Sequential addition of neuronal stem cell temporal cohorts generates a feed-forward circuit in the Drosophila larval nerve cord

Wang, Yiwen; Wreden, Chris C; Levy, Maayan; Meng, Julia L; Marshall, Zarion D; MacLean, Jason N.; Heckscher, Ellie S.

doi:10.7554/elife.79276

Cited by 4 publications

(3 citation statements)

References 59 publications

(178 reference statements)

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“…Brain input neurons (Fig. 1F) comprise two broad classes: 1) sensory neurons (SNs) with axons in the brain; many were reconstructed and characterized previously (45)(46)(47)61), and 2) ascending neurons (ANs) that transmit somatosensory signals from the VNC; several were previously reconstructed (38,41,44,(62)(63)(64). We reconstructed an additional set of A1 ANs, resulting in the most complete set of ANs from a nerve cord segment (A1) to date (Fig.…”

Section: Identification Of All Brain Input Neurons Interneurons and O...mentioning

confidence: 99%

The connectome of an insect brain

Winding

Pedigo

Barnes

et al. 2022

Preprint

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Brains contain networks of interconnected neurons, so knowing the network architecture is essential for understanding brain function. We therefore mapped the synaptic-resolution connectome of an insect brain (Drosophilalarva) with rich behavior, including learning, value-computation, and action-selection, comprising 3,013 neurons and 544,000 synapses. We characterized neuron-types, hubs, feedforward and feedback pathways, and cross-hemisphere and brain-nerve cord interactions. We found pervasive multisensory and interhemispheric integration, highly recurrent architecture, abundant feedback from descending neurons, and multiple novel circuit motifs. The brain's most recurrent circuits comprised the input and output neurons of the learning center. Some structural features, including multilayer shortcuts and nested recurrent loops, resembled powerful machine learning architectures. The identified brain architecture provides a basis for future experimental and theoretical studies of neural circuits.

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Section: Identification Of All Brain Input Neurons Interneurons and O...mentioning

confidence: 99%

The connectome of an insect brain

Winding

Pedigo

Barnes

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…To confirm the identities of unpublished neurons, we compared their morphology to light level examples ( Merritt and Whitington, 1995 ; Schrader and Merritt, 2000 ; Grueber et al, 2002 , 2007 ). For details of matching neurons in light-level data, see both Wreden et al (2017) and Wang et al (2022) . In addition, we compared each neuron in other segments to the A1 example of the same name and to its left-right hemisegment sister neuron.…”

Section: Methodsmentioning

confidence: 99%

Distinctive features of the central synaptic organization of Drosophila larval proprioceptors

Greaney¹,

Wreden²,

Heckscher³

2023

Front. Neural Circuits

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Proprioceptive feedback is critically needed for locomotor control, but how this information is incorporated into central proprioceptive processing circuits remains poorly understood. Circuit organization emerges from the spatial distribution of synaptic connections between neurons. This distribution is difficult to discern in model systems where only a few cells can be probed simultaneously. Therefore, we turned to a relatively simple and accessible nervous system to ask: how are proprioceptors’ input and output synapses organized in space, and what principles underlie this organization? Using the Drosophila larval connectome, we generated a map of the input and output synapses of 34 proprioceptors in several adjacent body segments (5–6 left-right pairs per segment). We characterized the spatial organization of these synapses, and compared this organization to that of other somatosensory neurons’ synapses. We found three distinguishing features of larval proprioceptor synapses: (1) Generally, individual proprioceptor types display segmental somatotopy. (2) Proprioceptor output synapses both converge and diverge in space; they are organized into six spatial domains, each containing a unique set of one or more proprioceptors. Proprioceptors form output synapses along the proximal axonal entry pathway into the neuropil. (3) Proprioceptors receive few inhibitory input synapses. Further, we find that these three features do not apply to other larval somatosensory neurons. Thus, we have generated the most comprehensive map to date of how proprioceptor synapses are centrally organized. This map documents previously undescribed features of proprioceptors, raises questions about underlying developmental mechanisms, and has implications for downstream proprioceptive processing circuits.

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“…Our findings reveal that multiple lineages participate in building a complex circuit. Drosophila larval ventral nerve cord cohorts were shown to be formed by sequential addition from different lineages over time, where circuit input neurons are born prior to the output neurons 97 .…”

Section: Lineage Specific Development Of CX Neuron Typesmentioning

confidence: 99%

The RNA-binding protein, Imp specifies olfactory navigation circuitry and behavior inDrosophila

Hamid,

Gattuso,

Caglar

et al. 2023

Preprint

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Complex behaviors depend on the precise developmental specification of neuronal circuits, but the relationship between genetic programs for neural development, circuit structure, and behavioral output is often unclear. The central complex (CX) is a conserved sensory-motor integration center in insects that governs many higher-order behaviors and largely derives from a small number of Type II neural stem cells. Here, we show that Imp, a conserved IGF-II mRNA-binding protein expressed in Type II neural stem cells, specifies components of CX olfactory navigation circuitry. We show: (1) that multiple components of olfactory navigation circuitry arise from Type II neural stem cells and manipulating Imp expression in Type II neural stem cells alters the number and morphology of many of these circuit elements, with the most potent effects on neurons targeting the ventral layers of the fan-shaped body. (2) Imp regulates the specification of Tachykinin expressing ventral fan-shaped body input neurons. (3) Imp in Type II neural stem cells alters the morphology of the CX neuropil structures. (4) Loss of Imp in Type II neural stem cells abolishes upwind orientation to attractive odor while leaving locomotion and odor-evoked regulation of movement intact. Taken together, our work establishes that a single temporally expressed gene can regulate the expression of a complex behavior through the developmental specification of multiple circuit components and provides a first step towards a developmental dissection of the CX and its roles in behavior.

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Sequential addition of neuronal stem cell temporal cohorts generates a feed-forward circuit in the Drosophila larval nerve cord

Cited by 4 publications

References 59 publications

The connectome of an insect brain

The connectome of an insect brain

Distinctive features of the central synaptic organization of Drosophila larval proprioceptors

The RNA-binding protein, Imp specifies olfactory navigation circuitry and behavior inDrosophila

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