Evidence for Functional Groupings of Vibrissae across the Rodent Mystacial Pad.

During natural exploration, rats exhibit two particularly conspicuous vibrissal-mediated behaviors: they follow along walls, and "dab" their snouts on the ground at frequencies related to the whisking cycle. In general, the walls and ground may be located at any distance from, and at any orientation relative to, the rat's head, which raises the question of how the rat might determine the position and orientation of these surfaces. Previous studies have compellingly demonstrated that rats can accurately determine the horizontal angle at which a vibrissa first touches an object, and we therefore asked whether this parameter could provide the rat with information about the pitch, distance, and yaw of a surface relative to its head. We used a three-dimensional model of the whisker array to construct mappings between the horizontal angle of contact of each vibrissa and every possible (pitch, distance, and yaw) configuration of the head relative to a flat surface. The mappings revealed striking differences in the patterns of contact for vibrissae in different regions of the array. The exterior (A, D, E) rows provide information about the relative pitch of the surface regardless of distance. The interior (B, C) rows provide distance cues regardless of head pitch. Yaw is linearly correlated with the difference between the number of right and left whiskers touching the surface. Compared to the long reaches that whiskers can make to the side and below the rat, the reachable distance in front of the rat's nose is relatively small. We confirmed key predictions of these functional groupings in a behavioral experiment that monitored the contact patterns that the vibrissae made with a flat vertical surface. These results suggest that vibrissae in different regions of the array are not interchangeable sensors, but rather functionally grouped to acquire particular types of information about the environment.

Probability distributions of whisker-surface contact: quantifying elements of the rat vibrissotactile natural scene.

Analysis of natural scene statistics has been a powerful approach for understanding neural coding in the auditory and visual systems. In the field of somatosensation, it has been more challenging to quantify the natural tactile scene, in part because somatosensory signals are so tightly linked to the animal's movements. The present work takes a step towards quantifying the natural tactile scene for the rat vibrissal system by simulating rat whisking motions to systematically investigate the probabilities of whisker-object contact in naturalistic environments. The simulations permit an exhaustive search through the complete space of possible contact patterns, thereby allowing for the characterization of the patterns that would most likely occur during long sequences of natural exploratory behavior. We specifically quantified the probabilities of 'concomitant contact', that is, given that a particular whisker makes contact with a surface during a whisk, what is the probability that each of the other whiskers will also make contact with the surface during that whisk? Probabilities of concomitant contact were quantified in simulations that assumed increasingly naturalistic conditions: first, the space of all possible head poses; second, the space of behaviorally preferred head poses as measured experimentally; and third, common head poses in environments such as cages and burrows. As environments became more naturalistic, the probability distributions shifted from exhibiting a 'row-wise' structure to a more diagonal structure. Results also reveal that the rat appears to use motor strategies (e.g. head pitches) that generate contact patterns that are particularly well suited to extract information in the presence of uncertainty.

Spatiotemporal Patterns of Contact Across the Rat Vibrissal Array During Exploratory Behavior.

The rat vibrissal system is an important model for the study of somatosensation, but the small size and rapid speed of the vibrissae have precluded measuring precise vibrissal-object contact sequences during behavior. We used a laser light sheet to quantify, with 1 ms resolution, the spatiotemporal structure of whisker-surface contact as five naïve rats freely explored a flat, vertical glass wall. Consistent with previous work, we show that the whisk cycle cannot be uniquely defined because different whiskers often move asynchronously, but that quasi-periodic (~8 Hz) variations in head velocity represent a distinct temporal feature on which to lock analysis. Around times of minimum head velocity, whiskers protract to make contact with the surface, and then sustain contact with the surface for extended durations (~25-60 ms) before detaching. This behavior results in discrete temporal windows in which large numbers of whiskers are in contact with the surface. These "sustained collective contact intervals" (SCCIs) were observed on 100% of whisks for all five rats. The overall spatiotemporal structure of the SCCIs can be qualitatively predicted based on information about head pose and the average whisk cycle. In contrast, precise sequences of whisker-surface contact depend on detailed head and whisker kinematics. Sequences of vibrissal contact were highly variable, equally likely to propagate in all directions across the array. Somewhat more structure was found when sequences of contacts were examined on a row-wise basis. In striking contrast to the high variability associated with contact sequences, a consistent feature of each SCCI was that the contact locations of the whiskers on the glass converged and moved more slowly on the sheet. Together, these findings lead us to propose that the rat uses a strategy of "windowed sampling" to extract an object's spatial features: specifically, the rat spatially integrates quasi-static mechanical signals across whiskers during the period of sustained contact, resembling an "enclosing" haptic procedure.

