Abstract
The neural networks that regulate animal behaviors are encoded in terms of neuronal excitation and inhibition at the synapse. However, how the temporal activity of neural circuits is dynamically and precisely characterized by each signaling interaction via excitatory or inhibitory synapses, and how both synaptic patterns are organized to achieve fine regulation of circuit activities is unclear. Here, we show that in Caenorhabditis elegans, the excitatory/inhibitory switch from asymmetric sensory neurons (ASEL/R) following changes in NaCl concentration is required for a rapid and fine response in postsynaptic interneurons (AIBs). We found that glutamate released by the ASEL neuron inhibits AIBs via a glutamate-gated chloride channel localized at the distal region of AIB neurites. Conversely, glutamate released by the ASER neuron activates AIBs via an AMPA-type ionotropic receptor and a G-protein-coupled metabotropic glutamate receptor. Interestingly, these excitatory receptors are mainly distributed at the proximal regions of the neurite. Our results suggest that these convergent synaptic patterns can tune and regulate the proper behavioral response to environmental changes in NaCl.
Highlights
Neuronal circuit activity is modulated by a balanced and well-organized combination of excitatory and inhibitory signals
We show that glutamate released by the ASEL inhibits postsynaptic AIBs through a glutamate-gated chloride channel and an unidentified receptor, whereas glutamate released by the ASER activates AIBs via AMPA-type ionotropic and G-protein-coupled metabotropic glutamate receptors
Each excitatory or inhibitory synapse is located on distinct regions of the postsynaptic AIB neurite. These results suggest that excitatory/inhibitory signaling from asymmetric sensory neurons is integral to the salt-chemotaxis neural circuit to achieve rapid and fine responses in postsynaptic neurons for suitable behavioral decisions
Summary
Neuronal circuit activity is modulated by a balanced and well-organized combination of excitatory and inhibitory signals. The circuit dynamics are temporally and spatially regulated by rate of synaptic transmission and are intrinsic for the brain functions that regulate numerous animal behaviors. Such behavioral responses to sensory stimuli are dynamic and finely tuned largely as a result of the interactions between excitatory and inhibitory signals. In the vertebrate visual system, the responses of ON and OFF bipolar neurons are finely tuned by photoreceptor neurons via both excitatory and inhibitory synapses, and these bipolar neurons transmit visual information to upper layer ganglion cells (Schiller et al, 1986). An information stream to discriminate between brightness and contrast in the retina has been proposed to be strictly regulated by excitatory and inhibitory signals (Molnar et al, 2009). Even robotic control systems integrate positive and negative signals to finely regulate dynamic
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