Prediction of Choice from Competing Mechanosensory and Choice-Memory Cues during Active Tactile Decision Making

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. Male mice were trained to localize 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 mechanosensory and choice-memory signals, and provides a new task well suited for the 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 behavior. Here we train mice in a novel behavioral 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 behavioral choices.

The Sensorimotor Basis of Whisker-Guided Anteroposterior Object Localization in Head-Fixed Mice

“…Alternatively, reward or choice history may influence choice during these types of tasks. A recent study of whisker-based object localization found that choice history had a significant influence on error trials [25]. However, we were unable to find an influence of choice history on choice in our current study.…”

“…Achieving this hyperacute localization resolution is not trivial. Head-fixed mice can also discriminate well-separated anteroposterior locations ($15 ) with a single whisker [23] using motor strategies that establish large differences in touch likelihood [24] or direction [25] between locations. The perceptual limits, motor strategies, and sensorimotor features that drive hyperacute object location perception remain unclear.…”

A system for tracking whisker kinematics and whisker shape in three dimensions

“…Since there was only one whisker, coordinates describing the whisker in one plane could be uniquely matched to those in the other plane. However, manual tracking is impractical for large data sets [6,7,9,11,14]. In sum, no method currently exists that achieves automatic and non-invasive tracking of multiple whiskers in 3D.…”

“…Previous studies have sought to measure the bending moment related to whisker-object contact by imaging in the horizontal plane [6,7,[9][10][11]14,24,25]. However, there are limitations of the planar imaging approach.…”

“…Since the whisker system is a major experimental model and since the whiskers are readily imageable [3,4], the whisker system is ideally suited to this endeavour. Tracking the whiskers of mice/rats has already deepened our understanding of active sensation and refined our capacity to relate behaviour to neural mechanisms [5][6][7][8][9][10][11][12][13][14]. Our aim here was to develop a method to track whisker movements and whisker shape in 3D in behaving mice at millisecond temporal resolution.…”