Simultaneous modeling of visual saliency and value computation improves predictions of economic choice.

Many decisions we make require visually identifying and evaluating numerous alternatives quickly. These usually vary in reward, or value, and in low-level visual properties, such as saliency. Both saliency and value influence the final decision. In particular, saliency affects fixation locations and durations, which are predictive of choices. However, it is unknown how saliency propagates to the final decision. Moreover, the relative influence of saliency and value is unclear. Here we address these questions with an integrated model that combines a perceptual decision process about where and when to look with an economic decision process about what to choose. The perceptual decision process is modeled as a drift-diffusion model (DDM) process for each alternative. Using psychophysical data from a multiple-alternative, forced-choice task, in which subjects have to pick one food item from a crowded display via eye movements, we test four models where each DDM process is driven by (i) saliency or (ii) value alone or (iii) an additive or (iv) a multiplicative combination of both. We find that models including both saliency and value weighted in a one-third to two-thirds ratio (saliency-to-value) significantly outperform models based on either quantity alone. These eye fixation patterns modulate an economic decision process, also described as a DDM process driven by value. Our combined model quantitatively explains fixation patterns and choices with similar or better accuracy than previous models, suggesting that visual saliency has a smaller, but significant, influence than value and that saliency affects choices indirectly through perceptual decisions that modulate economic decisions.

The morphology of the rat vibrissal array: a model for quantifying spatiotemporal patterns of whisker-object contact.

In all sensory modalities, the data acquired by the nervous system is shaped by the biomechanics, material properties, and the morphology of the peripheral sensory organs. The rat vibrissal (whisker) system is one of the premier models in neuroscience to study the relationship between physical embodiment of the sensor array and the neural circuits underlying perception. To date, however, the three-dimensional morphology of the vibrissal array has not been characterized. Quantifying array morphology is important because it directly constrains the mechanosensory inputs that will be generated during behavior. These inputs in turn shape all subsequent neural processing in the vibrissal-trigeminal system, from the trigeminal ganglion to primary somatosensory ("barrel") cortex. Here we develop a set of equations for the morphology of the vibrissal array that accurately describes the location of every point on every whisker to within ±5% of the whisker length. Given only a whisker's identity (row and column location within the array), the equations establish the whisker's two-dimensional (2D) shape as well as three-dimensional (3D) position and orientation. The equations were developed via parameterization of 2D and 3D scans of six rat vibrissal arrays, and the parameters were specifically chosen to be consistent with those commonly measured in behavioral studies. The final morphological model was used to simulate the contact patterns that would be generated as a rat uses its whiskers to tactually explore objects with varying curvatures. The simulations demonstrate that altering the morphology of the array changes the relationship between the sensory signals acquired and the curvature of the object. The morphology of the vibrissal array thus directly constrains the nature of the neural computations that can be associated with extraction of a particular object feature. These results illustrate the key role that the physical embodiment of the sensor array plays in the sensing process.

Variability in velocity profiles during free-air whisking behavior of unrestrained rats.

During exploratory behaviors, the velocity of an organism's sensory surfaces can have a pronounced effect on the incoming flow of sensory information. In this study, we quantified variability in the velocity profiles of rat whisking during natural exploratory behavior that included head rotations. A wide continuum of profiles was observed, including monotonic, delayed, and reversing velocities during protractions and retractions. Three alternative hypotheses for the function of the variable velocity profiles were tested: 1) that they produce bilateral asymmetry specifically correlated with rotational head velocity, 2) that they serve to generate bilaterally asymmetric and/or asynchronous whisker movements independent of head velocity, and 3) that the different profiles--despite increasing variability in instantaneous velocity--reduce variability in the average whisking velocity. Our results favor the third hypothesis and do not support the first two. Specifically, the velocity variability within a whisk can be observed as a shift in the phase of the maximum velocity. We discuss the implications of these results for the control of whisker motion, horizontal object localization, and processing in the thalamus and cortex of the rat vibrissal system.

