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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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Neural integration of two different types of information and decision on behavioral choice (Ishihara et al. 2002; Shinkai et al., 2011).(A) The assay system of interaction assay. (B) The reciprocal inhibition model of the attractive signaling to diacetyl and the avoidance signaling to Cu2+. (C) A neural circuit model of the interaction of two sensory signals and decision-making. The activity of AIA interneurons is regulated by the balance between excitatory inputs from AWA through the gap junction and inhibitory inputs from ASH and ADL neurons through the glutamate-gated chloride channel GLC-3. Activated AIA interneurons would increase the relative strength of the signals for diacetyl by inhibiting the signals for Cu2+. GCY-28 and SCD-2 may enhance the inhibitory synaptic outputs from AIA neurons. HEN-1, a secretory protein released from AIY neurons, may act on the receptor SCD-2. The details of the mechanism of HEN-1 action are not yet fully understood.
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Figure 5: Neural integration of two different types of information and decision on behavioral choice (Ishihara et al. 2002; Shinkai et al., 2011).(A) The assay system of interaction assay. (B) The reciprocal inhibition model of the attractive signaling to diacetyl and the avoidance signaling to Cu2+. (C) A neural circuit model of the interaction of two sensory signals and decision-making. The activity of AIA interneurons is regulated by the balance between excitatory inputs from AWA through the gap junction and inhibitory inputs from ASH and ADL neurons through the glutamate-gated chloride channel GLC-3. Activated AIA interneurons would increase the relative strength of the signals for diacetyl by inhibiting the signals for Cu2+. GCY-28 and SCD-2 may enhance the inhibitory synaptic outputs from AIA neurons. HEN-1, a secretory protein released from AIY neurons, may act on the receptor SCD-2. The details of the mechanism of HEN-1 action are not yet fully understood.

Mentions: Decision-making is the cognitive process by which animals select one action among several different choices. In order to study behavioral decision from two conflicting choices and the integration of two different sensory cues, an interaction assay system was developed (Ishihara et al., 2002). Diacetyl is an attractive odor sensed by AWA olfactory neurons and Cu2+ ion is aversive metal sensed by ASH and ADL sensory neurons (Bargmann et al., 1993; Sambongi et al., 2000). The attractive odor, diacetyl, is applied to one side of the assay plate, C. elegans animals are placed on the other side of the plate, and a Cu2+ barrier is established on the midline of the plate (Figure 5A). When C. elegans encounters the Cu2+ barrier during their migration toward diacetyl, the balance between concentrations of diacetyl and Cu2+ regulates the behavioral decision whether they go straight toward diacetyl or withdraw (Figure 5B).


Japanese studies on neural circuits and behavior of Caenorhabditis elegans.

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

Neural integration of two different types of information and decision on behavioral choice (Ishihara et al. 2002; Shinkai et al., 2011).(A) The assay system of interaction assay. (B) The reciprocal inhibition model of the attractive signaling to diacetyl and the avoidance signaling to Cu2+. (C) A neural circuit model of the interaction of two sensory signals and decision-making. The activity of AIA interneurons is regulated by the balance between excitatory inputs from AWA through the gap junction and inhibitory inputs from ASH and ADL neurons through the glutamate-gated chloride channel GLC-3. Activated AIA interneurons would increase the relative strength of the signals for diacetyl by inhibiting the signals for Cu2+. GCY-28 and SCD-2 may enhance the inhibitory synaptic outputs from AIA neurons. HEN-1, a secretory protein released from AIY neurons, may act on the receptor SCD-2. The details of the mechanism of HEN-1 action are not yet fully understood.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Neural integration of two different types of information and decision on behavioral choice (Ishihara et al. 2002; Shinkai et al., 2011).(A) The assay system of interaction assay. (B) The reciprocal inhibition model of the attractive signaling to diacetyl and the avoidance signaling to Cu2+. (C) A neural circuit model of the interaction of two sensory signals and decision-making. The activity of AIA interneurons is regulated by the balance between excitatory inputs from AWA through the gap junction and inhibitory inputs from ASH and ADL neurons through the glutamate-gated chloride channel GLC-3. Activated AIA interneurons would increase the relative strength of the signals for diacetyl by inhibiting the signals for Cu2+. GCY-28 and SCD-2 may enhance the inhibitory synaptic outputs from AIA neurons. HEN-1, a secretory protein released from AIY neurons, may act on the receptor SCD-2. The details of the mechanism of HEN-1 action are not yet fully understood.
Mentions: Decision-making is the cognitive process by which animals select one action among several different choices. In order to study behavioral decision from two conflicting choices and the integration of two different sensory cues, an interaction assay system was developed (Ishihara et al., 2002). Diacetyl is an attractive odor sensed by AWA olfactory neurons and Cu2+ ion is aversive metal sensed by ASH and ADL sensory neurons (Bargmann et al., 1993; Sambongi et al., 2000). The attractive odor, diacetyl, is applied to one side of the assay plate, C. elegans animals are placed on the other side of the plate, and a Cu2+ barrier is established on the midline of the plate (Figure 5A). When C. elegans encounters the Cu2+ barrier during their migration toward diacetyl, the balance between concentrations of diacetyl and Cu2+ regulates the behavioral decision whether they go straight toward diacetyl or withdraw (Figure 5B).

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