Whisking and whisker kinematics during a texture classification task

Rats explore objects by rhythmically whisking with their vibrissae. The goal of the present study is to learn more about the motor output used by rats to acquire texture information as well as the whisker motion evoked by texture contact. We trained four rats to discriminate between different grooved textures and used high-speed video to characterize whisker motion during the task. The variance in whisking parameters among subjects was notable. After whisker trimming, the animals changed their behaviour in ways that appear consistent with an optimization of whisker movement to compensate for lost information. These results lead to the intriguing notion that the rats use an information-seeking 'cognitive' motor strategy, instead of a rigid motor programme. Distinct stick/slip events occurred during texture palpation and their frequency increased in relation to the spatial frequency of the grooves. The results allow a preliminary assessment of three candidate texture-coding mechanisms-the number of grooves encountered during each touch, the temporal difference between groove contacts and the spatial pattern of groove contacts across the whiskers.     

Vibrissal kinematics in 3D: tight coupling of azimuth, elevation, and torsion across different whisking modes

Perception is usually an active process by which action selects and affects sensory information. During rodent active touch, whisker kinematics influences how objects activate sensory receptors. In order to fully characterize whisker motion, we reconstructed whisker position in 3D and decomposed whisker motion to all its degrees of freedom. We found that, across behavioral modes, in both head-fixed and freely moving rats, whisker motion is characterized by translational movements and three rotary components: azimuth, elevation, and torsion. Whisker torsion, which has not previously been described, was large (up to 100 degrees), and torsional angles were highly correlated with whisker azimuths. The coupling of azimuth and torsion was consistent across whisking epochs and rats and was similar along rows but systematically varied across rows such that rows A and E counterrotated. Torsional rotation of the whiskers enables contact information to be mapped onto the circumference of the whisker follicles in a predictable manner across protraction-retraction cycles.     

Neuronal encoding of texture in the whisker sensory pathway

A major challenge of sensory systems neuroscience is to quantify brain activity underlying perceptual experiences and to explain this activity as the outcome of elemental neuronal response properties. Rats make extremely fine discriminations of texture by “whisking” their vibrissae across an object's surface, yet the neuronal coding underlying texture sensations remains unknown. Measuring whisker vibrations during active whisking across surfaces, we found that each texture results in a unique “kinetic signature” defined by the temporal profile of whisker velocity. We presented these texture-induced vibrations as stimuli while recording responses of first-order sensory neurons and neurons in the whisker area of cerebral cortex. Each texture is encoded by a distinctive, temporally precise firing pattern. To look for the neuronal coding properties that give rise to texture-specific firing patterns, we delivered horizontal and vertical whisker movements that varied randomly in time (“white noise”) and found that the response probabilities of first-order neurons and cortical neurons vary systematically according to whisker speed and direction. We applied the velocity-tuned spike probabilities derived from white noise to the sequence of velocity features in the texture to construct a simulated texture response. The close match between the simulated and real responses indicates that texture coding originates in the selectivity of neurons to elemental kinetic events.     

Topography of whisking II: interaction of whisker and pad

The peripheral effector system mediating rodent whisking produces protraction/retraction movements of the whiskers and translation movements of the collagenous mystacial pad. To examine the interaction of these movements during whisking in air we used high-resolution, optoelectronic methods for two-dimensional monitoring of whisker and pad movements in head-fixed rats. Under these testing conditions (1) whisker movements on the same side of the face are synchronous and of similar amplitude; (2) pad movements exhibit the characteristic 'exploratory' rhythm (6-12 Hz) of whisking but their movements often have a low frequency (1-2 Hz) component; (3) Pad movements occur in both antero-posterior and dorso-ventral planes but there are considerable variations in the amplitude and topography of movement parameters in the two planes. We conclude that (a) both whisker and pad receive input from a common central rhythm generator; (b) differences in whisker and pad amplitude and topography probably reflect differences in the biomechanical properties of the structures receiving that input; (c) pad movements make a significant contribution to the kinematics of whisking behavior and (d) the two-dimensional nature of pad translation movements significantly increases the rat's flexible control of its mobile sensor.     

