R. Blythe Towal

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.

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 whiskers identity (row and column location within the array), the equations establish the whiskers 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 organisms 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.

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

Significance Many everyday decisions require viewing displays with several alternatives and then rapidly choosing one, e.g., choosing a snack from a vending machine. Each item has objective visual properties, such as saliency, and subjective properties, such as value. Objective and subjective properties are usually studied independently. We have implemented a single integrated paradigm that links perceptual with economic decision making by having subjects search through visual displays to choose a single food item that they want to eat. We demonstrate that two linked accumulator models, one modeling perceptual and the other modeling economic decisions, account for subjects’ viewing patterns and choices. 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.

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 objects spatial features: specifically, the rat spatially integrates quasi-static mechanical signals across whiskers during the period of sustained contact, resembling an “enclosing” haptic procedure.

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.

Principles and applications of active tactile sensing strategies in the rat vibrissal system

The importance of active sensing to animals suggests that it may confer significant advantages to engineered sensing systems. The rat vibrissal (whisker) system is an important model for studying tactile active sensing. To date, however, the small size and fast speeds of the whiskers have precluded characterization of the rats exploratory strategies. We have developed novel optical instrumentation that has allowed one of the first quantifications of tactile sampling during rat exploratory behavior. Results reveal characteristics of vibrissal active sensing that may find application in artificial tactile sensing systems; for example, the morphology of the whisker array allows rats to sample at multiple spatial scales within a single sampling cycle. Here, we describe the design and implementation of the novel optical system and how it is helping to uncover sampling strategies in this biological system.

Simultaneous modeling of èisual saliency and èalue computation improèes predictions of economic choice

Significance Many everyday decisions require viewing displays with several alternatives and then rapidly choosing one, e.g., choosing a snack from a vending machine. Each item has objective visual properties, such as saliency, and subjective properties, such as value. Objective and subjective properties are usually studied independently. We have implemented a single integrated paradigm that links perceptual with economic decision making by having subjects search through visual displays to choose a single food item that they want to eat. We demonstrate that two linked accumulator models, one modeling perceptual and the other modeling economic decisions, account for subjects’ viewing patterns and choices. 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.

From the Cover: PNAS Plus: Simultaneous modeling of visual saliency and value computation improves predictions of economic choice

Significance Many everyday decisions require viewing displays with several alternatives and then rapidly choosing one, e.g., choosing a snack from a vending machine. Each item has objective visual properties, such as saliency, and subjective properties, such as value. Objective and subjective properties are usually studied independently. We have implemented a single integrated paradigm that links perceptual with economic decision making by having subjects search through visual displays to choose a single food item that they want to eat. We demonstrate that two linked accumulator models, one modeling perceptual and the other modeling economic decisions, account for subjects’ viewing patterns and choices. 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.

Active sensing: Head and vibrissal velocity during exploratory behaviors of the rat

The vibrissal-trigeminal pathway of the rat has become an increasingly important model in neuroscience to study how sensory and motor signals are encoded, processed, and integrated in the nervous system, ultimately yielding “perception“ of an object. In this chapter, we focus specifically on the role of head and vibrissa (whisker) velocity during exploratory movements. The chapter begins by describing basic vibrissal anatomy and mechanics, and shows that different studies measure “vibrissa velocity“ under very different mechanical conditions, which will give rise to very different types of mechanoreceptor activation. It is thus critical to consider forces and bending moments at the whisker base in addition to vibrissa velocity when quantifying vibrissa-object contact during natural behavior. To illustrate this point, we summarize recent results demonstrating that whisking velocity at the time of collision with an object may influence the rat’s ability to determine the radial distance to the object as well as the horizontal angle of contact. Further, we present evidence suggesting that the rat may actively select velocities at different points in the whisking trajectory, perhaps to aid localization behavior in these two dimensions. Finally, because the whiskers are always acting in concert with the head, we describe correlations between whisking behavior and head velocity. Preliminary data suggest that the position, orientation, and velocity of the head — which moves at a very different spatial and temporal scale than the vibrissae — will have a large effect on the tactile information acquired by the vibrissal system.