Rat Vibrissa Research Articles

Mechanical resonance enhances the sensitivity of the vibrissa sensory system to near-threshold stimuli

The representation of high-frequency sensory information is a crucial problem faced by the nervous system. Rodent facial vibrissae constitute a high-resolution sensory system, capable of discriminating and detecting subtle changes in tactual input. During active sensing, the mechanical properties of vibrissae may play a key role in filtering sensory information and translating it into neural activity. Previous studies have shown that rat vibrissae resonate, conferring frequency specificity to trigeminal ganglion (NV) and primary somatosensory cortex (SI) neurons during suprathreshold sensory stimulation. In addition to frequency specificity, a further potential impact of vibrissa resonance is enhancement of sensitivity to near-threshold stimuli through signal amplification. To examine the effect of resonance on peri-threshold inputs (≤ 80 μm at the vibrissa tip), we recorded NV and SI neurons during stimulation at multiple amplitudes and frequencies, and generated minimal amplitude tuning curves. Several novel findings emerged from this study. First, vibrissa resonance significantly lowered the threshold for evoked neural activity, in many cases by an order of magnitude compared to stimuli presented at off-resonance frequencies. When stimulated at the fundamental resonance frequency, motions as small as 8 μm at the vibrissa tip, corresponding to angular deflections of less than 0.2°, drove neural firing in the periphery and cortex. Second, a closer match between vibrissal and neural frequency tuning was found for lower amplitude motions. Third, simultaneous paired recordings demonstrated that the minimal amplitude of resonant vibrissa stimulation required to evoke responses in SI increased significantly for recordings outside the primary vibrissa barrel column, providing additional evidence for somatotopically localized frequency columns. These data demonstrate that resonant amplification can increase the sensitivity of the vibrissa sensory system to an ecologically relevant range of low-amplitude, high-frequency stimuli.

Id2, Id3, and Id4 proteins show dynamic changes in expression during vibrissae follicle development

Id proteins are involved in the transcriptional control of many fundamental biological processes, including differentiation and lineage commitment. We studied Id2, Id3, and Id4 protein expression during different stages of rat vibrissa follicle development using immunohistochemistry. Id2 was highly expressed in the cytoplasm of specialized cells in the basal epidermis and outer root sheath during early stages of follicle development. These cells were identified as Merkel cells (MCs) by means of double-immunolabeling with synaptophysin and cytokeratin-20, and persisted in neonatal follicles. Id3 immunofluorescence was characterized by membrane-associated expression in basal epithelial cells of follicles early in development. Subsequently follicle epithelial cells switched to have strong nuclear labeling, also a feature of newly forming dermal papilla cells. Id4 expression was primarily associated with innervation of the developing follicle musculature. These observations illustrate dynamic expression patterns of Id2 and Id3 proteins in developing follicles and specifically link Id2 expression to Merkel cell specification.

The frequency response of rat vibrissae to sound

The motion of isolated rat vibrissae due to low frequency sound has been modeled and measured with good agreement (within a factor of 2) between the data and the model's predictions. As had been done in previous studies on the response of rat vibrissae to tactile stimulation [Hartmann, M. J., Johnson, N. J., Towal, R. B., and Assad, C., J. Neurosci 23, 6510-6519 (2003) and Neimark, M. A., Andermann, A. L., Hopfield, J. J., and Moore, C. I., J. Neurosci 23, 6449-6509 (2003)] the vibrissae were modeled as thin conical beams. The force of the vibrating air on a vibrissa was modeled using the exact solution for a vibrating infinite cylinder in linear fluid. A finite element method was used to model the motion of a single vibrissa fixed at its base, using the aforementioned fluid force. Values for Young's modulus and vibrissa mass density were taken from a previous study [Neimark et al. (above)]. The model had no freely fitted parameters. Motion of isolated vibrissae was measured using a video camera with microscope. The sound stimulation was created using a stereo speaker connected to a signal generator. The tuning was found to be sharp, with quality factors that varied between 3 and 7, much sharper than the motion of cricket cercal hairs or in vitro inner ear hair bundles.

