Comparison of neuronal response pattern in the rat somatosensory cortex during active and passive vibrissae movements

A comparative study of neuronal response in separate cortical columns of the somatosensory cortex (the barrel field area) was made in unanesthetized partially curarized white rats under various circumstances: during passive deflection of immobile vibrissa, unhindered volitional sweeping movement of the vibrissae, and during movement induced by stimulating the motor cortex and facial muscles. Differences in the response of the same neurons emerged under these different experimental situations. Different groups of neurons — responding before, during, and after volitional vibrissa movements were observed. Such response is thought to be triggered by different afferent trains reaching cortical column neurons from sources including the motor cortex, the vibrissa follicle receptors, and facial muscles.Institute of Neurocybernetics, State University, Rostov-on-Don. State University, Simferopol. Translated from Neirofiziologiya, Vol. 22, No. 2, pp. 235–242, March–April, 1990.     

Comparative histomorphology of intrinsic vibrissa musculature among primates: implications for the evolution of sensory ecology and “face touch”

Macrovibrissae are specialized tactile sensory hairs present in most mammalian orders, used in maxillary mechanoreception or “face touch.” Some mammals have highly organized vibrissae and are able to “whisk” them. Movement of vibrissae is influenced by intrinsic vibrissa musculature, striated muscle bands that attach directly to the vibrissa capsule. It is unclear if primates have organized vibrissae or intrinsic vibrissa musculature and it is uncertain if they can move their vibrissae. The present study used histomorphological techniques to compare vibrissae among 19 primates and seven non‐primate mammalian taxa. Upper lips of these mammals were sectioned and processed for histochemical analysis. While controlling for phylogenetic effects the following hypotheses were tested: 1) mammals with well‐organized vibrissae possess intrinsic vibrissa musculature and 2) intrinsic vibrissa musculature is best developed in nocturnal, arboreal taxa. Our qualitative analyses show that only arboreal, nocturnal prosimians possess intrinsic musculature. Not all taxa that possessed organized vibrissae had intrinsic vibrissa musculature. Phylogenetic comparative analyses revealed a 70% probability that stem mammals, primates, and haplorhines possessed intrinsic vibrissa musculature and well‐organized vibrissae. These two traits most likely coevolved according to a discrete phylogenetic analysis. These results indicate that nocturnal, arboreal primates have the potential to more actively use their vibrissae in spatial recognition and navigation tasks than diurnal, more terrestrial species, but there is a clear phylogenetic signal involved in the evolution of primate vibrissae and “face touch.” Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Local cortical interactions determine the form of cortical plasticity.

Competitive interactions between left and right eye inputs to visual cortex during development are usually explained by the thalamocortical axons competing more or less well for cortical territory during retraction into eye specific domains. Here we review the evidence for competitive and co-operative interactions between cortical columns in barrel cortex which are present several weeks after retraction of thalamocortical axons into barrels. Sensory responses in barrel cortex can be altered by a period of vibrissa deprivation. It was found that responses to previously deprived vibrissae (that had been allowed to regrow) were depressed more if neighboring vibrissae were spared than if all vibrissae were removed simultaneously. Depression of the deprived vibrissa response was greater the closer the cell lay to a spared barrel. It was also found that spared vibrissae responses were potentiated more if several neighboring vibrissae were left intact than if only a single vibrissae was spared. These results suggest a mechanism of cooperative potentiation, perhaps due to intracortical summation of excitation evoked by neighbouring vibrissa stimulation. Thalamic responses to vibrissa stimulation were unaffected by deprivation indicating a cortical origin. One of the consequences of deprivation was that the speed of transmission between barrels was increased for spared and decreased for deprived vibrissa. These results imply that inherent interactions between cortical columns give rise to a property of competition and co-operativity which amplify the effects of sensory deprivation.     

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.     

