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Japanese studies on neural circuits and behavior of Caenorhabditis elegans.

Sasakura H, Tsukada Y, Takagi S, Mori I - Front Neural Circuits (2013)

Bottom Line: Several laboratories have established unique and clever methods to study the underlying neuronal substrates of behavioral regulation in C. elegans.The technological advances applied to studies of C. elegans have allowed new approaches for the studies of complex neural systems.Through reviewing the studies on the neuronal circuits of C. elegans in Japan, we will analyze and discuss the directions of neural circuit studies.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Neurobiology, Division of Biological Science, Nagoya University Nagoya, Japan.

ABSTRACT
The nematode Caenorhabditis elegans is an ideal organism for studying neural plasticity and animal behaviors. A total of 302 neurons of a C. elegans hermaphrodite have been classified into 118 neuronal groups. This simple neural circuit provides a solid basis for understanding the mechanisms of the brains of higher animals, including humans. Recent studies that employ modern imaging and manipulation techniques enable researchers to study the dynamic properties of nervous systems with great precision. Behavioral and molecular genetic analyses of this tiny animal have contributed greatly to the advancement of neural circuit research. Here, we will review the recent studies on the neural circuits of C. elegans that have been conducted in Japan. Several laboratories have established unique and clever methods to study the underlying neuronal substrates of behavioral regulation in C. elegans. The technological advances applied to studies of C. elegans have allowed new approaches for the studies of complex neural systems. Through reviewing the studies on the neuronal circuits of C. elegans in Japan, we will analyze and discuss the directions of neural circuit studies.

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Circuit regulation of associative learning between temperature and food (Hedgecock and Russell, 1975; Mori and Ohshima, 1995; Mohri et al. 2005; Kodama et al. 2006; Sasakura and Mori, 2013).(A) Assay system and scheme for experiments. (B) Thermotaxis of wild type animals and aho-2/ins-1 mutants. Wild type animals cultivated with food at 17 or 25°C migrate to the past growth temperature on a radial thermal gradient plate. In contrast, wild type animals cultivated without food (starvation conditions) diffuse and avoid the growth temperature area. The aho-2/ins-1 mutants exhibited normal thermotaxis when grown with food, but exhibited abnormal thermotaxis when grown without food. Despite the starvation conditions, aho-2/ins-1 mutants migrate to the past growth temperature. (C) Exogenous serotonin mimics the well-fed state and octopamine mimics the starvation state in thermotaxis. C. elegans grown at 25°C without food but with serotonin behaves like well-fed animals, whereas C. elegans grown with food but with octopamine behaves like starved animals. (D) Proposed analogy between the thermotaxis neural circuit in C. elegans and the human brain. Neural operation logic in C. elegans thermotaxis is analogous to that in the human brain. Stored thermal information in AFD neurons is transmitted to the thermotaxis core interneurons AIY, AIZ, and RIA. Thermal information and food state are integrated and processed in those interneurons by monoamines and insulin to generate output behavior. In the human brain, working memory is coded in the cerebral cortex, and the coded information is conveyed to the basal ganglia, where learning and emotion proceed with modulation through monoamines. We propose here a functional analogy between the simple neural circuit in C. elegans thermotaxis and the functionally layered structure of the human brain.
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Figure 8: Circuit regulation of associative learning between temperature and food (Hedgecock and Russell, 1975; Mori and Ohshima, 1995; Mohri et al. 2005; Kodama et al. 2006; Sasakura and Mori, 2013).(A) Assay system and scheme for experiments. (B) Thermotaxis of wild type animals and aho-2/ins-1 mutants. Wild type animals cultivated with food at 17 or 25°C migrate to the past growth temperature on a radial thermal gradient plate. In contrast, wild type animals cultivated without food (starvation conditions) diffuse and avoid the growth temperature area. The aho-2/ins-1 mutants exhibited normal thermotaxis when grown with food, but exhibited abnormal thermotaxis when grown without food. Despite the starvation conditions, aho-2/ins-1 mutants migrate to the past growth temperature. (C) Exogenous serotonin mimics the well-fed state and octopamine mimics the starvation state in thermotaxis. C. elegans grown at 25°C without food but with serotonin behaves like well-fed animals, whereas C. elegans grown with food but with octopamine behaves like starved animals. (D) Proposed analogy between the thermotaxis neural circuit in C. elegans and the human brain. Neural operation logic in C. elegans thermotaxis is analogous to that in the human brain. Stored thermal information in AFD neurons is transmitted to the thermotaxis core interneurons AIY, AIZ, and RIA. Thermal information and food state are integrated and processed in those interneurons by monoamines and insulin to generate output behavior. In the human brain, working memory is coded in the cerebral cortex, and the coded information is conveyed to the basal ganglia, where learning and emotion proceed with modulation through monoamines. We propose here a functional analogy between the simple neural circuit in C. elegans thermotaxis and the functionally layered structure of the human brain.

Mentions: Caenorhabditis elegans associates past growth temperature with food. In its natural habitat, C. elegans likely adapts to the fluctuating temperatures in soil in order to stay near food sources. We can observe this behavior as thermotaxis in the laboratory (Hedgecock and Russell, 1975; Mori et al., 2007; Kimata et al., 2012; Sasakura and Mori, 2013). After animals were grown with food at a certain temperature ranging from 15 to 25°C and placed on an agar surface with a temperature gradient, they migrate toward the past growth temperature and move isothermally near that temperature (Figures 8A–C). Growth temperature-shift experiments indicated that the acquisition of a new temperature memory requires 2–4 h. Dynamic alternation of temperature preference is also induced by starvation. Growth without food at a certain temperature for several hours induces animals to disperse or avoid the past growth temperature (Figures 8B, C).


