Bilateral Discrimination of Tactile Patterns without Whisking in Freely Running Rats

A majority of whisker discrimination tasks in rodents are performed on head-fixed animals to facilitate tracking or control of the sensory inputs. However, head fixation critically restrains the behavior and thus the incoming stimuli compared with those occurring in natural conditions. In this study, we investigated whether freely behaving rats can discriminate fine tactile patterns while running, in particular when stimuli are presented simultaneously on both sides of the snout. We developed a two-alternative forced-choice task in an automated modified T-maze. Stimuli were either a surface with no bars (smooth) or with vertical bars spaced irregularly or regularly. While running at full speed, rats encountered simultaneously the two discriminanda placed on the two sides of the central aisle. Rats learned to recognize regular bars versus a smooth surface in 8 weeks. They solved the task while running at an average speed of 1 m/s, so that the contact with the stimulus lasted <1 typical whisking cycle, precluding the use of active whisking. Whisker-tracking analysis revealed an asymmetry in the position of the whiskers: they oriented toward the rewarded stimulus during successful trials as early as 60 ms after the first possible contact. We showed that the whiskers and activity in the primary somatosensory cortex are involved during the discrimination process. Finally, we identified irregular patterns of bars that the rats can discriminate from the regular one. This novel task shows that freely moving rodents can make simultaneous bilateral tactile discrimination without whisking.SIGNIFICANCE STATEMENT The whisker system of rodents is a widely used model to study tactile processing. Rats show remarkable abilities in discriminating surfaces by actively moving their whiskers (whisking) against stimuli, typically sampling them several times. This motor strategy affects considerably the way that tactile information is acquired and thus the way that neuronal networks process the information. However, when rats run at high speed, they protract their whiskers in front of the snout without large movements. Here, we investigated whether rats are able to discriminate regular and irregular patterns of vertical bars while running without whisking. We found that the animals can perform a bilateral simultaneous discrimination without whisking and that this involves both whiskers and barrel cortex activity.