The effect of vibrissa deprivation pattern on the form of plasticity induced in rat barrel cortex

Plasticity was induced in the barrel cortex of adolescent rats by depriving every second vibrissa on the contralateral vibrissa pad.This produced a chessboard pattern of barrels in the cortex where each barrel receiving its principal input from a spared vibrissa was surrounded by barrels for which the principal vibrissa had been deprived and conversely, each barrel receiving its principal input from a deprived vibrissa was surrounded by barrels for which the principal vibrissa had been spared. After 7 days' deprivation, responses to the regrown vibrissae were depressed in layers II/III (49% of control levels) and IV (60%). Depression was far greater than that seen with "all vibrissa" deprivation, suggesting that activity in the spared vibrissae accentuated the depression of the deprived vibrissae. Depression was not due to subcortical changes as thalamic Ventral Posterior Medial (VPM) responses to deprived vibrissa were unchanged. The short latency responses in layer IV (5-7 ms) were unaffected by deprivation, but the number of cells responding at intermediate latencies (8-13 ms) was markedly reduced (to 66% of control). Potentiation of the spared vibrissa response was substantial in the near side of the neighbouring barrel (2.2-fold increase in layers II/III, 2.9-fold in layer IV) but had not spread to the far side after 7 days' deprivation. Sparing multiple vibrissae may increase the rate of potentiation since 7 days is insufficient time for potentiation in single vibrissa spared animals. Potentiation was not due to subcortical changes as thalamic VPm responses to the spared vibrissa were normal. However, in the spared barrel the response latency decreased by 1-2 ms. Only the cells responding at short latency exhibited potentiated responses (39% increase) suggesting that some thalamocortical plasticity is still possible at P28-35. These results show that chessboard pattern deprivation is capable of inducing substantial plasticity over a wide area of barrel cortex. All the major forms of plasticity seen with other vibrissa deprivation patterns were present, although no other single deprivation pattern studied so far causes the complete repertoire seen with chessboard deprivation.     

Variation in Young's modulus along the length of a rat vibrissa

Rats use specialized tactile hairs on their snout, called vibrissae (whiskers), to explore their surroundings. Vibrissae have no sensors along their length, but instead transmit mechanical information to receptors embedded in the follicle at the vibrissa base. The transmission of mechanical information along the vibrissa, and thus the tactile information ultimately received by the nervous system, depends critically on the mechanical properties of the vibrissa. In particular, transmission depends on the bending stiffness of the vibrissa, defined as the product of the area moment of inertia and Young's modulus. To date, Young's modulus of the rat vibrissa has not been measured in a uniaxial tensile test. We performed tensile tests on 22 vibrissae cut into two halves: a tip-segment and a base-segment. The average Young's modulus across all segments was 3.34±1.48GPa. The average modulus of a tip-segment was 3.96±1.60GPa, and the average modulus of a base-segment was 2.90±1.25GPa. Thus, on average, tip-segments had a higher Young's modulus than base-segments. High-resolution images of vibrissae were taken to seek structural correlates of this trend. The fraction of the cross-sectional area occupied by the vibrissa cuticle was found to increase along the vibrissa length, and may be responsible for the increase in Young's modulus near the tip.     

The role of the ECoG theta- and alpha-frequency oscillations in rat vibrissa active movements

Characteristics of rat ECoG organization before and after vibrissa active movements were studied by means ofmicroelectrode recording. It was shown that different brain structures were recruited to a variable extent in planning and initiation of vibrissae active movements depending on a functional state.     

Unilateral vibrissa contact: changes in amplitude but not timing of rhythmic whisking

Electromyographic recordings from the mystacial pad of rats were used to assess the effect of unilateral vibrissa contact on the bilateral movement of the vibrissae. A first group of animals was trained to whisk freely in air and served to establish the baseline variability in bilateral symmetry. We observed that the electromyogram (EMG) activity across the two mystacial pads was rhythmic and synchronous to within 2 ms on a whisk-by-whisk basis; this value is small in comparison with the approximately 50 ms required for protraction during the whisk cycle. A second group of animals was trained to use their vibrissae to contact a sensor that was located on one side of the head. The average EMG activity across the two pads was synchronous at the time of vibrissa contact, albeit with higher variability than for the case of free whisking. In contrast, the average amplitude of the activity on the contact vs noncontact side of the face was transiently greater, by 25% or approximately 10 degrees, at the time of contact. These data show that the amplitude of the vibrissae on the two sides of the face can be controlled independently, while the timing of vibrissa movement is largely synchronous.     

