Tactile Receptive Fields Research Articles

Temporal coherency of mechanical stimuli modulates tactile form perception

The human hand can detect both form and texture information of a contact surface. The detection of skin displacement (sustained stimulus) and changes in skin displacement (transient stimulus) are thought to be mediated in different tactile channels; however, tactile form perception may use both types of information. Here, we studied whether both the temporal frequency and the temporal coherency information of tactile stimuli encoded in sensory neurons could be used to recognize the form of contact surfaces. We used the fishbone tactile illusion (FTI), a known tactile phenomenon, as a probe for tactile form perception in humans. This illusion typically occurs with a surface geometry that has a smooth bar and coarse textures in its adjacent areas. When stroking the central bar back and forth with a fingertip, a human observer perceives a hollow surface geometry even though the bar is physically flat. We used a passive high-density pin matrix to extract only the vertical information of the contact surface, suppressing tangential displacement from surface rubbing. Participants in the psychological experiment reported indented surface geometry by tracing over the FTI textures with pin matrices of the different spatial densities (1.0 and 2.0 mm pin intervals). Human participants reported that the relative magnitude of perceived surface indentation steeply decreased when pins in the adjacent areas vibrated in synchrony. To address possible mechanisms for tactile form perception in the FTI, we developed a computational model of sensory neurons to estimate temporal patterns of action potentials from tactile receptive fields. Our computational data suggest that (1) the temporal asynchrony of sensory neuron responses is correlated with the relative magnitude of perceived surface indentation and (2) the spatiotemporal change of displacements in tactile stimuli are correlated with the asynchrony of simulated sensory neuron responses for the fishbone surface patterns. Based on these results, we propose that both the frequency and the asynchrony of temporal activity in sensory neurons could produce tactile form perception.

Non-informative vision improves spatial tactile discrimination on the shoulder but does not influence detection sensitivity

Vision of the body has been reported to improve tactile acuity even when vision is not informative about the actual tactile stimulation. However, it is currently unclear whether this effect is limited to body parts such as hand, forearm or foot that can be normally viewed, or it also generalizes to body locations, such as the shoulder, that are rarely before our own eyes. In this study, subjects consecutively performed a detection threshold task and a numerosity judgment task of tactile stimuli on the shoulder. Meanwhile, they watched either a real-time video showing their shoulder or simply a fixation cross as control condition. We show that non-informative vision improves tactile numerosity judgment which might involve tactile acuity, but not tactile sensitivity. Furthermore, the improvement in tactile accuracy modulated by vision seems to be due to an enhanced ability in discriminating the number of adjacent active electrodes. These results are consistent with the view that bimodal visuotactile neurons sharp tactile receptive fields in an early somatosensory map, probably via top-down modulation of lateral inhibition.

From statistical regularities in multisensory inputs to peripersonal space representation and body ownership: Insights from a neural network model.

Peripersonal space (PPS), the interface between the self and the environment, is represented by a network of multisensory neurons with visual (or auditory) receptive fields anchored to specific body parts, and tactile receptive fields covering the same body parts. Neurophysiological and behavioural features of hand PPS representation have been previously modelled through a neural network constituted by one multisensory population integrating tactile inputs with visual/auditory external stimuli. Reference frame transformations were not explicitly modelled, as stimuli were encoded in pre‐computed hand‐centred coordinates. Here we present a novel model, aiming to overcome this limitation by including a proprioceptive population encoding hand position. We confirmed behaviourally the plausibility of the proposed architecture, showing that visuo‐proprioceptive information is integrated to enhance tactile processing on the hand. Moreover, the network's connectivity was spontaneously tuned through a Hebbian‐like mechanism, under two minimal assumptions. First, the plasticity rule was designed to learn the statistical regularities of visual, proprioceptive and tactile inputs. Second, such statistical regularities were simply those imposed by the body structure. The network learned to integrate proprioceptive and visual stimuli, and to compute their hand‐centred coordinates to predict tactile stimulation. Through the same mechanism, the network reproduced behavioural correlates of manipulations implicated in subjective body ownership: the invisible and the rubber hand illusion. We thus propose that PPS representation and body ownership may emerge through a unified neurocomputational process; the integration of multisensory information consistently with a model of the body in the environment, learned from the natural statistics of sensory inputs.