Whisker motor cortex ablation and whisker movement patterns

Previous studies, based on qualitative observations, reported that lesions of the whisker motor cortex produce no deficits in whisking behavior. We used high-resolution optoelectronic recording methods to compare the temporal organization and kinematics of whisker movements before and after unilateral lesions of whisker motor cortex in rats. We now report that while the lesion did not abolish whisking, it significantly disrupted whisking kinematics, coordination, and temporal organization. Lesioned animals showed significant increases in the velocity and amplitude of whisker protractions contralateral to the lesions, as well as a reduction in the synchrony of whisker movements on the two sides of the face. There was a marked shift in the distribution of whisking frequencies, with reduction of activity in the 5-7 Hz bandwidth and increased activity at < 2 Hz. Disruptions of the normal whisking pattern were evident on both sides of the face, and the magnitude of these effects was proportional to the extent of the cortical ablation. We suggest that the observed deficits reflect an imbalance in cortical inputs to a brainstem central pattern generator.     

Temporal organization of multi-whisker contact in rats

Previous work has established that during exploration and discrimination, rats move their whiskers at frequencies between 6 and 12 Hz and that whisking frequency changes during contact. One critical component of any tactile system is contact. In the rat whisker system, such contacts may involve one or more vibrissa in the whisker array and contact duration of each whisker may vary over a considerable range, depending upon the behavioral context. However, little is known about the variables controlling contact duration or about the temporal relationships among contacts by adjacent whiskers. To address these issues head fixed rats were trained to touch a piezo-contact-sensor with the shaft of their whiskers (Bermejo and Zeigler, Somatosens Mot Res 17: 373-377, 2000 ). During the task, whisker movements and contacts were monitored with a high-speed camera at 500 frames/s and stored on videotape. To facilitate analysis, animals had their whiskers selectively trimmed. Data are reported from animals with C1 & C2, D1 & D2, or Arc2 (E2, D2, C2, B2) whiskers intact. For both row and arc animals, when just a single whisker touched the sensor the duration of contact was significantly shorter than when multiple whiskers made contact. When multiple whiskers made contact, onset was rarely simultaneous. Furthermore, in row-intact animals, contact progressed in an orderly fashion such that the rostral whisker in a row made contact first followed 24 ms (SE = 1.9 ms) later by the caudal whisker. When contact reversed the caudal whisker lifted off first, followed by the rostral whisker. Thus, the order in which whiskers touch an object regulates contact duration: the first whisker to touch the sensor stays in contact longer than any other whisker. The temporal discharge properties of neurons in the trigeminal system are expected to reflect position of whiskers on the nose.     

Whisker motor cortex ablation and whisker movement patterns

Previous studies, based on qualitative observations, reported that lesions of the whisker motor cortex produce no deficits in whisking behavior. We used high-resolution optoelectronic recording methods to compare the temporal organization and kinematics of whisker movements before and after unilateral lesions of whisker motor cortex in rats. We now report that while the lesion did not abolish whisking, it significantly disrupted whisking kinematics, coordination, and temporal organization. Lesioned animals showed significant increases in the velocity and amplitude of whisker protractions contralateral to the lesions, as well as a reduction in the synchrony of whisker movements on the two sides of the face. There was a marked shift in the distribution of whisking frequencies, with reduction of activity in the 5–7?Hz bandwidth and increased activity at <?2?Hz. Disruptions of the normal whisking pattern were evident on both sides of the face, and the magnitude of these effects was proportional to the extent of the cortical ablation. We suggest that the observed deficits reflect an imbalance in cortical inputs to a brainstem central pattern generator.     