Japanese studies on neural circuits and behavior of Caenorhabditis elegans.

Sasakura H, Tsukada Y, Takagi S, Mori I - Front Neural Circuits (2013)

Circuit regulation of associative learning between temperature and food (Hedgecock and Russell, 1975; Mori and Ohshima, 1995; Mohri et al. 2005; Kodama et al. 2006; Sasakura and Mori, 2013).(A) Assay system and scheme for experiments. (B) Thermotaxis of wild type animals and aho-2/ins-1 mutants. Wild type animals cultivated with food at 17 or 25°C migrate to the past growth temperature on a radial thermal gradient plate. In contrast, wild type animals cultivated without food (starvation conditions) diffuse and avoid the growth temperature area. The aho-2/ins-1 mutants exhibited normal thermotaxis when grown with food, but exhibited abnormal thermotaxis when grown without food. Despite the starvation conditions, aho-2/ins-1 mutants migrate to the past growth temperature. (C) Exogenous serotonin mimics the well-fed state and octopamine mimics the starvation state in thermotaxis. C. elegans grown at 25°C without food but with serotonin behaves like well-fed animals, whereas C. elegans grown with food but with octopamine behaves like starved animals. (D) Proposed analogy between the thermotaxis neural circuit in C. elegans and the human brain. Neural operation logic in C. elegans thermotaxis is analogous to that in the human brain. Stored thermal information in AFD neurons is transmitted to the thermotaxis core interneurons AIY, AIZ, and RIA. Thermal information and food state are integrated and processed in those interneurons by monoamines and insulin to generate output behavior. In the human brain, working memory is coded in the cerebral cortex, and the coded information is conveyed to the basal ganglia, where learning and emotion proceed with modulation through monoamines. We propose here a functional analogy between the simple neural circuit in C. elegans thermotaxis and the functionally layered structure of the human brain.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3842693&req=5

Figure 8: Circuit regulation of associative learning between temperature and food (Hedgecock and Russell, 1975; Mori and Ohshima, 1995; Mohri et al. 2005; Kodama et al. 2006; Sasakura and Mori, 2013).(A) Assay system and scheme for experiments. (B) Thermotaxis of wild type animals and aho-2/ins-1 mutants. Wild type animals cultivated with food at 17 or 25°C migrate to the past growth temperature on a radial thermal gradient plate. In contrast, wild type animals cultivated without food (starvation conditions) diffuse and avoid the growth temperature area. The aho-2/ins-1 mutants exhibited normal thermotaxis when grown with food, but exhibited abnormal thermotaxis when grown without food. Despite the starvation conditions, aho-2/ins-1 mutants migrate to the past growth temperature. (C) Exogenous serotonin mimics the well-fed state and octopamine mimics the starvation state in thermotaxis. C. elegans grown at 25°C without food but with serotonin behaves like well-fed animals, whereas C. elegans grown with food but with octopamine behaves like starved animals. (D) Proposed analogy between the thermotaxis neural circuit in C. elegans and the human brain. Neural operation logic in C. elegans thermotaxis is analogous to that in the human brain. Stored thermal information in AFD neurons is transmitted to the thermotaxis core interneurons AIY, AIZ, and RIA. Thermal information and food state are integrated and processed in those interneurons by monoamines and insulin to generate output behavior. In the human brain, working memory is coded in the cerebral cortex, and the coded information is conveyed to the basal ganglia, where learning and emotion proceed with modulation through monoamines. We propose here a functional analogy between the simple neural circuit in C. elegans thermotaxis and the functionally layered structure of the human brain.
Mentions: Caenorhabditis elegans associates past growth temperature with food. In its natural habitat, C. elegans likely adapts to the fluctuating temperatures in soil in order to stay near food sources. We can observe this behavior as thermotaxis in the laboratory (Hedgecock and Russell, 1975; Mori et al., 2007; Kimata et al., 2012; Sasakura and Mori, 2013). After animals were grown with food at a certain temperature ranging from 15 to 25°C and placed on an agar surface with a temperature gradient, they migrate toward the past growth temperature and move isothermally near that temperature (Figures 8A–C). Growth temperature-shift experiments indicated that the acquisition of a new temperature memory requires 2–4 h. Dynamic alternation of temperature preference is also induced by starvation. Growth without food at a certain temperature for several hours induces animals to disperse or avoid the past growth temperature (Figures 8B, C).

Bottom Line: Several laboratories have established unique and clever methods to study the underlying neuronal substrates of behavioral regulation in C. elegans.The technological advances applied to studies of C. elegans have allowed new approaches for the studies of complex neural systems.Through reviewing the studies on the neuronal circuits of C. elegans in Japan, we will analyze and discuss the directions of neural circuit studies.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Molecular Neurobiology, Division of Biological Science, Nagoya University Nagoya, Japan.

ABSTRACT
The nematode Caenorhabditis elegans is an ideal organism for studying neural plasticity and animal behaviors. A total of 302 neurons of a C. elegans hermaphrodite have been classified into 118 neuronal groups. This simple neural circuit provides a solid basis for understanding the mechanisms of the brains of higher animals, including humans. Recent studies that employ modern imaging and manipulation techniques enable researchers to study the dynamic properties of nervous systems with great precision. Behavioral and molecular genetic analyses of this tiny animal have contributed greatly to the advancement of neural circuit research. Here, we will review the recent studies on the neural circuits of C. elegans that have been conducted in Japan. Several laboratories have established unique and clever methods to study the underlying neuronal substrates of behavioral regulation in C. elegans. The technological advances applied to studies of C. elegans have allowed new approaches for the studies of complex neural systems. Through reviewing the studies on the neuronal circuits of C. elegans in Japan, we will analyze and discuss the directions of neural circuit studies.

Show MeSH
Related in: MedlinePlus