-specific neuropeptide action. Sensory neurons required for avoidance of noxious light and escape in response to harsh touch, each converge on discrete domains of the same neuromodulatory hub neurons. These gate harsh touch responses via short Neuropeptide F, but noxious light avoidance via compartmentalized, acute Insulin-like peptide 7 action and cognate Relaxin-family receptor signaling in connected downstream neurons. Peptidergic hub neurons can thus act as central circuit elements for first order processing of converging sensory inputs to gate specific escape responses.

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Section: Discussionmentioning

confidence: 99%

Discrete escape responses are generated by neuropeptide-mediated circuit logic

Imambocus

Wittich

Tenedini

et al. 2020

Preprint

Self Cite

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“…Preferential connectivity of JONs within a particular subpopulation has also been shown with the JO-A and -B neurons (Kim et al, 2020). This type of connectivity among sensory neurons is an emerging theme that is increasingly being described in sensory neurons across modalities (Horne et al, 2018;Marin et al, 2020;Miroschnikow et al, 2018;Tobin et al, 2017). However, the functional significance of this type of connectivity remains unclear.…”

Section: Jon Axons Make Synaptic Connections With Each Othermentioning

confidence: 96%

Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Hampel

Eichler

Yamada

et al. 2020

Preprint

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Diverse subpopulations of mechanosensory neurons detect different mechanical forces and influence behavior. How these subpopulations connect with central circuits to influence behavior remains an important area of study. We previously discovered a neural circuit that elicits grooming of the Drosophila melanogaster antennae that is activated by an antennal mechanosensory chordotonal organ, the Johnston's organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations and define how they interface with the circuit that elicits antennal grooming. We show that the subpopulations project to distinct zones in the brain and differ in their responses to mechanical stimulation of the antennae. Each subpopulation elicits grooming through direct synaptic connections with a single interneuron in the circuit, the dendrites of which span the different mechanosensory afferent projection zones. Thus, distinct JO subpopulations converge onto the same neural circuit to elicit a common behavioral response.The fruit fly (Drosophila melanogaster) Johnston's organ (JO) is a chordotonal organ in the antennae that can be studied to address this outstanding question. The JO detects diverse types of subpopulations are each known to consist of morphologically heterogeneous JON types that have not been completely described (Kamikouchi et al., 2006), we first define their morphological diversity by reconstructing major portions of each subpopulation from an EM volume of the fly brain (Zheng et al., 2018). We next produce transgenic driver lines that selectively target expression in each subpopulation. These lines enable us to visualize the distribution of the different subpopulations in the antennae and determine that they respond differently to mechanical stimuli. Optogenetic activation experiments confirm our previous finding that each JON subpopulation can elicit grooming of the antennae (Hampel et al., 2015). However, we report here that one of the subpopulations also elicits an avoidance response, whereas the other elicits wing flapping movements. Finally, by employing EM reconstructions and functional imaging experiments, we determine that JONs within each subpopulation are synaptically and functionally connected with the antennal command circuit through the same interneuron (aBN1). These results provide a comprehensive description of the topography of the JO, and reveal how different JON subpopulations whose projections occupy different points in topographical space can converge on the same neural circuit to elicit a similar behavioral response. Results and discussion Electron microscopy-based reconstruction of different JON subpopulationsWe first sought to define the morphological diversity of the neurons within each JON subpopulation as a prerequisite for understanding how the subpopulations interface with the antennal command circuit. JONs project from the antennae through the antennal nerve into a region of the SEZ called the antennal mechanosensory and motor ce...

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“…Circuit convergence, divergence, and re-convergence can be found throughout the nervous systems of both invertebrates and vertebrates and plays a pivotal role in providing behavioral flexibility (Eschbach et al, 2020;Jeanne and Wilson, 2015;Man et al, 2013;Miroschnikow et al, 2018;Misic et al, 2014;Ohyama et al, 2015). Given the importance of the MBONs in driving behavioral choice, we first sought to reveal patterns of divergence and convergence by identifying the postsynaptic connections of the MBONs innervating each of the 15 MB compartments using trans-Tango.…”

Section: Divergence and Convergence Of The Mbons Circuitsmentioning

confidence: 99%

Transsynaptic mapping ofDrosophilamushroom body output neurons

Scaplen

Talay

Fisher

et al. 2020

Preprint

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The Mushroom Body (MB) is a well-characterized associative memory structure within the Drosophila brain. Although previous studies have analyzed MB connectivity and provided a map of inputs and outputs, a detailed map of the downstream targets is missing. Using the genetic anterograde transsynaptic tracing tool, trans-Tango, we identified divergent projections across the brain and convergent downstream targets of the MB output neurons (MBONs). Our analysis revealed at least three separate targets that receive convergent input from MBONs: other MBONs, the fan shaped body (FSB), and the lateral accessory lobe (LAL). We describe, both anatomically and functionally, a multilayer circuit in which inhibitory and excitatory MBONs converge on the same genetic subset of FSB and LAL neurons. This circuit architecture provides an opportunity for the brain to update information and integrate it with previous experience before executing appropriate behavioral responses.

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Convergence of monosynaptic and polysynaptic sensory paths onto common motor outputs in a Drosophila feeding connectome

Cited by 69 publications

References 69 publications

Discrete escape responses are generated by neuropeptide-mediated circuit logic

Discrete escape responses are generated by neuropeptide-mediated circuit logic

Convergence of distinct subpopulations of mechanosensory neurons onto a neural circuit that elicits grooming

Transsynaptic mapping ofDrosophilamushroom body output neurons

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