Active vibrissal sensing in rodents and marsupials

In rats, the long facial whiskers (mystacial macrovibrissae) are repetitively and rapidly swept back and forth during exploration in a behaviour known as 'whisking'. In this paper, we summarize previous evidence from rats, and present new data for rat, mouse and the marsupial grey short-tailed opossum (Monodelphis domestica) showing that whisking in all three species is actively controlled both with respect to movement of the animal's body and relative to environmental structure. Using automatic whisker tracking, and Fourier analysis, we first show that the whisking motion of the mystacial vibrissae, in the horizontal plane, can be approximated as a blend of two sinusoids at the fundamental frequency (mean 8.5, 11.3 and 7.3 Hz in rat, mouse and opossum, respectively) and its second harmonic. The oscillation at the second harmonic is particularly strong in mouse (around 22 Hz) consistent with previous reports of fast whisking in that species. In all three species, we found evidence of asymmetric whisking during head turning and following unilateral object contacts consistent with active control of whisker movement. We propose that the presence of active vibrissal touch in both rodents and marsupials suggests that this behavioural capacity emerged at an early stage in the evolution of therian mammals.     

Serotonin regulates rhythmic whisking

Many rodents explore their environment by rhythmically palpating objects with their mystacial whiskers. These rhythmic whisker movements ("whisking"; 5-9 Hz) are thought to be regulated by an unknown brainstem central pattern generator (CPG). We tested the hypothesis that serotonin (5-HT) inputs to whisking facial motoneurons (wFMNs) are part of this CPG. In response to exogenous serotonin, wFMNs recorded in vitro fire rhythmically at whisking frequencies, and selective 5-HT2 or 5-HT3 receptor antagonists suppress this rhythmic firing. In vivo, stimulation of brainstem serotonergic raphe nuclei evokes whisker movements. Unilateral infusion of selective 5-HT2 or 5-HT3 receptor antagonists suppresses ipsilateral whisking and substantially alters the frequencies and symmetry of whisker movements. These findings suggest that serotonin is both necessary and sufficient to generate rhythmic whisker movements and that serotonergic premotoneurons are part of a whisking CPG.     

Temporal organization of multi-whisker contact in rats

Previous work has established that during exploration and discrimination, rats move their whiskers at frequencies between 6 and 12 Hz and that whisking frequency changes during contact. One critical component of any tactile system is contact. In the rat whisker system, such contacts may involve one or more vibrissa in the whisker array and contact duration of each whisker may vary over a considerable range, depending upon the behavioral context. However, little is known about the variables controlling contact duration or about the temporal relationships among contacts by adjacent whiskers. To address these issues head fixed rats were trained to touch a piezo-contact-sensor with the shaft of their whiskers (Bermejo and Zeigler, Somatosens Mot Res 17: 373-377, 2000). During the task, whisker movements and contacts were monitored with a high-speed camera at 500 frames/s and stored on videotape. To facilitate analysis, animals had their whiskers selectively trimmed. Data are reported from animals with C1 & C2, D1 & D2, or Arc2 (E2, D2, C2, B2) whiskers intact. For both row and arc animals, when just a single whisker touched the sensor the duration of contact was significantly shorter than when multiple whiskers made contact. When multiple whiskers made contact, onset was rarely simultaneous. Furthermore, in row-intact animals, contact progressed in an orderly fashion such that the rostral whisker in a row made contact first followed 24 ms (SE = 1.9 ms) later by the caudal whisker. When contact reversed the caudal whisker lifted off first, followed by the rostral whisker. Thus, the order in which whiskers touch an object regulates contact duration: the first whisker to touch the sensor stays in contact longer than any other whisker. The temporal discharge properties of neurons in the trigeminal system are expected to reflect position of whiskers on the nose.     

