The role of lineage, hemilineage and temporal identity in establishing neuronal connectivity in the Drosophila larval CNS

Mapping Intimacies ◽

10.1101/617936 ◽

2019 ◽

Cited By ~ 2

Author(s):

Brandon Mark ◽

Sen-Lin Lai ◽

Aref Arzan Zarin ◽

Laurina Manning ◽

Albert Cardona ◽

...

Keyword(s):

Sensory Processing ◽

Neural Circuit ◽

Neuronal Morphology ◽

Neural Progenitors ◽

Neuronal Diversity ◽

Developmental Mechanism ◽

Temporal Identity ◽

Circuit Formation ◽

Synapse Targeting

AbstractThe mechanisms specifying neuronal diversity are well-characterized, yet it remains unclear how or if these mechanisms regulate neuronal morphology and connectivity. Here we map the developmental origin of 78 bilateral pairs of interneurons from seven identified neural progenitors (neuroblasts) within a complete TEM reconstruction of the Drosophila newly-hatched larval CNS. This allows us to correlate developmental mechanism with neuronal projections, synapse targeting, and connectivity. We find that clonally-related neurons from project widely in the neuropil, without preferential circuit formation. In contrast, the two NotchON/NotchOFF hemilineages from each neuroblast project to either dorsal motor neuropil (NotchON) or ventral sensory neuropil (NotchOFF). Thus, each neuroblast contributes both motor and sensory processing neurons. Lineage-specific constitutive Notch transforms sensory to motor hemilineages, showing hemilineage identity determines neuronal targeting. Within a hemilineage, temporal cohorts target processes and synapses to different sub-domains of the neuropil, effectively “tiling” the hemilineage neuropil, and hemilineage/temporal cohorts are enriched for shared connectivity. Thus, neuroblast lineage, hemilineage, and temporal identity progressively restrict neuropil targeting, synapse localization, and connectivity. We propose that mechanisms generating neural diversity are also determinants of neural circuit formation.

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A developmental framework linking neurogenesis and circuit formation in the Drosophila CNS

eLife ◽

10.7554/elife.67510 ◽

2021 ◽

Vol 10 ◽

Author(s):

Brandon Mark ◽

Sen-Lin Lai ◽

Aref Arzan Zarin ◽

Laurina Manning ◽

Heather Q Pollington ◽

...

Keyword(s):

Nervous System ◽

Neural Circuit ◽

Neural Progenitors ◽

Dependent Manner ◽

Neuronal Diversity ◽

Synaptic Targeting ◽

Connectivity Structure ◽

Temporal Identity ◽

And Function ◽

Circuit Formation

The mechanisms specifying neuronal diversity are well-characterized, yet it remains unclear how or if these mechanisms regulate neural circuit assembly. To address this, we mapped the developmental origin of 160 interneurons from seven bilateral neural progenitors (neuroblasts), and identify them in a synapse-scale TEM reconstruction of the Drosophila larval CNS. We find that lineages concurrently build the sensory and motor neuropils by generating sensory and motor hemilineages in a Notch-dependent manner. Neurons in a hemilineage share common synaptic targeting within the neuropil, which is further refined based on neuronal temporal identity. Connectome analysis shows that hemilineage-temporal cohorts share common connectivity. Finally, we show that proximity alone cannot explain the observed connectivity structure, suggesting hemilineage/temporal identity confers an added layer of specificity. Thus, we demonstrate that the mechanisms specifying neuronal diversity also govern circuit formation and function, and that these principles are broadly applicable throughout the nervous system.

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Role of microRNAs in Semaphorin function and neural circuit formation

Seminars in Cell and Developmental Biology ◽

10.1016/j.semcdb.2012.11.004 ◽

2013 ◽

Vol 24 (3) ◽

pp. 146-155 ◽

Cited By ~ 12

Author(s):

Marie-Laure Baudet ◽

Anaïs Bellon ◽

Christine E. Holt

Keyword(s):

Neural Circuit ◽

Circuit Formation

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The Hunchback temporal transcription factor determines motor neuron axon and dendrite targeting in Drosophila

10.1101/554188 ◽

2019 ◽

Cited By ~ 1

Author(s):

Austin Q. Seroka ◽

Chris Q. Doe

Keyword(s):

Transcription Factor ◽

Motor Neurons ◽

Neuronal Diversity ◽

Molecular Identity ◽

Extrinsic Cues ◽

Circuit Development ◽

Temporal Identity ◽

Morphological Differences ◽

And Behavior ◽

Circuit Formation

AbstractThe generation of neuronal diversity is essential for circuit formation and behavior. Morphological differences in sequentially born neurons could be due to intrinsic molecular identity specified by temporal transcription factors (henceforth called intrinsic temporal identity) or due to changing extrinsic cues. Here we use the Drosophila NB7-1 lineage to address this question. NB7-1 sequentially generates the U1-U5 motor neurons; each has a distinct intrinsic temporal identity due to inheritance of a different temporal transcription factor at time of birth. Here we show that the U1-U5 neurons project axons sequentially, followed by sequential dendrite extension. We misexpress the earliest temporal transcription factor, Hunchback, to create “ectopic” U1 neurons with an early intrinsic temporal identity but later birth-order. These ectopic U1 neurons have axon muscle targeting and dendrite neuropil targeting consistent with U1 intrinsic temporal identity, rather than their time of birth or differentiation. We conclude that intrinsic temporal identity plays a major role in establishing both motor axon muscle targeting and dendritic arbor targeting, which are required for proper motor circuit development.