A mechanism for spatial perception on human skin

Our perception of where touch occurs on our skin shapes our interactions with the world. Most accounts of cutaneous localisation emphasise spatial transformations from a skin-based reference frame into body-centred and external egocentric coordinates. We investigated another possible method of tactile localisation based on an intrinsic perception of ‘skin space’. The arrangement of cutaneous receptive fields (RFs) could allow one to track a stimulus as it moves across the skin, similarly to the way animals navigate using path integration. We applied curved tactile motions to the hands of human volunteers. Participants identified the location midway between the start and end points of each motion path. Their bisection judgements were systematically biased towards the integrated motion path, consistent with the characteristic inward error that occurs in navigation by path integration. We thus showed that integration of continuous sensory inputs across several tactile RFs provides an intrinsic mechanism for spatial perception.

A chronic neural interface to the macaque dorsal column nuclei.

The dorsal column nuclei (DCN) of the brain stem contain secondary afferent neurons, which process ascending somatosensory information. Most of the known physiology of the DCN in primates has been acquired in acute experiments with anesthetized animals. Here, we developed a technique to implant a multielectrode array (MEA) chronically in the DCN of macaque monkeys to enable experiments with the animals awake. Two monkeys were implanted with brain-stem MEAs for 2-5 mo with no major adverse effects. Responses of the cuneate and gracile nuclei were quantified at the level of both field potentials and single units. Tactile receptive fields (RFs) were identified for 315 single units. A subset of these units had very regular spiking patterns with spike frequencies predominantly in the alpha band (8-14 Hz). The stability of the neuronal recordings was assessed with a novel analysis that identified units by their mean spike waveform and by the spike-triggered average of activity on all other electrodes in the array. Fifty-six identified neurons were observed over two or more sessions and in a few cases for as long as 1 mo. RFs of stable neurons were largely consistent across days. The results demonstrate that a chronic DCN implant in a macaque can be safe and effective, yielding high-quality unit recording for several months. The unprecedented access to these nuclei in awake primates should lead to a better understanding of their role in sensorimotor behavior.

Activity of somatosensory-responsive neurons in high subdivisions of SI cortex during locomotion.

Responses of neurons in the primary somatosensory cortex during movements are poorly understood, even during such simple tasks as walking on a flat surface. In this study, we analyzed spike discharges of neurons in the rostral bank of the ansate sulcus (areas 1-2) in 2 cats while the cats walked on a flat surface or on a horizontal ladder, a complex task requiring accurate stepping. All neurons (n = 82) that had receptive fields (RFs) on the contralateral forelimb exhibited frequency modulation of their activity that was phase locked to the stride cycle during simple locomotion. Neurons with proximal RFs (upper arm/shoulder) and pyramidal tract-projecting neurons (PTNs) with fast-conducting axons tended to fire at peak rates in the middle of the swing phase, whereas neurons with RFs on the distal limb (wrist/paw) and slow-conducting PTNs typically showed peak firing at the transition between swing and stance phases. Eleven of 12 neurons with tactile RFs on the volar forepaw began firing toward the end of swing, with peak activity occurring at the moment of foot contact with floor, thereby preceding the evoked sensory volley from touch receptors. Requirement to step accurately on the ladder affected 91% of the neurons, suggesting their involvement in control of accuracy of stepping. During both tasks, neurons exhibited a wide variety of spike distributions within the stride cycle, suggesting that, during either simple or ladder locomotion, they represent the cycling somatosensory events in their activity both predictively before and reflectively after these events take place.

Referral of touch and ownership between the hands and the role of the somatosensory cortices.

