Biology subjects

Shahidi, R.

Publications and source records attributed to Shahidi, R..

8 recordsLinked to original sources

bioRxiv2024

Whole-body connectome of a segmented annelid larva

Nervous systems coordinate effectors across the body during movements. We know little about the cellular-level structure of synaptic circuits for such body-wide control. Here we describe the whole-body synaptic connectome of a segmented larva of the marine annelid Platynereis dumerilii. We reconstructed and annotated over 9,000 neuronal and non-neuronal cells in a whole-body serial electron microscopy dataset. Differentiated cells were classified into 202 neuronal and 92 non-neuronal cell types. We analyse modularity, multisensory integration, left-right and intersegmental connectivity and motor circuits for ciliated cells, glands, pigment cells and muscles. We identify several segment-specific cell types, demonstrating the heteromery of the annelid larval trunk. At the same time, segmentally repeated cell types across the head, the trunk segments and the pygidium suggest the serial homology of all segmental body regions. We also report descending and ascending pathways, peptidergic circuits and a multi-modal mechanosensory girdle. Our work provides the basis for understanding whole-body coordination in an entire segmented animal.

neuroscience↗

bioRxiv2023

A ciliary photoreceptor-cell circuit mediates pressure response in marine zooplankton

Hydrostatic pressure is a dominant environmental cue for vertically migrating marine organisms but the physiological mechanisms of responding to pressure changes remain unclear. Here we uncovered the cellular and circuit bases of a barokinetic response in the planktonic larva of the marine annelid Platynereis dumerilii. Increased pressure induced a rapid, graded and adapting upward swimming response due to the faster beating of cilia in the head multiciliary band. By calcium imaging, we found that brain ciliary photoreceptors showed a graded response to pressure changes. The photoreceptors in animals mutant for ciliary opsin-1 had a smaller sensory compartment and mutant larvae showed diminished pressure responses. The ciliary photoreceptors synaptically connect to the head multiciliary band via serotonergic motoneurons. Genetic inhibition of the serotonergic cells blocked pressure-dependent increases in ciliary beating. We conclude that ciliary photoreceptors function as pressure sensors and activate ciliary beating through serotonergic signalling during barokinesis.

animal behavior and cognition↗

bioRxiv2021

Desmosomal connectomics of all somatic muscles in an annelid larva

Cells form networks in animal tissues through synaptic, chemical and adhesive links. Invertebrate muscle cells often connect to other cells through desmosomes, adhesive junctions anchored by intermediate filaments. To study desmosomal networks, we skeletonised 853 muscle cells and their desmosomal partners in volume electron microscopy data covering an entire larva of the annelid Platynereis. Muscle cells adhere to each other, to epithelial, glial, ciliated, and bristle-producing cells and to the basal lamina, forming a desmosomal connectome of over 2,000 cells. The aciculae - chitin rods that form an endoskeleton in the segmental appendages - are highly connected hubs in this network. This agrees with the many degrees of freedom of their movement, as revealed by video microscopy. Mapping motoneuron synapses to the desmosomal connectome allowed us to infer the extent of tissue influenced by motoneurons. Our work shows how cellular-level maps of synaptic and adherent force networks can elucidate body mechanics.

animal behavior and cognition↗

bioRxiv2020

Whole-animal connectome and cell-type complement of the three-segmented Platynereis dumerilii larva

Nervous systems coordinate effectors across the body during movements. We know little about the cellular-level structure of synaptic circuits for such body-wide control. Here we describe the whole-body synaptic connectome and cell-type complement of a three-segmented larva of the marine annelid Platynereis dumerilii. We reconstructed and annotated over 1,500 neurons and 6,500 non-neuronal cells in a whole-body serial electron microscopy dataset. The differentiated cells fall into 180 neuronal and 90 non-neuronal cell types. We analyse the modular network architecture of the entire nervous system and describe polysynaptic pathways from 428 sensory neurons to four effector systems - ciliated cells, glands, pigment cells and muscles. The complete somatic musculature and its innervation will be described in a companion paper. We also investigated intersegmental differences in cell-type complement, descending and ascending pathways, and mechanosensory and peptidergic circuits. Our work provides the basis for understanding whole-body coordination in annelids.

neuroscience↗

bioRxiv2018

Neural circuitry of a polycystin-mediated hydrodynamic startle response for predator avoidance