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Neurotrophin, p75, and Trk Signaling Module in the Developing Nervous System of the Marine AnnelidPlatynereis dumerilii

BioMed Research International ◽

10.1155/2016/2456062 ◽

2016 ◽

Vol 2016 ◽

pp. 1-12 ◽

Cited By ~ 6

Author(s):

Antonella Lauri ◽

Paola Bertucci ◽

Detlev Arendt

Keyword(s):

Nervous System ◽

Neuronal Development ◽

Neural Circuit ◽

Circuit Development ◽

Circuit Formation ◽

Neurotrophic Signaling ◽

High Degree ◽

Developing Nervous System

In vertebrates, neurotrophic signaling plays an important role in neuronal development, neural circuit formation, and neuronal plasticity, but its evolutionary origin remains obscure. We found and validated nucleotide sequences encoding putative neurotrophic ligands (neurotrophin, NT) and receptors (Trk and p75) in two annelids,Platynereis dumerilii(Errantia) andCapitella teleta(Sedentaria, for which some sequences were found recently by Wilson, 2009). Predicted protein sequences and structures ofPlatynereisneurotrophic molecules reveal a high degree of conservation with the vertebrate counterparts; some amino acids signatures present in the annelid Trk sequences are absent in the basal chordate amphioxus, reflecting secondary loss in the cephalochordate lineage. In addition, expression analysis of NT, Trk, and p75 duringPlatynereisdevelopment by whole-mount mRNAin situhybridization supports a role of these molecules in nervous system and circuit development. These annelid data corroborate the hypothesis that the neurotrophic signaling and its involvement in shaping neural networks predate the protostome-deuterostome split and were present in bilaterian ancestors.

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Role of motoneuron-derived neurotrophin 3 in survival and axonal projection of sensory neurons during neural circuit formation

Development ◽

10.1242/dev.069997 ◽

2012 ◽

Vol 139 (6) ◽

pp. 1125-1132 ◽

Cited By ~ 20

Author(s):

N. Usui ◽

K. Watanabe ◽

K. Ono ◽

K. Tomita ◽

N. Tamamaki ◽

...

Keyword(s):

Sensory Neurons ◽

Neural Circuit ◽

Axonal Projection ◽

Neurotrophin 3 ◽

Circuit Formation

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Trans-Axonal Signaling in Neural Circuit Wiring

International Journal of Molecular Sciences ◽

10.3390/ijms21145170 ◽

2020 ◽

Vol 21 (14) ◽

pp. 5170 ◽

Cited By ~ 1

Author(s):

Olivia Spead ◽

Fabienne E. Poulain

Keyword(s):

Molecular Mechanisms ◽

Neural Circuits ◽

Neural Circuit ◽

Target Selection ◽

Synaptic Connectivity ◽

Recent Advances ◽

Complex Process ◽

Circuit Formation

The development of neural circuits is a complex process that relies on the proper navigation of axons through their environment to their appropriate targets. While axon–environment and axon–target interactions have long been known as essential for circuit formation, communication between axons themselves has only more recently emerged as another crucial mechanism. Trans-axonal signaling governs many axonal behaviors, including fasciculation for proper guidance to targets, defasciculation for pathfinding at important choice points, repulsion along and within tracts for pre-target sorting and target selection, repulsion at the target for precise synaptic connectivity, and potentially selective degeneration for circuit refinement. This review outlines the recent advances in identifying the molecular mechanisms of trans-axonal signaling and discusses the role of axon–axon interactions during the different steps of neural circuit formation.

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Epilogue

10.1093/oso/9780198725022.003.0010 ◽

2018 ◽

Author(s):

Bruno and

Keyword(s):

Sensory Processing ◽

Multisensory Processing ◽

Multisensory Perception ◽

Future Directions ◽

Life Problems ◽

Multisensory Interactions ◽

Contemporary Work ◽

New Perspective

Multisensory interactions in perception are pervasive and fundamental, as we have documented throughout this book. In this final chapter, we propose that contemporary work on multisensory processing is a paradigm shift in perception science, calling for a radical reconsideration of empirical and theoretical questions within an entirely new perspective. In making our case, we emphasize that multisensory perception is the norm, not the exception, and we remark that multisensory interactions can occur early in sensory processing. We reiterate the key notions that multisensory interactions come in different kinds and that principles of multisensory processing must be considered when tackling multisensory daily-life problems. We discuss the role of unisensory processing in a multisensory world, and we conclude by suggesting future directions for the multisensory field.

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Implications of Extended Inhibitory Neuron Development

International Journal of Molecular Sciences ◽

10.3390/ijms22105113 ◽

2021 ◽

Vol 22 (10) ◽

pp. 5113

Author(s):

Jae-Yeon Kim ◽

Mercedes F. Paredes

Keyword(s):

Neural Circuit ◽

Inhibitory Neuron ◽

Postnatal Period ◽

Specific Pattern ◽

Inhibitory Neurons ◽

Gabaergic Interneuron ◽

Gabaergic Interneurons ◽

Neuron Development ◽

Cortical Regions ◽

Circuit Formation

A prolonged developmental timeline for GABA (γ-aminobutyric acid)-expressing inhibitory neurons (GABAergic interneurons) is an amplified trait in larger, gyrencephalic animals. In several species, the generation, migration, and maturation of interneurons take place over several months, in some cases persisting after birth. The late integration of GABAergic interneurons occurs in a region-specific pattern, especially during the early postnatal period. These changes can contribute to the formation of functional connectivity and plasticity, especially in the cortical regions responsible for higher cognitive tasks. In this review, we discuss GABAergic interneuron development in the late gestational and postnatal forebrain. We propose the protracted development of interneurons at each stage (neurogenesis, neuronal migration, and network integration), as a mechanism for increased complexity and cognitive flexibility in larger, gyrencephalic brains. This developmental feature of interneurons also provides an avenue for environmental influences to shape neural circuit formation.

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