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OFF-responses of interneurons optimize avoidance behaviors depending on stimulus strength via electrical synapses.

ABSTRACT: Optimization of the types and timing of avoidance behaviors depending on the intensity of a noxious stimulus is essential for survival; however, processing in the central nervous system and its developmental basis are largely unknown. Here, we report that Caenorhabditis elegans preferentially selects one of three different types of avoidance behaviors depending on the strength of the noxious stimulus. We screened 210 neuronal transcription factors using a combination of optogenetics and RNA interference methods and identified 19 candidates required for avoidance behaviors. One candidate, gene lin-32 (abnormal cell LINeage 32), which encodes an atonal homolog, is required for the neural fate determination of AIB interneurons and functions by regulating the expression of electrical and chemical synapse genes, namely, inx-1 (innexin 1) and AMPA-type ionotropic glutamate receptor glr-1. When examined by Ca imaging, AIB showed an OFF calcium increase to the noxious stimulus. The OFF calcium increase was provoked only by strong stimulation, suggesting a role for optimization of the avoidance behavior. However, lin-32 mutants showed an impaired AIB OFF calcium increase, concomitant with a reduced occurrence of the dynamic avoidance behavior called the "omega turn". The AIB neural responses may be transferred to downstream inter/motor neurons projecting to the neck muscles via electrical synapses comprising inx-1. Finally, we found a correlation between powerful contractions of the neck muscles and omega turns. Thus, the central regulation of the magnitude and timing of activation of the AIB interneurons optimizes the probability of omega turn depending on the stimulus context.

SUBMITTER: Hori S

PROVIDER: S-EPMC6034901 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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OFF-responses of interneurons optimize avoidance behaviors depending on stimulus strength via electrical synapses.

Hori Sayaka S Oda Shigekazu S Suehiro Yuji Y Iino Yuichi Y Mitani Shohei S

PLoS genetics 20180625 6

Optimization of the types and timing of avoidance behaviors depending on the intensity of a noxious stimulus is essential for survival; however, processing in the central nervous system and its developmental basis are largely unknown. Here, we report that Caenorhabditis elegans preferentially selects one of three different types of avoidance behaviors depending on the strength of the noxious stimulus. We screened 210 neuronal transcription factors using a combination of optogenetics and RNA inte ...[more]

PMID: 29939997

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Project description:During the last decades it became increasingly evident that electrical synapses are capable of activity-dependent plasticity. However, measuring the actual strength of electrical transmission remains difficult. Usually changes in coupling strength can only be inferred indirectly from measures such as the coupling coefficient and the coupling conductance. Because these are affected by both junctional and non-junctional conductance, plastic changes can potentially be due to both components. Furthermore, these techniques also require the blocking of chemical transmission, so that processes that involve crosstalk between chemical and electrical synapses will be suppressed. To directly examine the magnitude of errors that can occur, we use dual whole-cell current- and voltage-clamp recordings from the soma of the pair of easily accessible, electrically coupled Retzius cells in the leech to simultaneously determine coupling coefficients, coupling conductances and directly measured gap junctional currents. We present the first direct and comparative analysis of gap junction conductance using all three methods and analyze how each method would characterize the response of gap junctions to serotonin. The traditional coupling coefficients showed severe deficits in assessing the symmetry and strength of electrical synapses. These were reduced when coupling conductances were determined and were absent in the direct method. Additionally, both coupling coefficient and coupling conductance caused large and systematic errors in assessing the size and time course of the serotonin-induced changes of gap junctional currents. Most importantly, both measurements can easily be misinterpreted as implying long-term gap junctional plasticity, although the direct measurements confirm its absence. We thus show directly that coupling coefficients and coupling conductances can severely confound plastic changes in membrane and junctional conductance. Wherever possible, voltage clamp measurements should be chosen to accurately characterize the timing and strength of plasticity of electrical synapses. However, we also demonstrate that coupling coefficients can still yield a qualitatively correct picture when amended by independent measurements of the course of membrane resistance during the experiments.

Dataset Information

OFF-responses of interneurons optimize avoidance behaviors depending on stimulus strength via electrical synapses.

Publications

OFF-responses of interneurons optimize avoidance behaviors depending on stimulus strength via electrical synapses.

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