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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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Koutsikou_2018_TJP_Simpledecision_CCBY_VoR.pdf (1.011Mb)
Date
15/12/2018
Author
Koutsikou, Stella
Merrison-Hort, Robert
Buhl, Edgar
Ferrario, Andrea
Li, Wen-Chang
Borisyuk, Roman
Soffe, Stephen R.
Roberts, Alan
Keywords
Decision-making
Xenopus laevis
Reticulospinal neurons
Locomotion
Somatosensory
BF Psychology
NDAS
BDC
Metadata
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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.
Citation
Koutsikou , S , Merrison-Hort , R , Buhl , E , Ferrario , A , Li , W-C , Borisyuk , R , Soffe , S R & Roberts , A 2018 , ' A simple decision to move in response to touch reveals basic sensory memory and mechanisms for variable response times ' , The Journal of Physiology , vol. 596 , no. 24 , pp. 6219-6233 . https://doi.org/10.1113/JP276356
Publication
The Journal of Physiology
Status
Peer reviewed
DOI
https://doi.org/10.1113/JP276356
ISSN
0022-3751
Type
Journal article
Rights
© 2018 The Authors The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Description
Funding: The Biotechnology and the Biological Sciences Research Council grants: BB/L002353/1, BB/L00111X/1 and BB/L000814/1.
Collections
  • University of St Andrews Research
URI
http://hdl.handle.net/10023/16438

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