Biomechanics of the Vibrissa Motor Plant in Rat: Rhythmic Whisking Consists of Triphasic Neuromuscular Activity

The biomechanics of a motor plant constrain the behavioral strategies that an animal has available to extract information from its environment. We used the rat vibrissa system as a model for active sensing and determined the pattern of muscle activity that drives rhythmic exploratory whisking. Our approach made use of electromyography to measure the activation of all relevant muscles in both head-fixed and unrestrained rats and two-dimensional imaging to monitor the position of the vibrissae in head-fixed rats. Our essential finding is that the periodic motion of the vibrissae and mystacial pad during whisking results from three phases of muscle activity. First, the vibrissae are thrust forward as the rostral extrinsic muscle, musculus (m.) nasalis, contracts to pull the pad and initiate protraction. Second, late in protraction, the intrinsic muscles pivot the vibrissae farther forward. Third, retraction involves the cessation of m. nasalis and intrinsic muscle activity and the contraction of the caudal extrinsic muscles m. nasolabialis and m. maxillolabialis to pull the pad and the vibrissae backward. We developed a biomechanical model of the whisking motor plant that incorporates the measured muscular mechanics along with movement vectors observed from direct muscle stimulation in anesthetized rats. The results of simulations of the model quantify how the combination of extrinsic and intrinsic muscle activity leads to an enhanced range of vibrissa motion than would be available from the intrinsic muscles alone.

Hypoglossal nuclei participation in rat mystacial pad control

Recently, we showed that extra-trigeminal axons, originating from the hypoglossal nucleus, travel with the infraorbital division of the trigeminal nerve (ION), which is known to innervate the rat mystacial pad. Dil was monolaterally injected into the rat XII nucleus to analyse the peripheral distribution of hypoglossal axons to the mystacial pad, to evaluate their involvement in facial sensory-motor control. Electromyographic responses of mystacial pad motor units to electrical stimulation of the ION were recorded, along with the evoked responses to electrical stimulation of the ipsilateral XII nucleus. The results showed that hypoglossal axon terminals target the ipsilateral extrinsic musculature of the mystacial pad, but they do not have any contact with the intrinsic muscles. ION electrical stimulation increased electromyographic activity in the ipsilateral pad extrinsic muscles, even following VII nerve transection. Hypoglossal nucleus electrical stimulation induced field potentials and monosynaptic responses in the same motor units that persisted even following VII nerve transection, these disappearing after cooling the ION. We suggest that the small hypoglossal neurons projecting to the extrinsic musculature of the mystacial pad are part of a hypoglossal-trigeminal loop that participates in the sensory-motor control of the rat vibrissae system.

Embodied Information Processing: Vibrissa Mechanics and Texture Features Shape Micromotions in Actively Sensing Rats

Peripheral sensory organs provide the first transformation of sensory information, and understanding how their physical embodiment shapes transduction is central to understanding perception. We report the characterization of surface transduction during active sensing in the rodent vibrissa sensory system, a widely used model. Employing high-speed videography, we tracked vibrissae while rats sampled rough and smooth textures. Variation in vibrissa length predicted motion mean frequencies, including for the highest velocity events, indicating that biomechanics, such as vibrissa resonance, shape signals most likely to drive neural activity. Rough surface contact generated large amplitude, high-velocity "stick-slip-ring" events, while smooth surfaces generated smaller and more regular stick-slip oscillations. Both surfaces produced velocities exceeding those applied in reduced preparations, indicating active sensation of surfaces generates more robust drive than previously predicted. These findings demonstrate a key role for embodiment in vibrissal sensing and the importance of input transformations in sensory representation.

