Effects of nonuniform viscosity on ciliary locomotion

AbstractCiliated 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.

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Sensory Regulation of Network Components Underlying Ciliary Locomotion in Hermissenda

Journal of Neurophysiology ◽

10.1152/jn.90759.2008 ◽

2008 ◽

Vol 100 (5) ◽

pp. 2496-2506 ◽

Cited By ~ 5

Author(s):

Terry Crow ◽

Lian-Ming Tian

Keyword(s):

Neural Network ◽

Spike Activity ◽

Electrical Coupling ◽

Rhythmic Activity ◽

Burst Activity ◽

Type I ◽

Sensory Regulation ◽

The Neural Network ◽

Efferent Neurons ◽

Ciliary Locomotion

Ciliary locomotion in the nudibranch mollusk Hermissenda is modulated by the visual and graviceptive systems. Components of the neural network mediating ciliary locomotion have been identified including aggregates of polysensory interneurons that receive monosynaptic input from identified photoreceptors and efferent neurons that activate cilia. Illumination produces an inhibition of type Ii (off-cell) spike activity, excitation of type Ie (on-cell) spike activity, decreased spike activity in type IIIi inhibitory interneurons, and increased spike activity of ciliary efferent neurons. Here we show that pairs of type Ii interneurons and pairs of type Ie interneurons are electrically coupled. Neither electrical coupling or synaptic connections were observed between Ie and Ii interneurons. Coupling is effective in synchronizing dark-adapted spontaneous firing between pairs of Ie and pairs of Ii interneurons. Out-of-phase burst activity, occasionally observed in dark-adapted and light-adapted pairs of Ie and Ii interneurons, suggests that they receive synaptic input from a common presynaptic source or sources. Rhythmic activity is typically not a characteristic of dark-adapted, light-adapted, or light-evoked firing of type I interneurons. However, burst activity in Ie and Ii interneurons may be elicited by electrical stimulation of pedal nerves or generated at the offset of light. Our results indicate that type I interneurons can support the generation of both rhythmic activity and changes in tonic firing depending on sensory input. This suggests that the neural network supporting ciliary locomotion may be multifunctional. However, consistent with the nonmuscular and nonrhythmic characteristics of visually modulated ciliary locomotion, type I interneurons exhibit changes in tonic activity evoked by illumination.

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

eLife ◽

10.7554/elife.26000 ◽

2017 ◽

Vol 6 ◽

Cited By ~ 32

Author(s):

Csaba Verasztó ◽

Nobuo Ueda ◽

Luis A Bezares-Calderón ◽

Aurora Panzera ◽

Elizabeth A Williams ◽

...

Keyword(s):

Beat Frequency ◽

Ciliary Beat Frequency ◽

Whole Body ◽

Ciliary Activity ◽

Ciliary Beating ◽

Stop And Go ◽

Multiciliated Cells ◽

Platynereis Dumerilii ◽

Catecholaminergic Cells ◽

Ciliary Locomotion

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.

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Network interneurons underlying ciliary locomotion in Hermissenda

Journal of Neurophysiology ◽

10.1152/jn.00803.2012 ◽

2013 ◽

Vol 109 (3) ◽

pp. 640-648 ◽

Cited By ~ 2

Author(s):

Terry Crow ◽

Nan Ge Jin ◽

Lian-Ming Tian

Keyword(s):

Spike Activity ◽

Excitatory Postsynaptic Potential ◽

Type I ◽

Type Ii ◽

Visually Guided ◽

Monosynaptic Connection ◽

Postsynaptic Potential ◽

The Neural Network ◽

Efferent Neurons ◽

Ciliary Locomotion

In the nudibranch mollusk Hermissenda, ciliary locomotion contributes to the generation of two tactic behaviors. Light elicits a positive phototaxis, and graviceptive stimulation evokes a negative gravitaxis. Two classes of light-responsive premotor interneurons in the network contributing to ciliary locomotion have been recently identified in the cerebropleural ganglia. Aggregates of type I interneurons receive monosynaptic excitatory (Ie) or inhibitory (Ii) input from identified photoreceptors. Type II interneurons receive polysynaptic excitatory (IIe) or inhibitory (IIi) input from photoreceptors. The ciliary network also includes type III inhibitory (IIIi) interneurons, which form monosynaptic inhibitory connections with ciliary efferent neurons (CENs). Illumination of the eyes evokes a complex inhibitory postsynaptic potential, a decrease of Ii spike activity, a complex excitatory postsynaptic potential, and an increase of Ie spike activity. Here, we characterized the contribution of identified I, II, and IIIi interneurons to the neural network supporting visually guided locomotion. In dark-adapted preparations, light elicited an increase in the tonic spike activity of IIe interneurons and a decrease in the tonic spike activity of IIi interneurons. Fluorescent dye-labeled type II interneurons exhibited diverse projections within the circumesophageal nervous system. However, a subclass of type II interneurons, IIe(cp) and IIi(cp) interneurons, were shown to terminate within the ipsilateral cerebropleural ganglia and indirectly modulate the activity of CENs. Type II interneurons form monosynaptic or polysynaptic connections with previously identified components of the ciliary network. The identification of a monosynaptic connection between Ie and IIIi interneurons shown here suggest that they provide a major role in the light-dependent modulation of CEN spike activity underlying ciliary locomotion.

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Neural Correlates of Pavlovian Conditioning in Components of the Neural Network Supporting Ciliary Locomotion in Hermissenda

Learning & Memory ◽

10.1101/lm.58603 ◽

2003 ◽

Vol 10 (3) ◽

pp. 209-216 ◽

Cited By ~ 14

Author(s):

T. Crow

Keyword(s):

Neural Network ◽

Pavlovian Conditioning ◽

Neural Correlates ◽

The Neural Network ◽

Ciliary Locomotion

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Interstitial Annelida

Diversity ◽

10.3390/d13020077 ◽

2021 ◽

Vol 13 (2) ◽

pp. 77

Author(s):

Katrine Worsaae ◽

Alexandra Kerbl ◽

Maikon Di Domenico ◽

Brett C. Gonzalez ◽

Nicolas Bekkouche ◽

...

Keyword(s):

Morphological Traits ◽

Life Forms ◽

Cryptic Diversity ◽

Special Issue ◽

Number Of Species ◽

Molecular Approaches ◽

High Degree ◽

Ciliary Locomotion

Members of the following marine annelid families are found almost exclusively in the interstitial environment and are highly adapted to move between sand grains, relying mostly on ciliary locomotion: Apharyngtidae n. fam., Dinophilidae, Diurodrilidae, Nerillidae, Lobatocerebridae, Parergodrilidae, Polygordiidae, Protodrilidae, Protodriloididae, Psammodrilidae and Saccocirridae. This article provides a review of the evolution, systematics, and diversity of these families, with the exception of Parergodrilidae, which was detailed in the review of Orbiniida by Meca, Zhadan, and Struck within this Special Issue. While several of the discussed families have previously only been known by a few described species, recent surveys inclusive of molecular approaches have increased the number of species, showing that all of the aforementioned families exhibit a high degree of cryptic diversity shadowed by a limited number of recognizable morphological traits. This is a challenge for studies of the evolution, taxonomy, and diversity of interstitial families as well as for their identification and incorporation into ecological surveys. By compiling a comprehensive and updated review on these interstitial families, we hope to promote new studies on their intriguing evolutionary histories, adapted life forms and high and hidden diversity.

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