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A simple decision to move in response to touch reveals basic sensory memory and mechanisms for variable response times

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Stella Koutsikou, Robert Merrison-Hort, Edgar Buhl, Andrea Ferrario, Wen-Chang Li, Roman Borisyuk, Stephen R. Soffe, Alan Roberts

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Abstract

Many motor responses to sensory input, like locomotion or eye movements, are much slower than reflexes. Can simpler animals provide fundamental answers about the cellular mechanisms for motor decisions? Can we observe the ‘accumulation’ of excitation to threshold proposed to underlie decision making elsewhere? We explore how somatosensory touch stimulation leads to the decision to swim in hatchling Xenopus tadpoles. Delays measured to swimming in behaving and immobilised tadpoles are long and variable. Activity in their extensively studied sensory and sensory pathway neurons is too short‐lived to explain these response delays. Instead, whole‐cell recordings from the hindbrain reticulospinal neurons that drive swimming show that these receive prolonged, variable synaptic excitation lasting for nearly a second following a brief stimulus. They fire and initiate swimming when this excitation reaches threshold. Analysis of the summation of excitation requires us to propose extended firing in currently undefined presynaptic hindbrain neurons. Simple models show that a small excitatory recurrent‐network inserted in the sensory pathway can mimic this process. We suggest that such a network may generate slow, variable summation of excitation to threshold. This excitation provides a simple memory of the sensory stimulus. It allows temporal and spatial integration of sensory inputs and explains the long, variable delays to swimming. The process resembles the ‘accumulation’ of excitation proposed for cortical circuits in mammals. We conclude that fundamental elements of sensory memory and decision making are present in the brainstem at a surprisingly early stage in development.
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Original languageEnglish
Pages (from-to)6219-6233
JournalThe Journal of Physiology
Volume596
Issue number24
Early online date19 Sep 2018
DOIs
Publication statusPublished - 15 Dec 2018

    Research areas

  • Decision-making, Xenopus laevis, Reticulospinal neurons, Locomotion, Somatosensory

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