Thalamocortical transformations of periodic stimuli: the effect of stimulus velocity and synaptic short-term depression in the vibrissa–barrel system

Recent works on the response of barrel neurons to periodic deflections of the rat vibrissae have shown that the stimulus velocity is encoded in the corti cal spike rate (Pinto et al., Journal of Neurophysiology, 83(3), 1158-1166, 2000; Arabzadeh et al., Journal of Neuroscience, 23(27), 9146-9154, 2003). Other studies have reported that repetitive pulse stimulation produces band-pass filtering of the barrel response rate centered around 7-10 Hz (Garabedian et al., Journal of Neurophysiology, 90, 1379-1391, 2003) whereas sinusoidal stimulation gives an increasing rate up to 350 Hz (Arabzadeh et al., Journal of Neuroscience, 23(27), 9146-9154, 2003). To explore the mechanisms underlying these results we propose a simple computational model consisting in an ensemble of cells in the ventro-posterior medial thalamic nucleus (VPm) encoding the stimulus velocity in the temporal profile of their response, connected to a single barrel cell through synapses showing short-term depression. With sinusoidal stimulation, encoding the velocity in VPm facilitates the response as the stimulus frequency increases and it causes the velocity to be encoded in the cortical rate in the frequency range 20-100 Hz. Synaptic depression does not suppress the response with sinusoidal stimulation but it produces a band-pass behavior using repetitive pulses. We also found that the passive properties of the cell membrane eventually suppress the response to sinusoidal stimulation at high frequencies, something not observed experimentally. We argue that network effects not included here must be important in sustaining the response at those frequencies.

Electrophysiological study in the infraorbital nerve of the rat: Spontaneous and evoked activity

In this work we present some studies in the afferent nerve of the rat vibrissae. Studies on spontaneous activity (SA) in this sensorial system are of long data. Nevertheless, SA recordings in the nerve of a single vibrissa have not been made until present. In this work, we use an algorithm based on signal decomposition with Continuous Wavelet Transform (CWT) to analyse the discharges of two nerves. The action potentials of both nerves were detected and the firing rates were calculated. These results suggest that the firing rate of one vibrissa innervation is low considering that this nerve contains hundred of fibers. In addition, we present preliminary studies suggesting important effects of the hair shaft length in the afferent discharge during the vibrissae movements. The experiments consisted in recording the nerve activity after the vibrissae were sectioned at two different levels. The results showed important differences in the signal energy contents. It suggests that the hair shaft length would produce a differential activation of the mechanoreceptors located in the vibrissae follicle.

Long-term effects of prenatal alcohol exposure on the size of the whisker representation in juvenile and adult rat barrel cortex

Children of mothers who abused alcohol during pregnancy are often reported to suffer from growth retardation and central nervous system (CNS) abnormalities. The use of prenatal alcohol exposed (PAE) animal models has revealed reductions in body and brain weights as well as regional specific brain deficits in neonatal pups. Recently, we and others reported reductions in the size of the posteromedial barrel subfield (PMBSF) in first somatosensory cortex (SI) associated with the representation of the large mystacial vibrissae in neonatal rats and mice that were exposed to alcohol at various times during gestation. While these reductions in barrel field size were reported in neonates, it was unclear whether similar reductions persisted later in life or whether some catch-up might take place in older animals. In the present study, we examined the effect of PAE on measures of barrel field size in juvenile (6 weeks of age) and adult (7 months of age) rats; body and brain weights were also measured. Pregnant rats (Sprague-Dawley) were intragastrically gavaged during gestational days 1–20 with alcohol (6 g/kg) to simulate a binge-like pattern of alcohol consumption (Alc); 6 g/kg alcohol produced blood alcohol levels ranging between 207.4 and 478.6 mg/dl. Chow-fed (CF), pair-fed (PF), and cross-foster (XF) groups served as normal, nutritional/stress, and maternal controls, respectively, for juvenile rats; an XF group was not included for adult rats. The major findings in the present study are (i) PAE significantly reduced the size of the total barrel field in Alc juvenile rats (13%) and adult rats (9%) compared to CF controls, (ii) PAE significantly reduced the total averaged sizes of individual PMBSF barrels in juvenile (14%) and adult (13%) rats, (iii) PAE did not significantly alter the septal area between barrels or the barrel pattern, (iv) PAE significantly reduced body weight of juvenile rats but only in comparison to PF controls (18%), (v) PAE significantly reduced whole brain (8%) and forebrain (7%) weights of juvenile rats but not adult rats, (vi) no differences were observed in forebrain/PMBSF body ratios nor was forebrain weight correlated with PMBSF area, and (vii) PAE resulted in a greater reduction in anterior barrels compared to posterior barrels. These results suggest that the effects of PAE previously reported in neonate PMBSF areas persist into adulthood.