"Real-time" monitoring of vibrissa contacts during rodent whisking

Rodent whisking behavior provides active touch as input into a widely studied model system of information processing and behavior. We previously developed a simple optoelectronic system to monitor whisker movements in "real time" in head held rats at rest or performing various tasks such as tactile discrimination. We now describe a simple piezioelectic film device for detecting initial whisker contacts during whisking also in real time. In some applications this is as effective as high-speed videos and can be configured to isolate the contacts from different whiskers. The construction of this simple device is detailed. In addition to providing information during recordings from awake animals, the device could be used, for example, as an operant "manipulandum" for contingent reinforcement of object detection with a whisker.     

Whisker primary afferents encode temporal frequency of moving gratings

To investigate the encoding of behaviorally relevant stimuli in the rodent whisker-somatosensory system, we recorded responses to moving gratings from trigeminal ganglion neurons. This allowed us to quantify how spike patterns in these neurons encode behaviorally distinguishable tactile stimuli presented with the variability inherent in a freely moving whisker paradigm. Our stimulus set consisted of three grating plates with raised bars of the same thickness (275 microm) having different spatial periods (1.0, 1.1, and 1.5 mm) swept rostro-caudally past the whiskers at velocities ranging from 50 to 330 mm/s. This resulted in 20 presentations each of nine different temporal frequencies (ranging from 50 to 220 Hz) for every grating plate. We found that despite the additional degrees of freedom introduced in this freely moving whisker paradigm, firing patterns from the majority (83%) of trigeminal ganglion neurons were statistically distinguishable, and corresponded to the temporal frequency of stimulation. The range of velocities (100-160 mm/s) that resulted in the most accurate and least variable representation of stimulus temporal frequency by trigeminal firing patterns closely corresponds to the whisking velocities employed by trained rats performing similar discrimination tasks. This suggests that, during naturally occurring whisking, individual primary afferents faithfully encode temporal frequency evoked by whisker contacts.     

“Real-time” monitoring of vibrissa contacts during rodent whisking

Rodent whisking behavior provides active touch as input into a widely studied model system of information processing and behavior. We previously developed a simple optoelectronic system to monitor whisker movements in “real time” in head held rats at rest or performing various tasks such as tactile discrimination. We now describe a simple piezioelectic film device for detecting initial whisker contacts during whisking also in real time. In some applications this is as effective as high-speed videos and can be configured to isolate the contacts from different whiskers. The construction of this simple device is detailed. In addition to providing information during recordings from awake animals, the device could be used, for example, as an operant manipulandum for contingent reinforcement of object detection with a whisker.     

Parallel thalamic pathways for whisking and touch signals in the rat

In active sensation, sensory information is acquired via movements of sensory organs; rats move their whiskers repetitively to scan the environment, thus detecting, localizing, and identifying objects. Sensory information, in turn, affects future motor movements. How this motor-sensory-motor functional loop is implemented across anatomical loops of the whisker system is not yet known. While inducing artificial whisking in anesthetized rats, we recorded the activity of individual neurons from three thalamic nuclei of the whisker system, each belonging to a different major afferent pathway: paralemniscal, extralemniscal (a recently discovered pathway), or lemniscal. We found that different sensory signals related to active touch are conveyed separately via the thalamus by these three parallel afferent pathways. The paralemniscal pathway conveys sensor motion (whisking) signals, the extralemniscal conveys contact (touch) signals, and the lemniscal pathway conveys combined whisking–touch signals. This functional segregation of anatomical pathways raises the possibility that different sensory-motor processes, such as those related to motion control, object localization, and object identification, are implemented along different motor-sensory-motor loops.     

