Motor Cortex Latent Dynamics Encode Spatial and Temporal Arm Movement Parameters Independently.

The fluid movement of an arm requires multiple spatiotemporal parameters to be set independently. Recent studies have argued that arm movements are generated by the collective dynamics of neurons in motor cortex. An untested prediction of this hypothesis is that independent parameters of movement must map to independent components of the neural dynamics. Using a task where three male monkeys made a sequence of reaching movements to randomly placed targets, we show that the spatial and temporal parameters of arm movements are independently encoded in the low-dimensional trajectories of population activity in motor cortex: each movement's direction corresponds to a fixed neural trajectory through neural state space and its speed to how quickly that trajectory is traversed. Recurrent neural network models show that this coding allows independent control over the spatial and temporal parameters of movement by separate network parameters. Our results support a key prediction of the dynamical systems view of motor cortex, and also argue that not all parameters of movement are defined by different trajectories of population activity.

Correction: A system for tracking whisker kinematics and whisker shape in three dimensions.

[This corrects the article DOI: 10.1371/journal.pcbi.1007402.].

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

Quantification of behaviour is essential for biology. Since the whisker system is a popular model, it is important to have methods for measuring whisker movements from behaving animals. Here, we developed a high-speed imaging system that measures whisker movements simultaneously from two vantage points. We developed a whisker tracker algorithm that automatically reconstructs 3D whisker information directly from the 'stereo' video data. The tracker is controlled via a Graphical User Interface that also allows user-friendly curation. The algorithm tracks whiskers, by fitting a 3D Bezier curve to the basal section of each target whisker. By using prior knowledge of natural whisker motion and natural whisker shape to constrain the fits and by minimising the number of fitted parameters, the algorithm is able to track multiple whiskers in parallel with low error rate. We used the output of the tracker to produce a 3D description of each tracked whisker, including its 3D orientation and 3D shape, as well as bending-related mechanical force. In conclusion, we present a non-invasive, automatic system to track whiskers in 3D from high-speed video, creating the opportunity for comprehensive 3D analysis of sensorimotor behaviour and its neural basis.

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

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.

Sensory adaptation in the barrel cortex during active sensation in the behaving mouse.

Sensory Adaptation (SA) is a prominent aspect of how neurons respond to sensory signals, ubiquitous across species and modalities. However, SA depends on the activation state of the brain and the extent to which SA is expressed in awake, behaving animals during active sensation remains unclear. Here, we addressed this question by training head-fixed mice to detect an object using their whiskers and recording neuronal activity from barrel cortex whilst simultaneously imaging the whiskers in 3D. We found that neuronal responses decreased during the course of whisker-object touch sequences and that this was due to two factors. First, a motor effect, whereby, during a sequence of touches, later touches were mechanically weaker than early ones. Second, a sensory encoding effect, whereby neuronal tuning to touch became progressively less sensitive during the course of a touch sequence. The sensory encoding effect was whisker-specific. These results show that SA does occur during active whisker sensing and suggest that SA is fundamental to sensation during natural behaviour.

Motor cortex latent dynamics encode arm movement direction and urgency independently.

The fluid movement of an arm is controlled by multiple parameters that can be set independently. Recent studies argue that arm movements are generated by the collective dynamics of neurons in motor cortex. An untested prediction of this hypothesis is that independent parameters of movement must map to independently-specifiable dynamics. Using a task where monkeys made sequential, varied arm movements, we show that independent parameters of arm movements are independently encoded in the low-dimensional trajectories of population activity: each movement's direction by a fixed neural trajectory and its urgency by how quickly that trajectory was traversed. Network models show this latent coding allows the direction and urgency of arm movement to be independently controlled. Our results support a key prediction of the dynamical systems view of motor cortex, but also argue that not all parameters of movement are defined by the initial conditions of those dynamics.