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Review, Integrative Systems

Integrative Neuroscience of Paramecium, a “Swimming Neuron”

Romain Brette
eNeuro 5 May 2021, 8 (3) ENEURO.0018-21.2021; https://doi.org/10.1523/ENEURO.0018-21.2021
Romain Brette
Sorbonne Université, Institut National de la Santé et de la Recherche Médicale, Centre National de la Recherche Scientifique, Institut de la Vision, Paris 75012, France
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  • Figure 1.
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    Figure 1.

    Paramecium morphology. A, Scanning electron microscopy image of P. tetraurelia; scale bar: 10 μm (Valentine et al., 2012). B, Paramecium caudatum (Jennings, 1899a), a large species (∼200 μm) with a pointed posterior end. a, anterior end; p, posterior end; g, oral groove; m, mouth; o, oral side; ab, aboral side; cv, contractile vacuole. The drawing also shows food vacuoles and cilia.

  • Figure 2.
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    Figure 2.

    The avoiding reaction triggered by an action potential. A, Avoiding reaction against an obstacle, as illustrated by Jennings (1906). B, Action potential in response to a 2-ms current pulse (top), recorded with the hanging droplet method (bottom; from Naitoh et al., 1972 with permission).

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    Figure 3.

    Swimming, feeding and reproducing. A, Spiral swimming, with the oral groove facing the spiral axis (Jennings, 1899a). B, Thigmotactic Paramecium resting against a fiber (Jennings, 1897). Arrows show water currents produced by oral cilia. C, Two paramecia in conjugation (sexual reproduction; Jennings, 1904).

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    Figure 4.

    The avoiding reaction is graded (Jennings, 1904): swinging of the anterior end in a weak reaction (A), a strong reaction (B) and a very strong reaction (C).

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    Figure 5.

    Paramecium navigation. A, Escape reaction triggered by a heat stimulus (laser) near the posterior end (star; Hamel et al., 2011). B, Sideways jumping from a strong heat stimulus (star) by throwing trichocysts (Hamel et al., 2011). C, Trajectory of Paramecium in a 5-mm capillary, showing an increase in backward swimming after 1 min, corresponding to ∼40 avoiding reactions (Kunita et al., 2014). D, Bending of P. caudatum in a 160-μm channel (Jana et al., 2015).

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    Figure 6.

    Chemotaxis and social behavior. A, Gathering of paramecia in a drop of weakly acid solution (Jennings, 1899a). B, Path followed by Paramecium in a drop of acid (Jennings, 1906). C, paramecia avoiding a drop of sodium carbonate (Jennings, 1899a). D, paramecia gathering in a cloud of carbon dioxide generated by their respiration (Jennings, 1899a).

  • Figure 7.
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    Figure 7.

    Adaptation. A, Change in swimming velocity when Paramecium adapted to a solution of 0.25 mm CaCl2 and 4 mm KCl is transferred to a solution of 0.25 mm CaCl2 and 1 mm (open circles), 2 mm (closed circles), 4 mm (squares), or 16 mm (triangles) KCl (from Oka et al., 1986). B, Resting potential versus KCl concentration for cells adapted to 2 mm, 4 mm, 8 mm, and 16 mm KCl (top to bottom; Oka et al., 1986, with permission). Arrows indicate the adapted state. C, Accumulation of Paramecium in a warm region (Jennings, 1899a). The top of the slide is placed on a 40°C bath while the bottom rests on ice. D, Change in avoiding reaction rate after paramecia cultured at 25°C are transferred to 30°C (from Nakaoka et al., 1982, with permission). Note the change in time scale.

  • Figure 8.
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    Figure 8.

    Spiral swimming. A, Organization of ciliary basal bodies on the oral (ventral) and aboral (dorsal) side (from Iftode et al., 1989, with permission). B, Ciliary beat cycle: power stroke (or effective stroke) and recovery stroke (Omori et al., 2020). C, Water currents produced by cilia for different orientations of Paramecium (Jennings, 1904). In the oral groove, currents are oriented toward the mouth. D, Metachronal waves represented by parallel lines, progressing transversally, with cilia’s power stroke oriented toward the right and rear (from Machemer, 1972, with permission). Cilia on parallel lines are at the same phase of the beat cycle. The curved arrow shows the direction of movement.

  • Figure 9.
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    Figure 9.

    Gravitactic behavior of Paramecium. A, Upwardly curved trajectories of Paramecium in a vertical chamber (from Roberts, 2010, with permission). B, Velocity change (corrected for sedimentation) as a function of cell orientation (from Nagel and Machemer, 2000, with permission), open circles correspond to a morphologic mutant. C, Avoiding reaction frequency as a function of acceleration in a centrifuge microscope, after 4 h of equilibration (from Nagel and Machemer, 2000, with permission). Triangles indicate cell direction.

  • Figure 10.
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    Figure 10.

    Details of the avoiding reaction. A, Reorganization of the ciliary beating pattern during the avoiding reaction (after Machemer, 1969). B, Cross-section of Paramecium seen from the anterior end, during forward swimming (a, corresponding to step 1) and during reorientation (b, corresponding to step 6), according to Jennings (1904). The arrows correspond to the induced movement of the body (opposite to the beating direction).

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    Figure 11.

    Membrane potential responses to mechanical stimulation with a glass stylus on the front (A) and on the rear (B; from Naitoh and Eckert, 1969, with permission; top traces: voltage command to the piezoelectric actuator).

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    Figure 12.

    Action potential currents in P. caudatum (from Brehm and Eckert, 1978a, with permission). A, Current recorded in voltage-clamp with different depolarization steps above resting potential. The first and last peaks are capacitive transients. The early negative transient is mediated by calcium; the late positive current is mediated by potassium. B, Early and late currents versus membrane potential (relative to rest).

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    Figure 13.

    Electromotor coupling. A, Calcium uncaging in cilia (circle) triggers local ciliary reversal (from Iwadate, 2003, with permission). B, Beating frequency (filled: positive; open: negative) as a function of membrane potential in voltage clamp (from Machemer, 1976, with permission). Reversal is indicated by dots. C, Beating frequency versus pCa (-log10 [Ca2+]) in a permeabilized cell (from Nakaoka et al., 1984, with permission). Squares and circles are two different permeabilized models, circles being more physiological. Cilia reverse at the minimum beating frequency. D, Cell length versus pCa in a permeabilized cell (from Nakaoka et al., 1984, with permission).

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    Figure 14.

    Mechanosensitive responses measured as a function of stimulation position (A: anterior; P: posterior) in a P. aurelia mutant with no action potential (from Satow et al., 1983, with permission). Below, K+ currents are blocked with TEA.

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Integrative Neuroscience of Paramecium, a “Swimming Neuron”
Romain Brette
eNeuro 5 May 2021, 8 (3) ENEURO.0018-21.2021; DOI: 10.1523/ENEURO.0018-21.2021

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Integrative Neuroscience of Paramecium, a “Swimming Neuron”
Romain Brette
eNeuro 5 May 2021, 8 (3) ENEURO.0018-21.2021; DOI: 10.1523/ENEURO.0018-21.2021
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  • Article
    • Abstract
    • Significance Statement
    • Introduction
    • The Life of Paramecium
    • The Motor System of Paramecium
    • The Physiologic Basis of Behavior
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Keywords

  • ciliates
  • excitability
  • Paramecium
  • sensorimotor

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