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Behavioral choice by presynaptic inhibition of tactile sensory terminals

Nature Neuroscience volume 12, pages 1450–1457 (2009)Cite this article

Abstract

When presented with multiple stimuli, animals generally choose to respond only to one input. The neuronal mechanisms determining such behavioral choices are poorly understood. We found that the medicinal leech had greatly diminished responses to moderate mechanosensory input as it fed. Feeding dominated other responses by suppressing transmitter release from mechanosensory neurons onto all of their neuronal targets. The effects of feeding on synaptic transmission could be mimicked by serotonin. Furthermore, the serotonin antagonist mianserin blocked feeding-induced decreases in synaptic transmission. These results indicate that feeding predominates behaviors by using serotonin at an early stage of sensory processing, namely on presynaptic terminals of mechanosensory neurons.

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Figure 1: Leech behavior and the semi-intact preparation.
Figure 2: Local bend motor responses during feeding and nonfeeding.
Figure 3: Feeding decreases the amplitudes of EPSPs at P cell synapses.
Figure 4: Increased PPR during feeding suggests a decrease in the probability of transmitter release at P-cell terminals.
Figure 5: Stimulation of swim-gating neurons elicits bouts of swimming during feeding.
Figure 6: Serotonin decreases the P cell–to–AP neuron synaptic potential amplitudes.
Figure 7: Serotonin mimics feeding by decreasing local bending.
Figure 8: Mianserin blocks feeding-induced depression of P-cell EPSPs and reduces local bending.

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Acknowledgements

The authors are extremely grateful to M. Scanziani for experimental suggestions and critical review of the manuscript. We would also like to thank K. Mesce for valuable editorial assistance and K. Todd for help with confocal microscopy and tissue processing. This work was supported by the US National Institutes of Health (MH43396 and NS35336 to W.B.K.) and the National Science Foundation (IOB-0523959 to K. Mesce and W.B.K.).

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Authors and Affiliations

  1. Division of Biological Sciences, Neurosciences Graduate Program, University of California San Diego, La Jolla, California, USA

    Quentin Gaudry & William B Kristan Jr

  2. Division of Biological Sciences, Neurobiology Section, University of California San Diego, La Jolla, California, USA

    William B Kristan Jr

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  1. Quentin Gaudry
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Contributions

Q.G. and W.B.K. designed the experiments and wrote the manuscript. Q.G. performed the experiments.

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Correspondence to William B Kristan Jr.

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Gaudry, Q., Kristan, W. Behavioral choice by presynaptic inhibition of tactile sensory terminals. Nat Neurosci 12, 1450–1457 (2009). https://doi.org/10.1038/nn.2400

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