Recent studies have shown that the feeling of body ownership can be fooled by simple visuo-tactile manipulations. Perceptual illusions have been reported in which participants sense phantom touch seen on a rubber hand (rubber hand illusion). While previous studies used homologous limbs for those experiments, we here examined an illusion where people feel phantom touch on a left rubber hand when they see it brushed simultaneously with brushes applied to their right hand. Thus, we investigated a referral of touch from the right to the left hand (across the body midline). Since it is known from animal studies that tactile illusions may alter early sensory processing, we expected a modulation of the primary somatosensory cortex (SI) corresponding to this illusion. Neuromagnetic source imaging of the functional topographic organization in SI showed a shift in left SI, associated with the strength of the referral of touch. Hence, we argue that SI seems to be closely associated with this perceptual illusion. The results suggest that the transfer of tactile information across the body midline could be mediated by neurons with bilateral tactile receptive fields (most likely BA2).

Weber's illusion and body shape: Anisotropy of tactile size perception on the hand.

The perceived distance between touches on a single skin surface is larger on regions of high tactile sensitivity than those with lower acuity, an effect known as Weber's illusion. This illusion suggests that tactile size perception involves a representation of the perceived size of body parts preserving characteristics of the somatosensory homunculus. Here, we investigated how body shape is coded within this representation by comparing tactile distances presented in different orientations on the hand. Participants judged which of two tactile distances on the dorsum of their left hand felt larger. One distance was aligned with the proximodistal axis (along the hand), the other with the mediolateral axis (across the hand). Across distances were consistently perceived as larger than along ones. A second experiment showed that this effect is specific to the hairy skin of the hand dorsum and does not occur on glabrous skin of the palm. A third experiment demonstrated that this bias reflects orientation on the hand surface, rather than an eye- or torso-centered reference frame. These results mirror known orientational anisotropies of both tactile acuity and of tactile receptive fields (RFs) of cortical neurons. We suggest that the dorsum of the hand is implicitly represented as wider than it actually is and that the shape of tactile RFs may partly explain distortions of mental body representations.

Textural-input-driven self-organization of tactile receptive fields

Sensory neurons in the primary sensory cortices preferentially respond to specific patterns of input. Our hypothesis is that tactile receptive fields (TRFs) can be self-organized using the same cortical development mechanism found in the visual cortex, simply by exposing it to texture-like inputs. We used the LISSOM model of visual cortical development [1] to test our hypothesis. The results showed that texture-like inputs lead to the self-organization of TRFs while natural-scene-like inputs lead to visual receptive fields (VRFs). We analyzed the effectiveness of the TRFs and VRFs in representing texture, using kernel Fisher discriminant analysis (KFD) [2]. The responses to different classes of textural input were more clearly separable for the TRF than for the VRF. To quantify the merit of the different RF types in dealing with textural input, we measured classification performance. We ran the experiment for 30 times and for each experiment 50% of data set were randomly used as training set and the rest as testing set. As a classifier, k-nearest neighbor (kNN) was used. Average classification rates were 89.8% (for TRF-based) and 83.4% (for VRF-based) respectively. The main results suggest that tactile RFs can be self-organized by texturelike input using a general cortical development model (LISSOM) initially inspired by the visual cortex, and that the representations from tactile RFs are better than visionbased ones for texture tasks. We expect our results to help us better understand the nature of texture as a fundamentally tactile property.

