Vibrissa Self-Motion and Touch Are Reliably Encoded along the Same Somatosensory Pathway from Brainstem through Thalamus

Active sensing involves the fusion of internally generated motor events with external sensation. For rodents, active somatosensation includes scanning the immediate environment with the mystacial vibrissae. In doing so, the vibrissae may touch an object at any angle in the whisk cycle. The representation of touch and vibrissa self-motion may in principle be encoded along separate pathways, or share a single pathway, from the periphery to cortex. Past studies established that the spike rates in neurons along the lemniscal pathway from receptors to cortex, which includes the principal trigeminal and ventral-posterior-medial thalamic nuclei, are substantially modulated by touch. In contrast, spike rates along the paralemniscal pathway, which includes the rostral spinal trigeminal interpolaris, posteromedial thalamic, and ventral zona incerta nuclei, are only weakly modulated by touch. Here we find that neurons along the lemniscal pathway robustly encode rhythmic whisking on a cycle-by-cycle basis, while encoding along the paralemniscal pathway is relatively poor. Thus, the representations of both touch and self-motion share one pathway. In fact, some individual neurons carry both signals, so that upstream neurons with a supralinear gain function could, in principle, demodulate these signals to recover the known decoding of touch as a function of vibrissa position in the whisk cycle.     

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 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.     

In vivo imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation

In the nematode C. elegans, genes encoding components of a putative mechanotransducing channel complex have been identified in screens for light-touch-insensitive mutants. A long-standing question, however, is whether identified MEC proteins act directly in touch transduction or contribute indirectly by maintaining basic mechanoreceptor neuron physiology. In this study, we used the genetically encoded calcium indicator cameleon to record cellular responses of mechanosensory neurons to touch stimuli in intact, behaving nematodes. We defined a gentle touch sensory modality that adapts with a time course of approximately 500 ms and primarily senses motion rather than pressure. The DEG/ENaC channel subunit MEC-4 and channel-associated stomatin MEC-2 are specifically required for neural responses to gentle mechanical stimulation, but do not affect the basic physiology of touch neurons or their in vivo responses to harsh mechanical stimulation. These results distinguish a specific role for the MEC channel proteins in the process of gentle touch mechanosensation.     

Positive feedback in a brainstem tactile sensorimotor loop

The trigeminal loop in the brainstem comprises the innermost level of sensorimotor feedback in the rat vibrissa system. Anatomy suggests that this loop relays tactile information from the vibrissae to the motoneurons that control vibrissa movement. We demonstrate, using in vitro and in vivo recordings, that the trigeminal loop consists of excitatory pathways from vibrissa sensory inputs to vibrissa motoneurons in the facial nucleus. We further show that the trigeminal loop implements a rapidly depressing reflex that provides positive sensory feedback to the vibrissa musculature during simulated whisking and contact. On the basis of these findings, we propose that the trigeminal loop provides an enhancement of vibrissa muscle tone upon contact during active touch.     

Fast Feedback in Active Sensing: Touch-Induced Changes to Whisker-Object Interaction

Whisking mediated touch is an active sense whereby whisker movements are modulated by sensory input and behavioral context. Here we studied the effects of touching an object on whisking in head-fixed rats. Simultaneous movements of whiskers C1, C2, and D1 were tracked bilaterally and their movements compared. During free-air whisking, whisker protractions were typically characterized by a single acceleration-deceleration event, whisking amplitude and velocity were correlated, and whisk duration correlated with neither amplitude nor velocity. Upon contact with an object, a second acceleration-deceleration event occurred in about 25% of whisk cycles, involving both contacting (C2) and non-contacting (C1, D1) whiskers ipsilateral to the object. In these cases, the rostral whisker (C2) remained in contact with the object throughout the double-peak phase, which effectively prolonged the duration of C2 contact. These “touch-induced pumps” (TIPs) were detected, on average, 17.9 ms after contact. On a slower time scale, starting at the cycle following first touch, contralateral amplitude increased while ipsilateral amplitude decreased. Our results demonstrate that sensory-induced motor modulations occur at various timescales, and directly affect object palpation.     

