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Prediction of Choice From Competing Mechanosensory and Choice-Memory Cues During Active Tactile Decision Making

Campagner Dario, Evans H Mathew, Chlebikova Katarina, Colins-Rodriguez Andrea, Loft S E Michaela, Fox Sarah, Pettifer David, Humphries D Mark, Svoboda Karel, Petersen S Rasmus
doi: https://doi.org/10.1101/400358
Campagner Dario
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
2Janelia Research Campus, HHMI, Ashburn, Virginia, 20147, United States of America
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Evans H Mathew
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
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Chlebikova Katarina
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
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Colins-Rodriguez Andrea
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
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Loft S E Michaela
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
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Fox Sarah
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
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Pettifer David
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
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Humphries D Mark
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
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Svoboda Karel
2Janelia Research Campus, HHMI, Ashburn, Virginia, 20147, United States of America
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Petersen S Rasmus
1Division of Neuroscience & Experimental Psychology, Faculty of Biology, Medicine and Health, the University of Manchester, Manchester, United Kingdom, M13 9PT
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  • For correspondence: r.petersen@manchester.ac.uk
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ABSTRACT

Perceptual decision making is an active process where animals move their sense organs to extract task-relevant information. To investigate how the brain translates sensory input into decisions during active sensation, we developed a mouse active touch task where the mechanosensory input can be precisely measured and that challenges animals to use multiple mechanosensory cues. Mice were trained to localise a pole using a single whisker and to report their decision by selecting one of three choices. Using high-speed imaging and machine vision we estimated whisker-object mechanical forces at millisecond resolution. Mice solved the task by a sensory-motor strategy where both the strength and direction of whisker bending were informative cues to pole location. We found competing influences of immediate sensory input and choice memory on mouse choice. On correct trials, choice could be predicted from the direction and strength of whisker bending, but not from previous choice. In contrast, on error trials, choice could be predicted from previous choice but not from whisker bending. This study shows that animal choices during active tactile decision making can be predicted from mechanosenory and choice-memory signals; and provides a new task, well-suited for future study of the neural basis of active perceptual decisions.

SIGNIFICANCE STATEMENT Due to the difficulty of measuring the sensory input to moving sense organs, active perceptual decision making remains poorly understood. The whisker system provides a way forward since it is now possible to measure the mechanical forces due to whisker-object contact during behaviour. Here we train mice in a novel behavioural task that challenges them to use rich mechanosensory cues, but can be performed using one whisker and enables task-relevant mechanical forces to be precisely estimated. This approach enables rigorous study of how sensory cues translate into action during active, perceptual decision making. Our findings provide new insight into active touch and how sensory/internal signals interact to determine behavioural choices.

Author contribution

Designed research: CD, RSP, KS

Performed research: CD, KC, DP, SF

Contributed unpublished analytic tools: MHE, MH

Analyzed data: CD, MHE,ACR, MSEL, SF

Wrote the first draft of the paper: CD, RSP

Edited the paper: CD, RSP, MHE, KS, MH

Acknowledgements

We dedicate this paper to the memory of Katarina Chlebikova. We thank Luciana Walendy and Nuo Li for their support with behavioural training; Robert Lucas for comments on the manuscript; Tiago Branco and Branco laboratory members for discussion. This work was funded by Biotechnology and Biological Sciences Research Council (BB/L007282/1, BB/ P021603/1), Medical Research Council (MR/L01064X7/1, MR/P005659/1), Wellcome Trust (097820/Z/11/B) and HHMI.

Footnotes

  • Current affiliation of the authors: DC, Sainsbury Wellcome Centre for Neural Circuits and Behaviour, University College London, London, United Kingdom; DP, School of Biosciences, University of Birmingham, Birmingham, United Kingdom; MHE, MH, School of Psychology, University of Nottingham, United Kingdom.

  • The authors declare no competing financial interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted August 29, 2018.
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Prediction of Choice From Competing Mechanosensory and Choice-Memory Cues During Active Tactile Decision Making
Campagner Dario, Evans H Mathew, Chlebikova Katarina, Colins-Rodriguez Andrea, Loft S E Michaela, Fox Sarah, Pettifer David, Humphries D Mark, Svoboda Karel, Petersen S Rasmus
bioRxiv 400358; doi: https://doi.org/10.1101/400358
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Prediction of Choice From Competing Mechanosensory and Choice-Memory Cues During Active Tactile Decision Making
Campagner Dario, Evans H Mathew, Chlebikova Katarina, Colins-Rodriguez Andrea, Loft S E Michaela, Fox Sarah, Pettifer David, Humphries D Mark, Svoboda Karel, Petersen S Rasmus
bioRxiv 400358; doi: https://doi.org/10.1101/400358

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