Visual, Somatosensory, and Bimodal Activities in the Macaque Parietal Area PEc

Caudal area PE (PEc) of the macaque posterior parietal cortex has been shown to be a crucial node in visuomotor coordination during reaching. The present study was aimed at studying visual and somatosensory organization of this cortical area. Visual stimulations activated 53% of PEc neurons. The overwhelming majority (89%) of these visual cells were best activated by a dark stimulus on a lighter background. Somatosensory stimulations activated 56% of PEc neurons: most were joint neurons (73%); a minority (24%) showed tactile receptive fields, most of them located on the arms. Area PEc has not a clear retinotopy or somatotopy. Among the cells tested for both somatosensory and visual sensitivity, 22% were bimodal, 25% unimodal somatosensory, 34% unimodal visual, and 19% were insensitive to either stimulation. No clear clustering of the different classes of sensory neurons was observed. Visual and somatosensory receptive fields of bimodal cells were not in register. The damage in the human brain of the likely homologous of macaque PEc produces deficits in locomotion and in whole-body interaction with the visual environment. Present data show that macaque PEc has sensory properties and a functional organization in line with the view of an involvement of this area in those processes.

Progress in Understanding Spatial Coordinate Systems in the Primate Brain

A new study in this issue of Neuron shows that when monkeys reach to a visual target, neurons in the dorsal premotor cortex compare the location of the target, the hand, and the point of visual fixation. The neurons therefore encode space through a combination of eye-centered and hand-centered coordinates.

Cortical influences on rapid brainstem plasticity

Cortical contributions to brainstem plasticity in the somatosensory system are poorly understood. Tactile receptive fields (RFs) of brainstem dorsal column nuclei (DCN) neurons rapidly enlarge when peripheral inputs are disrupted by local anesthetic blocks with lidocaine (LID). Cortical inputs appear to influence this plasticity because enlargements have been shown to be greater when cortical inputs are disrupted. Like disruptions of peripheral inputs, disruptions of DCN inhibition by DCN administration of the GABAA receptor antagonist bicuculline methiodide (BMI) also cause rapid enlargements of DCN RFs when cortical inputs are intact. These findings leave questions about interactions between cortical inputs, DCN inhibition, and DCN RF plasticity. To study potential interactions, the present experiments evaluated RF sizes of DCN tactilely responsive neurons in anesthetized rats following DCN microinjection of BMI when cortical inputs were acutely disrupted or intact. These tests were also supplemented by subsequent LID tests to directly compare post-BMI and post-LID effects on the same RF. BMI caused DCN RF enlargements when cortical inputs were disrupted or intact; however, enlargements after cortical input disruption were greater than when cortical inputs were intact. Following RF enlargement and retraction after BMI, LID often caused a second enlargement of the same RF, across skin that partially matched skin involved in the enlargement after BMI. This occurred when cortical inputs were disrupted or intact. We hypothesize that cortical inputs are not required for BMI and LID to initiate partially matching enlargements in individual DCN tactile RFs, however, cortical inputs constrain magnitudes of these enlargements.

Somatosensory Cells in Area PEc of Macaque Posterior Parietal Cortex

PEc is an area defined on cytoarchitectural grounds, located in the posterior part of the superior parietal lobule of macaque brain (Pandya and Seltzer, 1982). The aim of this work was to assess whether passive somatosensory stimulation elicited responses in PEc neurons. Extracellular recordings were performed in three awake Macaca fascicularis. Passive somatosensory stimulation was performed in darkness, and eye movements were monitored continuously. Recording sites were assigned to different areas according to the cytoarchitectonic criteria described by Pandya and Seltzer (1982) and Luppino et al. (2005). Only recording sites within the limits of the cytoarchitecturally defined area PEc were taken into account in this work. Of 147 PEc cells, 83 (56%) were modulated by passive somatosensory stimulation. The majority of them (73%) responded to joint rotations, and 24% responded to tactile skin stimulation. The majority of PEc somatosensory responses (90%) were evoked by contralateral stimulation. Joint-modulated cells were mostly activated by the upper limbs (82%). The majority of tactile receptive fields (61%) were located on the arms, and a minority was located on the legs and trunk. One-half of PEc somatosensory cells were polysensory, because they were sensitive to visual stimulation. The majority of PEc somatosensory cells were activated by active reaching movements. Somatosensory cells, somatosensory submodalities, and body part representations were not clustered in PEc subregions; in other words, PEc does not show a somatotopic organization. Although the caudal sector of the superior parietal lobule has been traditionally considered as a somatosensory area, this is the first demonstration of the presence of somatosensory cells in this cortical region.