Primary motor cortex reports efferent control of vibrissa motion on multiple timescales

Exploratory whisking in rat is an example of self-generated movement on multiple timescales, from slow variations in the envelope of whisking to the rapid sequence of muscle contractions during?a single whisk cycle. We find that, as a population, spike trains of single units in primary vibrissa motor cortex report the absolute angle of vibrissa position. This representation persists after sensory nerve transection, indicating an efferent source. About two-thirds of the units are modulated by slow variations in the envelope of whisking, while relatively few units report rapid changes in position within the whisk cycle. The combined results from this study and past measurements, which show that primary sensory cortex codes the whisking envelope as?a motor copy signal, imply that signals present in both sensory and motor cortices are necessary to compute angular coordinates based on vibrissa touch.     

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.     

Synaptic mechanisms underlying sparse coding of active touch

Sensory information is actively gathered by animals, but the synaptic mechanisms driving neuronal circuit function during active sensory processing are poorly understood. Here, we investigated the synaptically driven membrane potential dynamics during active whisker sensation using whole-cell recordings from layer 2/3 pyramidal neurons in the primary somatosensory barrel cortex of behaving mice. Although whisker contact with an object evoked rapid depolarization in all neurons, these touch responses only drove action potentials in ～10% of the cells. Such sparse coding was ensured by cell-specific reversal potentials of the touch-evoked response that were hyperpolarized relative to action potential threshold for most neurons. Intercontact interval profoundly influenced touch-evoked postsynaptic potentials, interestingly without affecting the peak membrane potential of the touch response. Dual whole-cell recordings indicated highly correlated membrane potential dynamics during active touch. Sparse action potential firing within synchronized cortical layer 2/3 microcircuits therefore appears to robustly signal each active touch response.     

Serotonin and whisking

Rhythmic whisker movements, called "whisking," are produced by a brainstem central pattern generator (CPG) that uses serotonin to induce periodic firing in facial motorneurons. During active touch, motor cortex could regulate whisking frequency by controlling the rate of firing of the serotonergic neurons.     

Object localization with whiskers

Rats use their large facial hairs (whiskers) to detect, localize and identify objects in their proximal three-dimensional (3D) space. Here, we focus on recent evidence of how object location is encoded in the neural sensory pathways of the rat whisker system. Behavioral and neuronal observations have recently converged to the point where object location in 3D appears to be encoded by an efficient orthogonal scheme supported by primary sensory-afferents: each primary-afferent can signal object location by a spatial (labeled-line) code for the vertical axis (along whisker arcs), a temporal code for the horizontal axis (along whisker rows), and an intensity code for the radial axis (from the face out). Neuronal evidence shows that (i) the identities of activated sensory neurons convey information about the vertical coordinate of an object, (ii) the timing of their firing, in relation to other reference signals, conveys information about the horizontal object coordinate, and (iii) the intensity of firing conveys information about the radial object coordinate. Such a triple-coding scheme allows for efficient multiplexing of 3D object location information in the activity of single neurons. Also, this scheme provides redundancy since the same information may be represented in the activity of many neurons. These features of orthogonal coding increase accuracy and reliability. We propose that the multiplexed information is conveyed in parallel to different readout circuits, each decoding a specific spatial variable. Such decoding reduces ambiguity, and simplifies the required decoding algorithms, since different readout circuits can be optimized for a particular variable.     

