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.     

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.     

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.     

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.     

Motor cortex gates vibrissal responses in a thalamocortical projection pathway

Higher-order thalamic nuclei receive input from both the cerebral cortex and prethalamic sensory pathways. However, at rest these nuclei appear silent due to inhibitory input from extrathalamic regions, and it has therefore remained unclear how sensory gating of these nuclei takes place. In the rodent, the ventral division of the zona incerta (ZIv) serves as a relay station within the paralemniscal thalamocortical projection pathway for whisker-driven motor activity. Most, perhaps all, ZIv neurons are GABAergic, and recent studies have shown that these cells participate in a feedforward inhibitory circuit that blocks sensory transmission in the thalamus. The present study provides evidence that the stimulation of the vibrissa motor cortex suppresses vibrissal responses in ZIv via an intra-incertal GABAergic circuit. These results provide support for the proposal that sensory transmission operates via a top-down disinhibitory mechanism that is contingent on motor activity.     

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.     

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.     

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.     

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.     

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.     

Conditioned Whisking in the Rat

The rat's mystacial vibrissae are active during exploratory and discriminative behaviors, with individual vibrissae serving as elements in a receptive array scanned across object surfaces. To facilitate neurobehavioral analysis of this sensorimotor system, we have developed an experimental paradigm that confines vibrissa movements to a defined physical location, makes possible on-line monitoring of “whisking” activity, and brings such activity under associative control using operant conditioning procedures. Rats were secured, and movements of an identified bilaterally homologous pair of vibrissae (right and left gamma straddlers) were detected by laser-based photodetectors. Subjects were maintained on a water deprivation schedule, and whisker movements were monitored during adaptation to the test situation and after the clipping of other vibrissae on both sides of the snout. Rats were reinforced with water delivery for emitting vibrissa movements in the presence of a conditioned stimulus (tone) whose presentation was made contingent upon a prior period of nonwhisking. The rate and temporal distribution of vibrissa movements were brought under experimental control by means of interval and ratio reinforcement schedules. Although the procedures provide minimal information about the kinematics or topography of conditioned vibrissa movements, they permit the investigator to manipulate response parameters normally under the voluntary control of the animal in a preparation amenable to neurophysiological analysis     

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.     

Parietal control of hand action

Recent advances suggest that neurons of the anterior intraparietal area play a critical role in the visual guidance of hand action. The parietal cortex appears to process in-coming binocular visual signals of the three-dimensional features of objects and matches these signals with the motor signals, which come from the ventral premotor cortex, that will be required for hand manipulation of the object.     

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.     

The role of the posterior parietal cortex in coordinate transformations for visual-motor integration

Lesion to the posterior parietal cortex in monkeys and humans produces spatial deficits in movement and perception. In recording experiments from area 7a, a cortical subdivision in the posterior parietal cortex in monkeys, we have found neurons whose responses are a function of both the retinal location of visual stimuli and the position of the eyes in the orbits. By combining these signals area 7 a neurons code the location of visual stimuli with respect to the head. However, these cells respond over only limited ranges of eye positions (eye-position-dependent coding). To code location in craniotopic space at all eye positions (eye-position-independent coding) an additional step in neural processing is required that uses information distributed across populations of area 7a neurons. We describe here a neural network model, based on back-propagation learning, that both demonstrates how spatial location could be derived from the population response of area 7a neurons and accurately accounts for the observed response properties of these neurons.     

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.     

Increased activity in human visual cortex during directed attention in the absence of visual stimulation

When subjects direct attention to a particular location in a visual scene, responses in the visual cortex to stimuli presented at that location are enhanced, and the suppressive influences of nearby distractors are reduced. What is the top-down signal that modulates the response to an attended versus an unattended stimulus? Here, we demonstrate increased activity related to attention in the absence of visual stimulation in extrastriate cortex when subjects covertly directed attention to a peripheral location expecting the onset of visual stimuli. Frontal and parietal areas showed a stronger signal increase during this expectation than did visual areas. The increased activity in visual cortex in the absence of visual stimulation may reflect a top-down bias of neural signals in favor of the attended location, which derives from a fronto-parietal network.     

Frisking the whiskers: patterned sensory input in the rat vibrissa system

How are two prominent environmental features, surface texture and object location, transduced and encoded as rats whisk? Recent papers show that textures may excite intrinsic mechanical vibrations of the vibrissae. Although these vibrations are too rapid to be directly followed by cortical neurons, there is evidence that their speed is encoded by contact-dependent sensory signals. In addition to contact, sensory signals exist that report the angular position of the vibrissae. The combination of contact and reference signals may be used to decode spatial variations in the environment, particularly the location of objects in head-centered coordinates.     

Crossmodal processing of object features in human anterior intraparietal cortex: an fMRI study implies equivalencies between humans and monkeys

The organization of macaque posterior parietal cortex (PPC) reflects its functional specialization in integrating polymodal sensory information for object recognition and manipulation. Neuropsychological and recent human imaging studies imply equivalencies between human and macaque PPC, and in particular, the cortex buried in the intraparietal sulcus (IPS). Using functional MRI, we tested the hypothesis that an area in human anterior intraparietal cortex is activated when healthy subjects perform a crossmodal visuo-tactile delayed matching-to-sample task with objects. Tactile or visual object presentation (encoding and recognition) both significantly activated anterior intraparietal cortex. As hypothesized, neural activity in this area was further enhanced when subjects transferred object information between modalities (crossmodal matching). Based on both the observed functional properties and the anatomical location, we suggest that this area in anterior IPS is the human equivalent of macaque area AIP.     

Hippocampal representation of touch-guided behavior in rats: persistent and independent traces of stimulus and reward location

Understanding the mechanisms by which sensory experiences are stored remains a compelling challenge for neuroscience. Previous work has described how the activity of neurons in the sensory cortex allows rats to discriminate the physical features of an object contacted with their whiskers. But to date there is no evidence about how neurons represent the behavioural significance of tactile stimuli, or how they are encoded in memory. To investigate these issues, we recorded single-unit firing and local field potentials from the CA1 region of hippocampus while rats performed a task in which tactile stimuli specified reward location. On each trial the rat touched a textured plate with its whiskers, and then turned towards the Left or Right water spout. Two textures were associated with each reward location. To determine the influence of the rat's position on sensory coding, we placed it on a second platform in the same room where it performed the identical texture discrimination task. Over 25 percent of the sampled neurons encoded texture identity--their firing differed for two stimuli associated with the same reward location--and over 50 percent of neurons encoded the reward location with which the stimuli were associated. The neuronal population carried texture and reward location signals continuously, from the moment of stimulus contact until the end of reward collection. The set of neurons discriminating between one texture pair was found to be independent of, and partially overlapping, the set of neurons encoding the discrimination between a different texture pair. In a given neuron, the presence of a tactile signal was uncorrelated with the presence, magnitude, or timing of reward location signals. These experiments indicate that neurons in CA1 form a texture representation independently of the action the stimulus is associated with and retain the stimulus representation through reward collection.