Startle responses triggered by aversive stimuli including predators are widespread across animals. These coordinated whole-body actions require the rapid and simultaneous activation of a large number of muscles. Here we study a startle response in a planktonic larva to understand the whole-body circuit implementation of the behavior. Upon encountering water vibrations, larvae of the annelid Platynereis close their locomotor cilia and simultaneously contract the body and raise the parapodia. The startle response is mediated by collar receptor neurons expressing the polycystins PKD1-1 and PKD2-1. CRISPR-generated PKD1-1 and PKD2-1 mutant larvae do not startle and fall prey to a copepod predator at a higher rate. Reconstruction of the whole-body connectome of the collar-receptor-cell circuitry revealed converging feedforward circuits to the ciliary bands and muscles. The wiring diagram suggests circuit mechanisms for the intersegmental and left-right coordination of the response. Our results reveal how polycystin-mediated mechanosensation can trigger a coordinated whole-body effector response involved in predator avoidance.\n\nShort SummaryThe neuronal circuitry of the Platynereis startle response links polycystin-dependent hydrodynamic sensors to muscle and ciliary effector cells

neuroscience↗

bioRxiv2018

Ciliary and rhabdomeric photoreceptor-cell circuits form a spectral depth gauge in marine zooplankton

Ciliary and rhabdomeric photoreceptor cells represent two main lines of photoreceptor evolution in animals. The two photoreceptor-cell types coexist in some animals, however how they functionally integrate is unknown. We used connectomics to map synaptic paths between ciliary and rhabdomeric photoreceptors in the planktonic larva of the annelid Platynereis and found that ciliary photoreceptors are presynaptic to the rhabdomeric circuit. The behaviors mediated by the ciliary and rhabdomeric cells also interact hierarchically. The ciliary photoreceptors are UV-sensitive and mediate downward swimming to non-directional UV light, a behavior absent in ciliary-opsin knockouts. UV avoidance antagonizes positive phototaxis mediated by the rhabdomeric eyes so that vertical swimming direction is determined by the ratio of blue/UV light. Since this ratio increases with depth, Platynereis larvae may use it as a depth gauge during planktonic migration. Our results revealed a functional integration of ciliary and rhabdomeric photoreceptors with implications for eye and photoreceptor evolution.

neuroscience↗

bioRxiv2017

Synaptic and peptidergic connectome of a neurosecretory centre in the annelid brain

Neurosecretory centres in animal brains use peptidergic signalling to influence physiology and behaviour. Understanding neurosecretory centre function requires mapping cell types, synapses, and peptidergic networks. Here we use electron microscopy and gene expression mapping to analyse the synaptic and peptidergic connectome of an entire neurosecretory centre. We mapped 78 neurosecretory neurons in the brain of larval Platynereis dumerilii, a marine annelid. These neurons form an anterior neurosecretory organ expressing many neuropeptides, including hypothalamic peptide orthologues and their receptors. Analysis of peptide-receptor pairs revealed sparsely connected networks linking specific neuronal subsets. We experimentally analysed one peptide-receptor pair and found that a neuropeptide can couple neurosecretory and synaptic brain signalling. Our study uncovered extensive non-synaptic signalling within a neurosecretory centre and its connection to the synaptic brain.

neuroscience↗

bioRxiv2017

Ciliomotor circuitry underlying whole-body coordination of ciliary activity in the Platynereis larva

Ciliated surfaces harbouring synchronously beating cilia can generate fluid flow or drive locomotion. In ciliary swimmers, ciliary beating, arrests, and changes in beat frequency are often coordinated across extended or discontinuous surfaces. To understand how such coordination is achieved, we studied the ciliated larvae of Platynereis dumerilii, a marine annelid. Platynereis larvae have segmental multiciliated cells that regularly display spontaneous coordinated ciliary arrests. We used whole-body connectomics, activity imaging, transgenesis, and neuron ablation to characterize the ciliomotor circuitry. We identified cholinergic, serotonergic, and catecholaminergic ciliomotor neurons. The synchronous rhythmic activation of cholinergic cells drives the coordinated arrests of all cilia. The serotonergic cells are active when cilia are beating. Serotonin inhibits the cholinergic rhythm, and increases ciliary beat frequency. Based on their connectivity and alternating activity, the catecholaminergic cells may generate the rhythm. The ciliomotor circuitry thus constitutes a stop-and-go pacemaker system for the whole-body coordination of ciliary locomotion.

neuroscience↗