Neuronal activity in rat barrel cortex underlying texture discrimination

Rats and mice palpate objects with their whiskers to generate tactile sensations. This form of active sensing endows the animals with the capacity for fast and accurate texture discrimination. The present work is aimed at understanding the nature of the underlying cortical signals. We recorded neuronal activity from barrel cortex while rats used their whiskers to discriminate between rough and smooth textures. On whisker contact with either texture, firing rate increased by a factor of two to ten. Average firing rate was significantly higher for rough than for smooth textures, and we therefore propose firing rate as the fundamental coding mechanism. The rat, however, cannot take an average across trials, but must make an immediate decision using the signals generated on each trial. To estimate single-trial signals, we calculated the mutual information between stimulus and firing rate in the time window leading to the rat's observed choice. Activity during the last 75 ms before choice transmitted the most informative signal; in this window, neuronal clusters carried, on average, 0.03 bits of information about the stimulus on trials in which the rat's behavioral response was correct. To understand how cortical activity guides behavior, we examined responses in incorrect trials and found that, in contrast to correct trials, neuronal firing rate was higher for smooth than for rough textures. Analysis of high-speed films suggested that the inappropriate signal on incorrect trials was due, at least in part, to nonoptimal whisker contact. In conclusion, these data suggest that barrel cortex firing rate on each trial leads directly to the animal's judgment of texture.     

Coherence between Rat Sensorimotor System and Hippocampus Is Enhanced during Tactile Discrimination

Rhythms with time scales of multiple cycles per second permeate the mammalian brain, yet neuroscientists are not certain of their functional roles. One leading idea is that coherent oscillation between two brain regions facilitates the exchange of information between them. In rats, the hippocampus and the vibrissal sensorimotor system both are characterized by rhythmic oscillation in the theta range, 5–12 Hz. Previous work has been divided as to whether the two rhythms are independent or coherent. To resolve this question, we acquired three measures from rats—whisker motion, hippocampal local field potential (LFP), and barrel cortex unit firing—during a whisker-mediated texture discrimination task and during control conditions (not engaged in a whisker-mediated memory task). Compared to control conditions, the theta band of hippocampal LFP showed a marked increase in power as the rats approached and then palpated the texture. Phase synchronization between whisking and hippocampal LFP increased by almost 50% during approach and texture palpation. In addition, a greater proportion of barrel cortex neurons showed firing that was phase-locked to hippocampal theta while rats were engaged in the discrimination task. Consistent with a behavioral consequence of phase synchronization, the rats identified the texture more rapidly and with lower error likelihood on trials in which there was an increase in theta-whisking coherence at the moment of texture palpation. These results suggest that coherence between the whisking rhythm, barrel cortex firing, and hippocampal LFP is augmented selectively during epochs in which the rat collects sensory information and that such coherence enhances the efficiency of integration of stimulus information into memory and decision-making centers.     

Millisecond-timescale local network coding in the rat primary somatosensory cortex

Correlation among neocortical neurons is thought to play an indispensable role in mediating sensory processing of external stimuli. The role of temporal precision in this correlation has been hypothesized to enhance information flow along sensory pathways. Its role in mediating the integration of information at the output of these pathways, however, remains poorly understood. Here, we examined spike timing correlation between simultaneously recorded layer V neurons within and across columns of the primary somatosensory cortex of anesthetized rats during unilateral whisker stimulation. We used bayesian statistics and information theory to quantify the causal influence between the recorded cells with millisecond precision. For each stimulated whisker, we inferred stable, whisker-specific, dynamic bayesian networks over many repeated trials, with network similarity of 83.3±6% within whisker, compared to only 50.3±18% across whiskers. These networks further provided information about whisker identity that was approximately 6 times higher than what was provided by the latency to first spike and 13 times higher than what was provided by the spike count of individual neurons examined separately. Furthermore, prediction of individual neurons' precise firing conditioned on knowledge of putative pre-synaptic cell firing was 3 times higher than predictions conditioned on stimulus onset alone. Taken together, these results suggest the presence of a temporally precise network coding mechanism that integrates information across neighboring columns within layer V about vibrissa position and whisking kinetics to mediate whisker movement by motor areas innervated by layer V.     