Reversible blockade of rodent whisking: Botulinum toxin as a tool for developmental studies

Studies of sensorimotor systems such as the whisking system of rodents have suggested that associations between body movements and their sensory consequences during development may make an important contribution to the functional organization of the system. In the present study we have explored the possible utility of Botulinum toxin for developmental studies of whisking. Botox selectively blocks whisking-generated afference leaving other sources of whisker afference intact. We describe appropriate modes of injection, define dosage levels, and assess the effects of prolonged whisking paralysis during development upon the basic motor competency of the adult rat. Our findings indicate that: (a) Botulinum toxin may be used to block whisking behavior in adult and developing rats, (b) that the duration of the whisking paralysis produced by Botox treatment blockade is dose dependent in both developing and adult animals, (c) that the blockade is functionally reversible and (d) that Botox treatment during development does not impair either the kinematics or the rhythmic patterning of adult whisking behavior. Botox may be a useful tool for studying the role of experiential factors in the development of "active touch" in rodents.     

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.     

Biomimetic vibrissal sensing for robots

Active vibrissal touch can be used to replace or to supplement sensory systems such as computer vision and, therefore, improve the sensory capacity of mobile robots. This paper describes how arrays of whisker-like touch sensors have been incorporated onto mobile robot platforms taking inspiration from biology for their morphology and control. There were two motivations for this work: first, to build a physical platform on which to model, and therefore test, recent neuroethological hypotheses about vibrissal touch; second, to exploit the control strategies and morphology observed in the biological analogue to maximize the quality and quantity of tactile sensory information derived from the artificial whisker array. We describe the design of a new whiskered robot, Shrewbot, endowed with a biomimetic array of individually controlled whiskers and a neuroethologically inspired whisking pattern generation mechanism. We then present results showing how the morphology of the whisker array shapes the sensory surface surrounding the robot's head, and demonstrate the impact of active touch control on the sensory information that can be acquired by the robot. We show that adopting bio-inspired, low latency motor control of the rhythmic motion of the whiskers in response to contact-induced stimuli usefully constrains the sensory range, while also maximizing the number of whisker contacts. The robot experiments also demonstrate that the sensory consequences of active touch control can be usefully investigated in biomimetic robots.     

Reversible blockade of rodent whisking: Botulinum toxin as a tool for developmental studies

Studies of sensorimotor systems such as the whisking system of rodents have suggested that associations between body movements and their sensory consequences during development may make an important contribution to the functional organization of the system. In the present study we have explored the possible utility of Botulinum toxin for developmental studies of whisking. Botox selectively blocks whisking-generated afference leaving other sources of whisker afference intact. We describe appropriate modes of injection, define dosage levels, and assess the effects of prolonged whisking paralysis during development upon the basic motor competency of the adult rat. Our findings indicate that: (a) Botulinum toxin may be used to block whisking behavior in adult and developing rats, (b) that the duration of the whisking paralysis produced by Botox treatment blockade is dose dependent in both developing and adult animals, (c) that the blockade is functionally reversible and (d) that Botox treatment during development does not impair either the kinematics or the rhythmic patterning of adult whisking behavior. Botox may be a useful tool for studying the role of experiential factors in the development of "active touch" in rodents.     

Upregulation of barrel GABAergic neurons is associated with cross-modal plasticity in olfactory deficit

Background

Loss of a sensory function is often followed by the hypersensitivity of other modalities in mammals, which secures them well-awareness to environmental changes. Cellular and molecular mechanisms underlying cross-modal sensory plasticity remain to be documented.

Methodology/Principal Findings

Multidisciplinary approaches, such as electrophysiology, behavioral task and immunohistochemistry, were used to examine the involvement of specific types of neurons in cross-modal plasticity. We have established a mouse model that olfactory deficit leads to a whisking upregulation, and studied how GABAergic neurons are involved in this cross-modal plasticity. In the meantime of inducing whisker tactile hypersensitivity, the olfactory injury recruits more GABAergic neurons and their fine processes in the barrel cortex, as well as upregulates their capacity of encoding action potentials. The hyperpolarization driven by inhibitory inputs strengthens the encoding ability of their target cells.

Conclusion/Significance

The upregulation of GABAergic neurons and the functional enhancement of neuronal networks may play an important role in cross-modal sensory plasticity. This finding provides the clues for developing therapeutic approaches to help sensory recovery and substitution.     

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.     

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.