Neural correlates of vibrissa resonance; band-pass and somatotopic representation of high-frequency stimuli

The array of vibrissae on a rat's face is the first stage of a high-resolution tactile sensing system. Recently, it was discovered that vibrissae (whiskers) resonate when stimulated at specific frequencies, generating several-fold increases in motion amplitude. We investigated the neural correlates of vibrissa resonance in trigeminal ganglion and primary somatosensory cortex (SI) neurons (regular and fast spiking units) by presenting low-amplitude, high-frequency vibrissa stimulation. We found that somatosensory neurons showed band-pass tuning and enhanced sensitivity to small amplitude stimuli, reflecting the resonance amplification of vibrissa motion. Further, a putative somatotopic map of frequency selectivity was observed in SI, with isofrequency columns extending along the representations of arcs of vibrissae, in agreement with the gradient in vibrissa resonance across the vibrissa pad. These findings suggest several parallels between frequency processing in the vibrissa system and the auditory system and have important implications for detection and discrimination of tactile information.     

Afferent inhibition and functional properties of neurons in the vibrissae projection area of the cat somatosensory cortex]

The aim of this study was to investigate the role of inhibitory processes in S-1 cortex of cats. The inhibition was evoked by "natural" afferent stimulation of the fascial vibrissae. For this purpose, two neighboring vibrissae were sequentially stimulated by mechanical deflection; single unit activity was recorded simultaneously from the cortex. Results showed that conditioning by afferent stimulation significantly influenced the directional sensitivity of cortical neurons. These data and analysis of spatial pattern of stimulated vibrissa indicate that detector neurons could be quickly modified during sensory processing.     

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.     

Movements of the cranial vibrissae in the Golden hamster (Mesocricetus auratus)

Vibrissae are highly refined vibrotactile receptors that are present on most mammals. The Golden hamster exhibits three different behaviours of its mystacial, supraorbital, and genal vibrissae. During rest, all the vibrissae are reclined and motionless. When hamsters are alert, the vibrissae are partly or fully erect and essentially motionless. During active investigation, the mystacial vibrissae "whisk" or "sweep" through antero–posterior excursions. The genal vibrissa moves only slightly in periodic erection. The supraorbital vibrissae carry through a wide erection arc and have limited excursions with movements of the upper eyelid. The mystacial vibrissae whisk quickly (about 16 sweepsls). Whisking is divisible into contact (relatively high amplitude, low frequency), non–contact (relatively low amplitude, high frequency), and double–pump (combination contact and non–contact) types, and can be either bilaterally symmetric or asymmetric. The dimensions of the mystacial territory around the snout change throughout whisking due to coordinated changes in the shape of the mystacial pad and the tilting of the vibrissae relative to the pad. Such differential movements have implications for sensory physiology as they point to an ability for fine sensory monitoring of the environment.     

A Penile Spine/Vibrissa Enhancer Sequence Is Missing in Modern and Extinct Humans but Is Retained in Multiple Primates with Penile Spines and Sensory Vibrissae

Previous studies show that humans have a large genomic deletion downstream of the Androgen Receptor gene that eliminates an ancestral mammalian regulatory enhancer that drives expression in developing penile spines and sensory vibrissae. Here we use a combination of large-scale sequence analysis and PCR amplification to demonstrate that the penile spine/vibrissa enhancer is missing in all humans surveyed and in the Neandertal and Denisovan genomes, but is present in DNA samples of chimpanzees and bonobos, as well as in multiple other great apes and primates that maintain some form of penile integumentary appendage and facial vibrissae. These results further strengthen the association between the presence of the penile spine/vibrissa enhancer and the presence of penile spines and macro- or micro- vibrissae in non-human primates as well as show that loss of the enhancer is both a distinctive and characteristic feature of the human lineage.     

