The Input-Output Relationship of AIY Interneurons in Caenorhabditis elegans in Noisy Environment

摘要

class="head no_bottom_margin" id="sec1title">IntroductionInformation processing from sensory inputs to regulate behavior in noisy environments is a fundamental topic in neuroscience. To improve our understanding of such information processing, the relationship between the noise level of the stimulation and animal perception has been studied in depth (, , ). However, at the neuronal level these relationships remain largely unclear. Although the input-output relationship in neurons has also been thoroughly investigated (, , , , , , ), it remains unknown how neurotransmitter inputs affect postsynaptic neuronal activity in vivo in noisy environments, because simultaneous measurement of input and output in vivo is technically difficult due to the complexity of the networks involved (, , ).The nematode Caenorhabditis elegans is a suitable model for investigating this question. It has a simple neuronal circuit (), as well as optical transparency, making it well suited for visualization with various imaging techniques (). The AIY interneurons of C. elegans are particularly suitable for this purpose; they receive various sensory inputs, including gustatory, olfactory, and thermal information (href="#bib5" rid="bib5" class=" bibr popnode">Chalasani et al., 2007, href="#bib7" rid="bib7" class=" bibr popnode">Clark et al., 2006, href="#bib40" rid="bib40" class=" bibr popnode">Satoh et al., 2014), which regulate the animal's behavior following integration (href="#bib22" rid="bib22" class=" bibr popnode">Kocabas et al., 2012, href="#bib28" rid="bib28" class=" bibr popnode">Li et al., 2014, href="#bib40" rid="bib40" class=" bibr popnode">Satoh et al., 2014). Furthermore, AIY interneurons show a sporadic Ca²⁺ response regardless of the presence of explicit stimulation (href="#bib5" rid="bib5" class=" bibr popnode">Chalasani et al., 2007, href="#bib7" rid="bib7" class=" bibr popnode">Clark et al., 2006), whereas sensory neurons show a deterministic Ca²⁺ response to environmental stimulation (href="#bib5" rid="bib5" class=" bibr popnode">Chalasani et al., 2007, href="#bib7" rid="bib7" class=" bibr popnode">Clark et al., 2006, href="#bib20" rid="bib20" class=" bibr popnode">Kato et al., 2014, href="#bib46" rid="bib46" class=" bibr popnode">Tsukada et al., 2016). Both glutamate receptor mutations and the ablation of sensory neurons have been shown to abolish the Ca²⁺ response to sensory stimulation in AIY (href="#bib5" rid="bib5" class=" bibr popnode">Chalasani et al., 2007, href="#bib7" rid="bib7" class=" bibr popnode">Clark et al., 2006). This suggests that glutamate input to AIY can evoke the sporadic Ca²⁺ response as a result of sensory input integration under natural noise.We used several simultaneous fluorescence imaging techniques to identify the input-output relationship in AIY in a noisy environment in vivo. To ensure that Ca²⁺ spikes could be considered AIY output, we first showed that depolarization of the membrane potential precedes Ca²⁺ spikes, by simultaneously imaging both in AIY. We used an odor, isoamyl alcohol (IAA) as model stimulation to modulate the sensory inputs, and simultaneous imaging of glutamate input and the Ca²⁺ response showed that glutamate input decreases when the Ca²⁺ spikes occur, with or without odor stimulation, and vice versa. We also investigated these relationships in both the glutamate receptor and glutamate-defective mutants and showed that fluctuations in glutamate input evoke the sporadic Ca²⁺ response in AIY. As far as we know, this is the first report identifying the input-output relationship for fluctuations under natural environmental noise in vivo. Glutamate inputs represent sensory inputs, and AIY neurons have been reported to regulate behavior; our results thus suggest that fluctuation in sensory input induces behavioral variability.