Behavioral plasticity, learning, and memory in C. elegans

Sasakura, Hiroyuki; Mori, Ikue

doi:10.1016/j.conb.2012.09.005

Cited by 94 publications

(80 citation statements)

References 70 publications

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“…Recent insights into more complex locomotion behaviors [70,71], the orchestration of sequential behaviors [16 ,62 ,63,64], and the variety of modulation pathways [71,72] suggest that extrasynaptic circuit mechanisms should be given more prominence in future models. Indeed what emerges is a much richer view of the C. elegans nervous system, as a dynamic, reconfigurable and overlaid circuit, in which neuronal-environmental loops act in a variety of mechanisms across a wide range of time scales.…”

Section: Discussionmentioning

confidence: 99%

Nematode locomotion: dissecting the neuronal–environmental loop

Cohen

Sanders

2014

Current Opinion in Neurobiology

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With a fully reconstructed and extensively characterized neural circuit, the nematode Caenorhabditis elegans is a promising model system for integrating our understanding of neuronal, circuit and whole-animal dynamics. Fundamental to addressing this challenge is the need to consider the tight neuronal-environmental coupling that allows the animal to survive and adapt to changing conditions. Locomotion behaviors are affected by environmental variables both at the biomechanical level and via adaptive sensory responses that drive and modulate premotor and motor circuits. Here we review significant advances in our understanding of proprioceptive control of locomotion, and more abstract models of spatial orientation and navigation. The growing evidence of the complexity of the underlying circuits suggests that the intuition gained is but the first step in elucidating the secrets of neural computation in this relatively simple system. http://dx.doi.org/10. 1016/j.conb.2013.12.003 Introduction To survive, animals process sensory information to drive motor behaviors and to move about their environment. Among locomotion strategies, undulations are remarkably effective across scales and in a variety of environments [1][2][3]. Common to most locomotion and to undulationbased strategies, in particular, is the tight neuronalenvironmental loop, in which the shape of the body and the way in which the sensory organs sample the environment are integral to the neural dynamics. The nematode Caenorhabditis elegans (C. elegans) is a powerful system in which to study this loop, due to its small nervous system and experimental tractability. Indeed, with a largely specified neural circuit and rapidly advancing technologies for recording and manipulating neuronal activity [4 ,5], significant progress is being made in deciphering the dynamics this neural circuit supports.Here we review recent progress in understanding the motor programs underpinning undulatory locomotion as well as higher level command of locomotion primitives and sensorimotor programs in C. elegans. We discuss how progress in understanding the neuronal-environmental loop is contributing to the ongoing effort and fundamental challenges in assembling a whole animal model of C. elegans behavior. The ventral nerve cordC. elegans is a small (1 mm long) unsegmented worm with 302 nerve cells [6][7][8]. The animal's undulations are controlled by head and ventral nerve cord (VNC) circuits. Extensive characterization of defects (through ablation of individual classes of neurons) [9][10][11] has provided a strong basis for an intuitive understanding of the operation of this otherwise irregular circuit architecture [12 ,13]. Indeed, evidence suggests that semi-independent VNC subcircuits control forward and backward locomotion [6,14,15,16 ,17 ,18 ,19 ] and are gated by distinct premotor (so-called command) interneurons. The forward locomotion circuit in the ventral nerve cordIn forward locomotion, cholinergic motor neurons excite muscles on either side of the body while ...

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Section: Discussionmentioning

confidence: 99%

Nematode locomotion: dissecting the neuronal–environmental loop

Cohen

Sanders

2014

Current Opinion in Neurobiology

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“…elegans learns and remembers a cultivation temperature (T c ) at which high-quality food is provided (22)(23)(24)(25). When conditioned animals are exposed to a thermal gradient, thermotaxis is observed: animals migrate to the T c and then move isothermally.…”

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confidence: 99%

A Calcium- and Diacylglycerol-Stimulated Protein Kinase C (PKC), Caenorhabditis elegans PKC-2, Links Thermal Signals to Learned Behavior by Acting in Sensory Neurons and Intestinal Cells