Flexible Probes for Characterizing Surface Topology: From Biology to Technology

In nature, several species use flexible probes to actively explore their environment and acquire important sensory information, such as surface topology, texture, and water or air flow velocity. For example, rats and other rodents have an array of facial vibrissae (or whiskers) with which they gather tactile information about the external world. The complex mechanisms by which mechanical deformations of the probe lead to neuronal activity in the animal's nervous system are still far from being completely understood. This is due to the intricacy of the deformation mechanics of the flexible sensors, the processes responsible for transforming the deformation to electrical activity, and the subsequent representation of the sensory information by the nervous system. Understanding how these mechano- sensory signals are transduced and extracted by the nervous system promises great insight into biological function, and has novel technological applications. To understand the mechanical aspect of sensory transduction, here we moni- tored the deformation of a rat's vibrissa as it strikes rigid objects with different topologies (surface features) during locomotion, using high-speed videography. Motivated by our observations, we developed detailed numerical models to study the mechanics of such flexible probes. Our findings elucidate how active sensation with vibrissae might provide sensory information and in addition have direct implications for several technological areas. To put this in perspective, we propose strategies in which flexible probes can be used to characterize surface topology at high speeds, which is a desirable feature in several technological applications such as memory retrieval.

Superior sensation: superior colliculus participation in rat vibrissa system

BackgroundThe superior colliculus, usually considered a visuomotor structure, is anatomically positioned to perform sensorimotor transformations in other modalities. While there is evidence for its potential participation in sensorimotor loops of the rodent vibrissa system, little is known about its functional role in vibrissa sensation or movement. In anesthetized rats, we characterized extracellularly recorded responses of collicular neurons to different types of vibrissa stimuli.ResultsCollicular neurons had large receptive fields (median = 14.5 vibrissae). Single units displayed responses with short latencies (5.6 ± 0.2 msec, median = 5.5) and relatively large magnitudes (1.2 ± 0.1 spikes/stimulus, median = 1.2). Individual neurons could entrain to repetitive vibrissa stimuli delivered at ≤ 20 Hz, with little reduction in phase locking, even when response magnitude was decreased. Neurons responded preferentially to vibrissa deflections at particular angles, with 43% of the cells having high (≥ 5) angular selectivity indices.ConclusionResults are consistent with a proposed role of the colliculus in somatosensory-mediated orienting. These properties, together with the connections of the superior colliculus in sensorimotor loops, are consistent with its involvement in orienting, alerting and attentive functions related to the vibrissa system.

Active Spatial Perception in the Vibrissa Scanning Sensorimotor System

Haptic perception is an active process that provides an awareness of objects that are encountered as an organism scans its environment. In contrast to the sensation of touch produced by contact with an object, the perception of object location arises from the interpretation of tactile signals in the context of the changing configuration of the body. A discrete sensory representation and a low number of degrees of freedom in the motor plant make the ethologically prominent rat vibrissa system an ideal model for the study of the neuronal computations that underlie this perception. We found that rats with only a single vibrissa can combine touch and movement to distinguish the location of objects that vary in angle along the sweep of vibrissa motion. The patterns of this motion and of the corresponding behavioral responses show that rats can scan potential locations and decide which location contains a stimulus within 150 ms. This interval is consistent with just one to two whisk cycles and provides constraints on the underlying perceptual computation. Our data argue against strategies that do not require the integration of sensory and motor modalities. The ability to judge angular position with a single vibrissa thus connects previously described, motion-sensitive neurophysiological signals to perception in the behaving animal.