Biomechanical models for radial distance determination by the rat vibrissal system.

Rats use active, rhythmic movements of their whiskers to acquire tactile information about three-dimensional object features. There are no receptors along the length of the whisker; therefore all tactile information must be mechanically transduced back to receptors at the whisker base. This raises the question: how might the rat determine the radial contact position of an object along the whisker? We developed two complementary biomechanical models that show that the rat could determine radial object distance by monitoring the rate of change of moment (or equivalently, the rate of change of curvature) at the whisker base. The first model is used to explore the effects of taper and inherent whisker curvature on whisker deformation and used to predict the shapes of real rat whiskers during deflections at different radial distances. Predicted shapes closely matched experimental measurements. The second model describes the relationship between radial object distance and the rate of change of moment at the base of a tapered, inherently curved whisker. Together, these models can account for recent recordings showing that some trigeminal ganglion (Vg) neurons encode closer radial distances with increased firing rates. The models also suggest that four and only four physical variables at the whisker base -- angular position, angular velocity, moment, and rate of change of moment -- are needed to describe the dynamic state of a whisker. We interpret these results in the context of our evolving hypothesis that neural responses in Vg can be represented using a state-encoding scheme that includes combinations of these four variables.

Right-left asymmetries in the whisking behavior of rats anticipate head movements.

Rats use rhythmic movements of their vibrissae (whiskers) to tactually explore their environment. This "whisking" behavior has generally been reported to be strictly synchronous and symmetric about the snout, and it is thought to be controlled by a brainstem central pattern generator. Because the vibrissae can move independently of the head, however, maintaining a stable perception of the world would seem to require that rats adjust the bilateral symmetry of whisker movements in response to head movements. The present study used high-speed videography to reveal dramatic bilateral asymmetries and asynchronies in free-air whisking during head rotations. Kinematic analysis suggested that these asymmetric movements did not serve to maintain any fixed temporal relationship between right and left arrays, but rather to redirect the whiskers to a different region of space. More specifically, spatial asymmetry was found to be strongly correlated with rotational head velocity, ensuring a "look-ahead" distance of almost exactly one whisk. In contrast, bilateral asynchrony and velocity asymmetry were only weakly dependent on head velocity. Bilateral phase difference was found to be independent of the whisking frequency, suggesting the presence of two distinct left and right central pattern generators, connected as coupled oscillators. We suggest that the spatial asymmetries are analogous to the saccade that occurs during the initial portion of a combined head-eye gaze shift, and we begin to develop the rat vibrissal system as a new model for studying vestibular and proprioceptive contributions to the acquisition of sensory data.

Mechanical characteristics of rat vibrissae: resonant frequencies and damping in isolated whiskers and in the awake behaving animal.

We investigated the natural resonance properties and damping characteristics of rat macrovibrissae (whiskers). Isolated whiskers rigidly fixed at the base showed first-mode resonance peaks between 27 and 260 Hz, principally depending on whisker length. These experimentally measured resonant frequencies were matched using a theoretical model of the whisker as a conical cantilever beam, with Young's modulus as the only free parameter. The best estimate for Young's modulus was approximately 3-4 GPa. Results of both vibration and impulse experiments showed that the whiskers are strongly damped, with damping ratios between 0.11 and 0.17. In the behaving animal, whiskers that deflected past an object were observed to resonate but were damped significantly more than isolated whiskers. The time course of damping varied depending on the individual whisker and the phase of the whisking cycle, which suggests that the rat may modulate biomechanical parameters that affect damping. No resonances were observed for whiskers that did not contact the object or during free whisking in air. Finally, whiskers on the same side of the face were sometimes observed to move in opposite directions over the full duration of a whisk. We discuss the potential roles of resonance during natural exploratory behavior and specifically suggest that resonant oscillations may be important in the rat's tactile detection of object boundaries.