Tactile Modulation of Whisking via the Brainstem Loop: Statechart Modeling and Experimental Validation

Rats repeatedly sweep their facial whiskers back and forth in order to explore their environment. Such explorative whisking appears to be driven by central pattern generators (CPGs) that operate independently of direct sensory feedback. Nevertheless, whisking can be modulated by sensory feedback, and it has been hypothesized that some of this modulation already occurs within the brainstem. However, the interaction between sensory feedback and CPG activity is poorly understood. Using the visual language of statecharts, a dynamic, bottom-up computerized model of the brainstem loop of the whisking system was built in order to investigate the interaction between sensory feedback and CPG activity during whisking behavior. As a benchmark, we used a previously quantified closed-loop phenomenon of the whisking system, touched-induced pump (TIP), which is thought to be mediated by the brainstem loop. First, we showed that TIPs depend on sensory feedback, by comparing TIP occurrence in intact rats with that in rats whose sensory nerve was experimentally cut. We then inspected several possible feedback mechanisms of TIPs using our model. The model ruled out all hypothesized mechanisms but one, which adequately simulated the corresponding motion observed in the rat. Results of the simulations suggest that TIPs are generated via sensory feedback that activates extrinsic retractor muscles in the mystacial pad. The model further predicted that in addition to the touching whisker, all whiskers found on the same side of the snout should exhibit a TIP. We present experimental results that confirm the predicted movements in behaving rats, establishing the validity of the hypothesized interaction between sensory feedback and CPG activity we suggest here for the generation of TIPs in the whisking system.     

Topography of rodent whisking--I. Two-dimensional monitoring of whisker movements

During 'active touch' the rodent whiskers scan the environment in a series of repetitive movements ('whisks') generating afferent signals which transform the spatial properties of objects into spatio-temporal patterns of neural activity. Based upon analyses carried out in a single movement plane, it has been generally assumed that these trajectories are essentially uni-dimensional, although more complex movements have been described in some rodents. The present study was designed to examine this assumption and to more precisely characterize whisking topography by monitoring whisking trajectories along both the antero-posterior and dorso-ventral axes. Using optoelectronic monitoring techniques with high-spatio-temporal resolution, movement data were obtained from a population of vibrissae sampled at different locations on the mystacial pad in head-fixed rats isolated from the perturbing effects of contact. For a substantial proportion of the population of whisking movements sampled, the trajectories generated by a single whisker is most accurately described as occupying an expended two-dimensional space in which the A-P component predominates. However, the whisker system exhibits a considerable range of trajectory types, suggesting a high degree of movement flexibility. For each vibrissa position, it was possible to delineate a 'trajectory' domain-that portion of the animal's whisking space which is scanned by the movements of that vibrissa during whisking. Since the 'domains' of adjacent whiskers in the same row tend to overlap, synchronized movements of a subset of whiskers could generate a set of overlapping somatosensory fields analogous to overlapping retinal receptive fields. The organization of such trajectory domains within the rats' whisking space could provide the spatial component of the spatio-temporal integration process required to extract information about environmental features from the inputs generated by its recursive whisking movements.     

Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact

Rats sweep their facial whiskers back and forth to generate tactile sensory information through contact with environmental structure. The neural processes operating on the signals arising from these whisker contacts are widely studied as a model of sensing in general, even though detailed knowledge of the natural circumstances under which such signals are generated is lacking. We used digital video tracking and wireless recording of mystacial electromyogram signals to assess the effects of whisker-object contact on whisking in freely moving animals exploring simple environments. Our results show that contact leads to reduced protraction (forward whisker motion) on the side of the animal ipsilateral to an obstruction and increased protraction on the contralateral side. Reduced ipsilateral protraction occurs rapidly and in the same whisk cycle as the initial contact. We conclude that whisker movements are actively controlled so as to increase the likelihood of environmental contacts while constraining such interactions to involve a gentle touch. That whisking pattern generation is under strong feedback control has important implications for understanding the nature of the signals reaching upstream neural processes.