Vibrotactile Coding Capacities of Spinocervical Tract Neurons in the Cat

The response characteristics and tactile coding capacities of individual dorsal horn neurons, in particular, those of the spinocervical tract (SCT), have been examined in the anesthetized cat. Twenty one of 38 neurons studied were confirmed SCT neurons based on antidromic activation procedures. All had tactile receptive fields on the hairy skin of the hindlimb. Most (29/38) could also be activated transynaptically by electrical stimulation of the cervical dorsal columns, suggesting that a common set of tactile primary afferent fibers may provide the input for both the dorsal column-lemniscal pathway and for parallel ascending pathways, such as the SCT. All but 3 of the 38 neurons studied displayed a pure dynamic sensitivity to controlled tactile stimuli but were unable to sustain their responsiveness throughout 1s trains of vibration at vibration frequencies exceeding 5-10 Hz. Stimulus-response relations revealed a very limited capacity of individual SCT neurons to signal, in a graded way, the intensity parameter of the vibrotactile stimulus. Furthermore, because of their inability to respond on a cycle-by-cycle pattern at vibration frequencies >5-10 Hz, these neurons were unable to provide any useful signal of vibration frequency beyond the very narrow bandwidth of approximately 5-10 Hz. Similar limitations were observed in the responsiveness of these neurons to repetitive forms of antidromic and transynaptic inputs generated by electrical stimulation of the spinal cord. In summary, the observed limitations on the vibrotactile bandwidth of SCT neurons and on the precision and fidelity of their temporal signaling, suggest that SCT neurons could serve as little more than coarse event detectors in tactile sensibility, in contrast to DCN neurons the bandwidth of vibrotactile responsiveness of which may extend beyond 400 Hz and is therefore broader by approximately 40-50 times than that of SCT neurons.

Cortical influences on sizes and rapid plasticity of tactile receptive fields in the dorsal column nuclei

The cerebral cortex influences subcortical processing. In the somatosensory system, descending cortical inputs contribute in specific ways to the sizes and plasticity of tactile receptive fields (RFs) in the thalamus, but less is known about cortical influences on these aspects of brainstem RFs. The present studies evaluated how loss of cortical inputs affects sizes and plasticity of RFs in the brainstem dorsal column nuclei (DCN) when peripheral inputs were normal and when peripheral inputs were acutely disrupted. Loss of cortical inputs was produced by acute lesion of somatosensory, motor, and adjacent cortex, whereas disruption of peripheral inputs was produced by cutaneous microinjection of lidocaine (LID). Modest or no changes in sizes of DCN RFs, comparable to changes during control periods of no treatment, were seen in response to cortical lesion. LID caused rapid enlargements in RFs when cortex was intact. LID also caused rapid RF enlargements after cortical lesion, and these enlargements were greater than post-LID enlargements when cortex was intact. These results indicate that normally sized RFs continue to be produced in the DCN after loss of cortical input. Cortex is also not required for RF enlargements after LID; however, cortical inputs have a constraining effect on these enlargements. Considered with findings from previous thalamic studies, these results suggest that cortical influences on RF size and plasticity in the DCN and thalamus differ in some respects.

Reference frames for representing visual and tactile locations in parietal cortex

The ventral intraparietal area (VIP) receives converging inputs from visual, somatosensory, auditory and vestibular systems that use diverse reference frames to encode sensory information. A key issue is how VIP combines those inputs together. We mapped the visual and tactile receptive fields of multimodal VIP neurons in macaque monkeys trained to gaze at three different stationary targets. Tactile receptive fields were found to be encoded into a single somatotopic, or head-centered, reference frame, whereas visual receptive fields were widely distributed between eye- to head-centered coordinates. These findings are inconsistent with a remapping of all sensory modalities in a common frame of reference. Instead, they support an alternative model of multisensory integration based on multidirectional sensory predictions (such as predicting the location of a visual stimulus given where it is felt on the skin and vice versa). This approach can also explain related findings in other multimodal areas.