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.     

Radial distance determination in the rat vibrissal system and the effects of Weber's law

Rats rhythmically tap and brush their vibrissae (whiskers) against objects to tactually explore the environment. To extract a complex feature such as the contour of an object, the rat must at least implicitly estimate radial object distance, that is, the distance from the base of the vibrissa to the point of object contact. Radial object distance cannot be directly measured, however, because there are no mechanoreceptors along the vibrissa. Instead, the mechanical signals generated by the vibrissa's interaction with the environment must be transmitted to mechanoreceptors near the vibrissa base. The first part of this paper surveys the different mechanical methods by which the rat could determine radial object distance. Two novel methods are highlighted: one based on measurement of bending moment and axial force at the vibrissa base, and a second based on measurement of how far the vibrissa rotates beyond initial contact. The second part of the paper discusses the application of Weber's law to two methods for radial distance determination. In both cases, Weber's law predicts that the rat will have greatest sensing resolution close to the vibrissa tip. These predictions could be tested with behavioural experiments that measure the perceptual acuity of the rat.     

A comparative analysis of vibrissa count and infraorbital foramen area in primates and other mammals

Vibrissae are specialized sensory “hairs” that respond to mechanical stimuli. Sensory information from vibrissae is transmitted to the brain via the infraorbital nerve, which passes through the infraorbital foramen (IOF). Several analyses have documented that primates have smaller IOFs than non-primate mammals, and that haplorhines have smaller IOFs than strepsirrhines. These grade shifts in IOF area were attributed to differences in “vibrissa development.” Following earlier analyses, IOF area has been used to derive a general estimate of “whiskeredness” in extinct primates, and consequently, IOF area has been used in phylogenetic and paleoecological interpretations. Yet, the relationship between IOF area and vibrissa count has not been tested, and little is known about how IOF area and vibrissa counts vary among mammals. This study explores how relative IOF area and vibrissa count differ among 25 mammalian orders, and tests for a correlation between IOF area and vibrissa count. Results indicate that primates and dermopterans (Primatomorpha) have smaller IOFs than most non-primate mammals, but they do not have fewer vibrissae. In addition, strepsirrhines and haplorhines do not differ from one another in relative IOF area or vibrissa counts. Despite different patterns documented for IOF area and vibrissa count variation across mammals, results from this study do confirm that vibrissa count and IOF area are significantly and positively correlated (p < 0.0001). However, there is considerable scatter in the data, suggesting that vibrissa counts cannot be predicted from IOF area. There are three implications of these finding. First, IOF area reflects all mechanoreceptors in the maxillary region, not just vibrissae. Second, IOF area may be an informative feature in interpretations of the fossil record. Third, paleoecological interpretations based on vibrissae are not recommended.     

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.     

Learning-induced plasticity in the barrel cortex is disrupted by inhibition of layer 4 somatostatin-containing interneurons

Gaba-ergic neurons are a diverse cell class with extensive influence over cortical processing, but their role in experience-dependent plasticity is not completely understood. Here we addressed the role of cortical somatostatin- (SOM-INs) and vasoactive intestinal polypeptide- (VIP-INs) containing interneurons in a Pavlovian conditioning where stimulation of the vibrissae is used as a conditioned stimulus and tail shock as unconditioned one. This procedure induces a plastic change observed as an enlargement of the cortical functional representation of vibrissae activated during conditioning. Using layer-targeted, cell-selective DREADD transductions, we examined the involvement of SOM-INs and VIP-INs activity in learning-related plastic changes. Under optical recordings, we injected DREADD-expressing vectors into layer IV (L4) barrels or layer II/III (L2/3) areas corresponding to the activated vibrissae. The activity of the interneurons was modulated during all conditioning sessions, and functional 2-deoxyglucose (2DG) maps were obtained 24 h after the last session.In mice with L4 but not L2/3 SOM-INs suppressed during conditioning, the plastic change of whisker representation was absent. The behavioral effect of conditioning was disturbed. Both L4 SOM-INs excitation and L2/3 VIP-INs inhibition during conditioning did not affect the plasticity or the conditioned response.We found the activity of L4 SOM-INs is indispensable in the formation of learning-induced plastic change. We propose that L4 SOM-INs may provide disinhibition by blocking L4 parvalbumin interneurons, allowing a flow of information into upper cortical layers during learning.     