The Whisking Rhythm Generator: A Novel Mammalian Network for the Generation of Movement

Using the rat vibrissa system, we provide evidence for a novel mechanism for the generation of movement. Like other central pattern generators (CPGs) that underlie many movements, the rhythm generator for whisking can operate without cortical inputs or sensory feedback. However, unlike conventional mammalian CPGs, vibrissa motoneurons (vMNs) actively participate in the rhythmogenesis by converting tonic serotonergic inputs into the patterned motor output responsible for movement of the vibrissae. We find that, in vitro, a serotonin receptor agonist, alpha-Me-5HT, facilitates a persistent inward current (PIC) and evokes rhythmic firing in vMNs. Within each motoneuron, increasing the concentration of alpha-Me-5HT significantly increases the both the magnitude of the PIC and the motoneuron's firing rate. Riluzole, which selectively suppresses the Na(+) component of PICs at low concentrations, causes a reduction in both of these phenomena. The magnitude of this reduction is directly correlated with the concentration of riluzole. The joint effects of riluzole on PIC magnitude and firing rate in vMNs suggest that the two are causally related. In vivo we find that the tonic activity of putative serotonergic premotoneurons is positively correlated with the frequency of whisking evoked by cortical stimulation. Taken together, these results support the hypothesized novel mammalian mechanism for movement generation in the vibrissa motor system where vMNs actively participate in the rhythmogenesis in response to tonic drive from serotonergic premotoneurons.

What Generates Whisking? Focus on: “The Whisking Rhythm Generator: A Novel Mammalian Network for the Generation of Movement”

A central goal of neuroscience is to explain how neural networks generate organized and repetitive motor patterns, such as active whisking used by rodents to navigate the environment. Whisking consists of fast rhythmic ellipsoid vibrissae movements through the air and over objects at between 4 and

Stimulus Dependence of Barrel Cortex Directional Selectivity

Neurons throughout the rat vibrissa somatosensory pathway are sensitive to the angular direction of whisker movement. Could this sensitivity help rats discriminate stimuli? Here we use a simple computational model of cortical neurons to analyze the robustness of directional selectivity. In the model, directional preference emerges from tuning of synaptic conductance amplitude and latency, as in recent experimental findings. We find that directional selectivity during stimulation with random deflection sequences is strongly dependent on the mean deflection frequency: Selectivity is weakened at high frequencies even when each individual deflection evokes strong directional tuning. This variability of directional selectivity is due to generic properties of synaptic integration by the neuronal membrane, and is therefore likely to hold under very general physiological conditions. Our results suggest that directional selectivity depends on stimulus context. It may participate in tasks involving brief whisker contact, such as detection of object position, but is likely to be weakened in tasks involving sustained whisker exploration (e.g., texture discrimination).

A novel stimulus system for applying tactile stimuli to the macrovibrissae in electrophysiological experiments

The rat's vibrissae are a wonderful system for the study of sensory neural encoding in relation to behaviour because the vibrissae are easily identifiable and accessible for manipulation, allowing easy application of a variety of different types of deflections that mimic natural whisking. Here we report the development of a powerful and flexible method for precisely deflecting these vibrissae. Recordings from CNS neurons showed, in response to variations in the parameters of a trapezoid whisker deflection stimulus that mimics the basic unit of whisking, a variety of complex responses as well as complex interactions between different response components. The recordings also included a response that is reported to be found during active whisking (movement under muscle control) and not passive whisker movements and thus to differentiate active from passive whisker deflections. Thus, this system could well be used in anaesthetized animals to apply whisker deflections that well mimic natural active whisking in awake animals, thereby allowing highly detailed study of the neuronal responses and neuronal interactions found with natural whisking behaviour.

Mapping the Gates. Focus on “Relationship Between Physiological Response Type (RA and SA) and Vibrissal Receptive Field of Neurons Within the Rat Trigeminal Ganglion”

Four decades ago, Hubel and Wiesel demonstrated that cortical neurons show a response specificity that does not exist in the thalamus or retina and triggered a universal pursuit after cortical mechanisms of perception. Under this pursuit hid an implicit assumption that whatever is needed to be known

The Dynamics of Spatiotemporal Response Integration in the Somatosensory Cortex of the Vibrissa System

