A fundamental question in the investigation of any sensory system is what physical signals drive its sensory neurons during natural behavior. Surprisingly, in the whisker system, it is only recently that answers to this question have emerged. Here, we review the key developments, focussing mainly on the first stage of the ascending pathway - the primary whisker afferents (PWAs). We first consider a biomechanical framework, which describes the fundamental mechanical forces acting on the whiskers during active sensation. We then discuss technical progress that has allowed such mechanical variables to be estimated in awake, behaving animals. We discuss past electrophysiological evidence concerning how PWAs function and reinterpret it within the biomechanical framework. Finally, we consider recent studies of PWAs in awake, behaving animals and compare the results to related studies of the cortex. We argue that understanding 'what the whiskers tell the brain' sheds valuable light on the computational functions of downstream neural circuits, in particular, the barrel cortex.

The topography of the cerebellar cortex is described by at least three different maps, with the basic units of each map termed "microzones," "patches," and "bands." These are defined, respectively, by different patterns of climbing fiber input, mossy fiber input, and Purkinje cell (PC) phenotype. Based on embryological development, the "one-map" hypothesis proposes that the basic units of each map align in the adult animal and the aim of the present study was to test this possibility. In barbiturate anesthetized adult rats, nanoinjections of bidirectional tracer (Retrobeads and biotinylated dextran amine) were made into somatotopically identified regions within the hindlimb C1 zone in copula pyramidis. Injection sites were mapped relative to PC bands defined by the molecular marker zebrin II and were correlated with the pattern of retrograde cell labeling within the inferior olive and in the basilar pontine nuclei to determine connectivity of microzones and patches, respectively, and also with the distributions of biotinylated dextran amine-labeled PC terminals in the cerebellar nuclei. Zebrin bands were found to be related to both climbing fiber and mossy fiber inputs and also to cortical representation of different parts of the ipsilateral hindpaw, indicating a precise spatial organization within cerebellar microcircuitry. This precise connectivity extends to PC terminal fields in the cerebellar nuclei and olivonuclear projections. These findings strongly support the one-map hypothesis and suggest that, at the microcircuit level of resolution, the cerebellar cortex has a common plan of spatial organization for major inputs, outputs, and PC phenotype.

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 noninvasive, 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.

25Quantification of behaviour is essential for systems neuroscience. Since the whisker system is a major model system for 26 investigating the neural basis of behaviour, it is important to have methods for measuring whisker movements from 27 behaving animals. Here, we developed a high-speed imaging system that measures whisker movements simultaneously 28 from two vantage points. We developed an algorithm that uses the 'stereo' video data to track multiple whiskers by 29 fitting 3D curves to the basal section of each target whisker. By using temporal information to constrain the fits, the 30 algorithm is able to track multiple whiskers in parallel with low error rate. We used the output of the tracker to produce a 31 3D description of each tracked whisker, including its 3D orientation and 3D shape, as well as bending-related mechanical 32 force. In conclusion, we present an automatic system to track whiskers in 3D from high-speed video, creating the 33 opportunity for comprehensive 3D analysis of sensorimotor behaviour and its neural basis. 34 Author summary 35The great ethologist Niko Tinbergen described a crucial challenge in biology to measure the "total movements made by 36 the intact animal". Advances in high-speed video and machine analysis of such data have made it possible to make 37 profound advances. Here, we target the whisker system. The whisker system is a major experimental model in 38 neurobiology and, since the whiskers are readily imageable, the system is ideally suited to machine vision. Rats and mice 39 explore their environment by sweeping their whiskers to and fro. It is important to measure whisker movements in 3D, 40 since whiskers move in 3D and since the mechanical forces that act on them are 3D. However, the problem of 41 automatically tracking whiskers in 3D from video has generally been regarded as prohibitively difficult. Our innovation 42 here is to extract 3D information about whiskers using a two-camera, high-speed imaging system and to develop 43 computational methods to infer 3D whisker state from the imaging data. Our hope is that this study will facilitate 44 comprehensive, 3D analysis of whisker behaviour and, more generally, contribute new insight into brain mechanisms of 45 perception and behaviour. 46 47 48 50 Substantial progress towards the long-standing ambition of measuring "total movements made by the intact animal" (1) is 51 coming from the application of powerful machine vision methods to video recordings of behaving animals (2). Since the 52 whisker system is a major experimental model in neuroscience and since the whiskers are readily imageable (3,4), the 53 whisker system is ideally suited to this endeavour. Tracking the whiskers of mice/rats has already deepened our 54 understanding of active sensation and refined our capacity to relate behaviour to neural mechanisms (5-10) Our aim here 55 was to develop a method to track whisker movements and whisker shape in 3D in behaving mice at millisecond temporal 56 resolution. 57Whisker movement is 3D. During each whisking...

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.