Diving in darkness: whiskers as sense organs of the ringed seal (Phoca hispida saimensis)

Underwater vocalization and the functional structure of different vibrissae of the ringed seal ( Phoca hispida saimensis ) of Lake Saimaa, Eastern Finland, were studied. These seals live in darkness under the ice cover for several months during the year. It is known that blind seals are managing well in the lake. Visibility under water in some parts of the area where the seals live is only 2 m. It is suggested that echolocation is used in orientation and feeding. The Saimaa seal has click and click trial underwater vocalizations. However, both the frequency and intensity of the vocalization are low compared with, for example, those of dolphins. The structural adaptations for underwater sound localization are also not well developed.
The ringed seal has, however, extremely well-developed vibrissae. The innervation of one vibrissa is more than 10 times greater than normally found in mammals. The main structural deviations from normal mammalian vibrissae are: (1) an upper cavernous sinus, (2) a groove in the wall of the capsule at the level of the lower cavernous sinus, (3) elasticity of the connective tissue bands fixing the hair root to the capsule in the lower cavernous sinus and especially (4) the structure and innervation of the ring sinus area. Sensory elements are situated upon the glassy membrane on the surface of the outer rootsheath and in the basal cell layer of the outer rootsheath which is like a sensory epithelium. Below this epithelium a layer of liquid or gelatinous material and large amounts of glycogen are found. This sensory epithelium is especially well developed in the superciliary vibrissae. These vibrissae are protruded some millimetres when the seals are attentive. It is suggested that the vibrissae also sense sounds, which are transmitted to the sensory elements by tissue conduction through the capsule wall and via the blood sinuses. The seals may possibly detect compressional waves with the vibrissae.     

Facial morphology and vibrissal movement in the golden hamster

The major cranial vibrissae in the golden hamster can be moved in complex ways that suggest they are served by a finely controlled motor system. Movements are hypothesized to be the products of differential blood flow and pressure regulation in the sinus surrounding each vibrissal follicle, contractions of the striated facial muscles, and elastic rebound in the connective tissues. The vasculature contributes hydrostatic forces that erect the vibrissae slightly and distort their connective tissue bedding, rigidify the vibrissal capsules, thus forming firm bases of attachment for certain facial muscles, and theoretically provide a pressure plate around the follicle, important in lowering the firing thresholds of receptor endings. The facial muscles supply the major forces in erection and protraction of the vibrissae by acting on both the capsules and the connective tissue bedding. The connective tissues are organized into capsular and extracapsular systems that serve to stabilize the vibrissae and return them to initial rest positions. The slight movements of the genal vibrissa are the effects of vascular and connective tissue dynamics, the musculature being uninvolved. Wide angle movements of the supraorbital vibrissae are products of the vasculature and connective tissues, plus contractions of the Mm. orbicularis oculi and frontalis. Mystacial vibrissal movement is quite complex. The vasculature supplies a small degree of capsular erection and mystacial pad distortion, but primarily rigidifies the capsules. The bulk of erection and protraction is produced by the M. nasolabialis profundus (NLP) and the vibrissal capsular muscles (VCM). The NLP distorts the mystacial pad; the VCM tilt the capsules relative to the pad. Retraction is mainly accomplished by elastic rebound in the pad, this being aided in its extreme degrees by the Mm. nasolabialis and maxillolabialis. The Mm. nasolabialis superficialis and buccinator pars orbicularis oris help to spread the vibrissae into a dorsoventral fan and stabilize the mystacial pad during whisking.