Spatiotemporal response integration across the neural receptive field (RF) is a general feature of sensory coding and has an important role in shaping responses to naturalistic stimuli. In the primary somatosensory cortex of the rat vibrissa pathway, such integration across the vibrissa array strongly shapes the coding of spatiotemporally distributed deflections. Using a spatiotemporal paired-pulse paradigm, this study revealed that fundamentally different types of pairwise interactions have similar qualitative behavior but that the magnitude, latency, and precision of the neural responses depend on the specific RF components being engaged. In all cases, however, increase in the suppression of response magnitude accompanied a lengthening of latency and a decrease in response precision. Furthermore, nonlinear interactions evoked by stimulation of multiple RF subregions strongly influence both response magnitude and timing to more complex sequences. Despite their complexity, such response interactions are highly predictable from elementary pairwise interactions. To understand the functional role of spatiotemporal interactions in coding, we developed a response model that incorporated the experimentally measured modulations in response magnitude, latency, and precision induced by cross-vibrissa interactions. Simulations of a simplified textural discrimination task indicate that spatiotemporal interactions enhance discrimination under certain stimulus time scales. This improvement follows from a nonlinear response property that acts to restore the neural response in the face of suppression. Together, the present findings highlight the role of response integration in shaping single-cell responses and provide predictions about how changes in response parameters influence coding accuracy.

Transient and Steady-State Dynamics of Cortical Adaptation

Adaptation is a ubiquitous property of all sensory pathways of the brain and thus likely critical in the encoding of behaviorally relevant sensory information. Despite evidence identifying specific biophysical mechanisms contributing to sensory adaptation, its functional role in sensory encoding is not well understood, particularly in the natural environment where transient rather than steady-state activity could dominate the neuronal representation. Here, we show that the heterogeneous transient and steady-state adaptation dynamics of single cortical neurons in the rat vibrissa system were well characterized by an underlying state variable. The state was directly predictable from temporal response properties that capture the time course of postexcitatory suppression following an isolated vibrissa deflection. Altering the initial state, by preceding the periodic stimulus with an additional vibrissa deflection, strongly influenced single-cell transient cortical adaptation responses. Despite the different transient activity, neurons reached the same steady-state adapted response with a time to steady state that was independent of the initial state. However, the differences in transient activity observed on small time scales were not present when activity was integrated over the longer time scale of a stimulus cycle. Taken together, the results here demonstrate that although adaptation can have significant effects on transient neuronal activity and direction selectivity, a simple measure of the time course of suppression following an isolated stimulus predicted a large portion of the observed adaptation dynamics.

Metabotropic glutamate receptor antagonists selectively enhance responses of slowly adapting type I mechanoreceptors

There is evidence that glutamate may participate as a transmitter at the junction between Merkel cells and the nerve terminals of slowly adapting type I (St I) units. We recorded extracellularly from the deep vibrissal nerve of an isolated rat vibrissa preparation in vitro. Five second trapezoid stimulus ramp deflections of the hair shaft were used to evoke responses. We bath-applied two compounds, which we planned would interfere with glutamatergic transmission. (2S)-2-Amino-2-[(1S,2S)-2-carboxycycloprop-1-yl]-3-(xanth-9-yl) propanoic acid (LY341495) was used at concentrations up to 100 microM to block all known metabotropic glutamate (mGlu) receptors. The racemic mixture (RS)-4-carboxy-3-hydroxyphenylglycine ((RS)-4C3HPG) was used up to 100 microM to block ionotropic and Group I metabotropic glutamate receptors, and as an agonist at Group II mGlu receptors. Unexpectedly, both compounds had rapid onset excitatory effects on mechanically-evoked responses. (RS)-4C3HPG increased responses, with a mean 146% of control (P < 0.05) in a concentration-dependent manner. LY341495 increased responses, with a mean 128% of control (P < 0.05). With (RS)-4C3HPG in particular, it was noted that the static component (the firing during the last 1 s plateau) was preferentially enhanced relative to the dynamic component (firing during the first 0.5 s). Rapid recovery was seen after wash. Slowly adapting type II units, which have no junctional transmission, were completely unaffected by these compounds up to 200 microM. These results suggest that mGlu receptors play a role in Merkel cell-neurite complex mechanotransduction, although other explanations are considered.