Predictive whisker kinematics reveal context-dependent sensorimotor strategies

Avner Wallach, David Deutsch, Tess Baker Oram, Ehud Ahissar

Research output: Contribution to journalArticlepeer-review

Abstract

Animals actively move their sensory organs in order to acquire sensory information. Some rodents, such as mice and rats, employ cyclic scanning motions of their facial whiskers to explore their proximal surrounding, a behavior known as whisking. Here, we investigated the contingency of whisking kinematics on the animal's behavioral context that arises from both internal processes (attention and expectations) and external constraints (available sensory and motor degrees of freedom). We recorded rat whisking at high temporal resolution in 2 experimental contexts-freely moving or head-fixed-and 2 spatial sensory configurations- a single row or 3 caudal whiskers on each side of the snout. We found that rapid sensorimotor twitches, called pumps, occurring during free-air whisking carry information about the rat's upcoming exploratory direction, as demonstrated by the ability of these pumps to predict consequent head and body locomotion. Specifically, pump behavior during both voluntary motionlessness and imposed head fixation exposed a backward redistribution of sensorimotor exploratory resources. Further, head-fixed rats employed a wide range of whisking profiles to compensate for the loss of head- and body-motor degrees of freedom. Finally, changing the number of intact vibrissae available to a rat resulted in an alteration of whisking strategy consistent with the rat actively reallocating its remaining resources. In sum, this work shows that rats adapt their active exploratory behavior in a "homeostatic" attempt to preserve sensorimotor coverage under changing environmental conditions and changing sensory capacities, including those imposed by various laboratory conditions.

Original languageEnglish
Article numbere3000571
JournalPLoS Biology
Volume18
Issue number5
DOIs
StatePublished - May 2020
Externally publishedYes

Bibliographical note

Funding Information:
Funding:EAhasreceivedfundingfromthe EuropeanResearchCouncil(ERC)undertheEU Horizon2020ResearchandInnovationProgram (grantagreementno.786949),theMinerva FoundationfundedbytheFederalGermanMinistry forEducationandResearch,theUnitedStates-IsraelBinationalScienceFoundation(BSF,grant No.2017216),theAdelisfoundation,andtheIrving B.HarrisFundforNewDirectionsinBrain Research.Thefundershadnoroleinstudydesign, datacollectionandanalysis,decisiontopublish,or preparationofthemanuscript.

Funding Information:
EA has received funding from the European Research Council (ERC) under the EU Horizon 2020 Research and Innovation Program (grant agreement no. 786949), the Minerva Foundation funded by the Federal German Ministry for Education and Research, the United States-Israel Binational Science Foundation (BSF, grant No. 2017216), the Adelis foundation, and the Irving B. Harris Fund for New Directions in Brain Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Publisher Copyright:
© 2020 Wallach et al.

ASJC Scopus subject areas

  • Neuroscience (all)
  • Biochemistry, Genetics and Molecular Biology (all)
  • Immunology and Microbiology (all)
  • Agricultural and Biological Sciences (all)

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