Land

Rubin

2017

Molecular and Cellular Biology

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Ca 2ϩ -and diacylglycerol (DAG)-activated protein kinase C (cPKC) promotes learning and behavioral plasticity. However, knowledge of in vivo regulation and exact functions of cPKCs that affect behavior is limited. We show that PKC-2, a Caenorhabditis elegans cPKC, is essential for a complex behavior, thermotaxis. C. elegans memorizes a nutrient-associated cultivation temperature (T c ) and migrates along the T c within a 17 to 25°C gradient. pkc-2 gene disruption abrogated thermotaxis; a PKC-2 transgene, driven by endogenous pkc-2 promoters, restored thermotaxis behavior in pkc-2 Ϫ/Ϫ animals. Cell-specific manipulation of PKC-2 activity revealed that thermotaxis is controlled by cooperative PKC-2-mediated signaling in both AFD sensory neurons and intestinal cells. Cold-directed migration (cryophilic drive) precedes T c tracking during thermotaxis. Analysis of temperature-directed behaviors elicited by persistent PKC-2 activation or inhibition in AFD (or intestine) disclosed that PKC-2 regulates initiation and duration of cryophilic drive. In AFD neurons, PKC-2 is a Ca 2ϩ sensor and signal amplifier that operates downstream from cyclic GMP-gated cation channels and distal guanylate cyclases. UNC-18, which regulates neurotransmitter and neuropeptide release from synaptic vesicles, is a critical PKC-2 effector in AFD. UNC-18 variants, created by mutating Ser 311 or Ser 322 , disrupt thermotaxis and suppress PKC-2-dependent cryophilic migration.KEYWORDS C. elegans signal integration, MUNC18 and UNC-18, calcium, diacylglycerol-activated PKC, cyclic GMP-gated channel, protein kinase C, regulation of learned behavior, sensory neuron, signal transduction, thermotaxis D iacylglycerol (DAG) and free cytoplasmic Ca 2ϩ mediate actions of hormones, neurotransmitters (NTs), and other stimuli that activate phospholipases C␤ and C␥ (1). Conventional protein kinase C isoforms (cPKCs ␣, ␤I, ␤II, and ␥) are widely expressed effectors of Ca 2ϩ and DAG in mammalian tissues (2-5). cPKCs are translocated to membranes and activated by binding Ca 2ϩ and DAG via their respective C2 and C1 domains. Thus, cPKCs are poised to receive, amplify, and disseminate the complete spectrum of intracellular signals generated by phospholipase C activation. Accordingly, cPKCs often couple extracellular stimuli to physiological processes that are coregulated by dynamic changes in Ca 2ϩ and DAG levels. In contrast, novel PKC isoforms (nPKCs ␦, , , and ) are activated by DAG alone.Some cell functions are redundantly regulated by combinations of PKCs. However, individual cPKCs can control key aspects of homeostasis or, when misregulated, promote pathological processes. For example, PKC␣ selectively regulates cardiac contrac-

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“…The animal exhibits several types of quiescence behaviors, which feature characteristics of sleep [31]. Furthermore, the nervous system features habituation as well as simple forms of (associative) learning [2,34]. Single modes of behavior are often controlled by a few neurons that form simple circuits.…”

Section: Simple Nervous System Complex Behaviormentioning

confidence: 99%

Optogenetic analyses of neuronal network function and synaptic transmission in Caenorhabditis elegans

Gottschalk

2014

E-Neuroforum

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Caenorhabditis elegans is a popular model organism in the neurosciences [4]. This animal stands out in particular due to a (seemingly) simple nervous system consisting of only 302 neurons. Based on the fundamental research by John White and colleagues from the 1970s and 1980s, these neurons are precisely mapped in the entirety of their synaptic connections (chemical and electrical synapses; [51]): by means of serial electron microscopy, the entire nervous system, synapse by synapse and including all anatomical connections, has been unraveled. Since eutely (having a fixed number of somatic cells) occurs in every single individual of C. elegans and since it can be expected that the synapses are genetically determined and not destined by plasticity or learning, one can expect consistency of synapses between individuals. However, evidence for this still needs to be provided by serial electron microscopy and connectomics being conducted on several individuals; even with modern block-face imaging and semi-automatic segmentation, this requires huge effort. White et al. [51] have been able to map about 7000 synapses in between the 302 neurons and muscle cells. In this neuronal network, elementary circuits can be found which, in an analogous, logical way of operation, can also be found in the nervous system of higher animals, with the difference that they exist in myriads of copies and work in parallel in order to comply with more complex tasks. The majority of synaptic key factors is highly conserved between humans and nematodes and, in most cases, these have been identified in C. elegans for the first time [6,29]. Thus, the nervous system of C. elegans is not only a valid model for higher nervous systems on the protein level, but also on the level of basic circuits or logical circuitry modules. Simple nervous system, complex behaviorAs simple as C. elegans seems to be as an animal, the more versatile upon closer analysis are the behavioral patterns this animal is able to generate [39]. C. elegans carries out several types of locomotion, navigation in two and three dimensions, as well as complex mating behaviors [5]. The nematode has sensors for numerous modalities, e.g., temperature, chemicals, tastants, oxygen and CO 2 , perception of light and magnetic fields, as well as various types of mechano-and nociception. Most of these sensory modalities lead to responses in the form of taxis, escape behavior, or altered navigation. However, long-term changes in behavior can also occur, as well as switching between different behavioral states (mainly regulated by neuromodulators). The animal exhibits several types of quiescence behaviors, which feature characteristics of sleep [31]. Furthermore, the nervous system features habituation as well as simple forms of (associative) learning [2,34]. Single modes of behavior are often controlled by a few neurons that form simple circuits. This means that the control of behavior is determined by the physiological characteristics and synaptic connections of the 302 neurons.Cultivation of...

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Behavioral plasticity, learning, and memory in C. elegans

Cited by 94 publications

References 70 publications

Nematode locomotion: dissecting the neuronal–environmental loop

Nematode locomotion: dissecting the neuronal–environmental loop

A Calcium- and Diacylglycerol-Stimulated Protein Kinase C (PKC), Caenorhabditis elegans PKC-2, Links Thermal Signals to Learned Behavior by Acting in Sensory Neurons and Intestinal Cells

Optogenetic analyses of neuronal network function and synaptic transmission in Caenorhabditis elegans

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