Complex movements evoked by microstimulation of the ventral intraparietal area.

Most neurons in the ventral intraparietal area (VIP) of the macaque brain respond to both visual and tactile stimuli. The tactile receptive field is usually on the face, and the visual receptive field usually corresponds spatially to the tactile receptive field. In this study, electrical microstimulation of VIP, but not of surrounding tissue, caused a constellation of movements including eye closure, facial grimacing, head withdrawal, elevation of the shoulder, and movements of the hand to the space beside the head or shoulder. A similar set of movements was evoked by an air puff to the monkey's cheek. One interpretation is that VIP contributes to defensive movements triggered by stimuli on or near the head.

Reticular thalamic responses to nociceptive inputs in anesthetized rats

The present study compares nociceptive responses of neurons in the reticular thalamic nucleus (RT) to those of the ventroposterior lateral nucleus (VPL). Extracellular single-unit activities of cells in the RT and VPL were recorded in anesthetized rats. Only units with identified tactile receptive fields in the forepaw or hindpaw were studied. In the first series of experiments, RT and VPL responses to pinching with a small artery clamp were tested with the rats under pentobarbital, urethane, ketamine, or halothane anesthesia. Under all types of anesthesia, many RT units were inhibited. Second, the specificity of the nociceptive response was tested by pinching and noxious heating of the unit’s tactile receptive field. Of the 39 VPL units tested, 20 were excited by both types of noxious stimuli. In sharp contrast, of the 30 RT units tested, none were excited and 17 were inhibited. In a third series of experiments, low-intensity and beam-diffused CO 2 laser irradiation was used to activate peripheral nociceptive afferents. Wide-dynamic-range VPL units responded with short- and long-latency excitations. In contrast, RT units had short-latency excitation followed by long-latency inhibition. Nociceptive input inhibited RT units in less than 500 ms. We conclude that a significant portion of RT neurons were polysynaptically inhibited by nociceptive inputs. Since all the cells tested were excited by light tactile inputs, the somatosensory RT may serve in the role of a modality gate, which modifies (i.e. inhibits) tactile inputs while letting noxious inputs pass.

The clothing effect: tactile neurons in the precentral gyrus do not respond to the touch of the familiar primate chair.

Neurons in a restricted zone in the precentral gyrus of macaque monkeys respond to tactile, visual, and auditory stimuli. The tactile receptive fields of these multimodal cells are usually located on the face, arm, or upper torso. In the present study, in awake monkeys sitting in a primate chair, the neurons responded to a tactile probe touching the skin within the tactile receptive field. However, the same neurons did not respond when the tactile receptive field was touched by the primate chair, to which the monkey was habituated.

Noninformative vision improves the spatial resolution of touch in humans

Research on sensory perception now often considers more than one sense at a time. This approach reflects real-world situations, such as when a visible object touches us. Indeed, vision and touch show great interdependence: the sight of a body part can reduce tactile target detection times [1], visual and tactile attentional systems are spatially linked [2], and the texture of surfaces that are actively touched with the fingertips is perceived using both vision and touch [3]. However, these previous findings might be mediated by spatial attention [1, 2] or by improved guidance of movement [3] via visually enhanced body position sense [4–6]. Here, we investigate the direct effects of viewing the body on passive touch. We measured tactile two-point discrimination thresholds [7] on the forearm while manipulating the visibility of the arm but holding gaze direction constant. The spatial resolution of touch was better when the arm was visible than when it was not. Tactile performance was further improved when the view of the arm was magnified. In contrast, performance was not improved by viewing a neutral object at the arm's location, ruling out improved spatial orienting as a possible account. Controls confirmed that no information about the tactile stimulation was provided by visibility of the arm. This visual enhancement of touch may point to online reorganization of tactile receptive fields.