Active Tactile Discrimination Research Articles

Fronto-Central Changes in Multiple Frequency Bands in Active Tactile Width Discrimination Task.

The neural basis of tactile processing in humans has been extensively studied; however, the neurophysiological basis of human width discrimination remains relatively unexplored. In particular, the changes that occur in neural networks underlying active tactile width discrimination learning have yet to be described. Here, it is hypothesized that subjects learning to perform the active version of the width discrimination task would present changes in behavioral data and in the neurophysiological activity, specifically in networks of electrodes relevant for tactile and motor processing. The specific hypotheses tested here were that the performance and response latency of subjects would change between the first and the second blocks; the power of the different frequency bands would change between the first and the second blocks; electrode F4 would encode task performance and response latency through changes in the power of the delta, theta, alpha, beta, and low-gamma frequency bands; the relative power in the alpha and beta frequency bands in electrodes C3 and C4 (Interhemispheric Spectral Difference-ISD) would change because of learning between the first and the second blocks. To test this hypothesis, we recorded and analyzed electroencephalographic (EEG) activity while subjects performed a session where they were tested twice (i.e., two different blocks) in an active tactile width discrimination task using their right index finger. Subjects (n = 18) presented high performances (high discrimination accuracy) already in their first block, and therefore no significant improvements were found in the second block. Meanwhile, a reduction in response latency was observed between the two blocks. EEG recordings revealed an increase in power for the low-gamma frequency band (30-45 Hz) for electrodes F3 and C3 from the first to the second block. This change was correlated with neither performance nor latency. Analysis of the neural activity in electrode F4 revealed that the beta frequency band encoded the subjects' performance. Meanwhile, the delta frequency band in the same electrode revealed a complex pattern where blocks appeared clustered in two different patterns: an Upper Pattern (UP), where power and latency were highly correlated (Rho = 0.950), and a sparser and more uncorrelated Lower Pattern (LP). Blocks belonging to the UP or LP patterns did not differ in performance and were not specific to the first or the second block. However, blocks belonging to the LP presented an increase in response latency, increased variability in performance, and an increased ISD in alpha and beta frequency bands for the pair of electrodes C3-C4, suggesting that the LP may reflect a state related to increased cognitive load or task difficulty. These results suggest that changes in performance and latency in an active tactile width discrimination task are encoded in the delta, alpha, beta, and low-gamma frequency bands in a fronto-central network. The main contribution of this study is therefore related to the description of neural dynamics in frontal and central networks involved in the learning process of active tactile width discrimination.

Active tactile discrimination is coupled with and modulated by the cardiac cycle.

Perception and cognition are modulated by the phase of the cardiac signal in which the stimuli are presented. This has been shown by locking the presentation of stimuli to distinct cardiac phases. However, in everyday life sensory information is not presented in this passive and phase-locked manner, instead we actively move and control our sensors to perceive the world. Whether active sensing is coupled and modulated with the cardiac cycle remains largely unknown. Here, we recorded the electrocardiograms of human participants while they actively performed a tactile grating orientation task. We show that the duration of subjects' touch varied as a function of the cardiac phase in which they initiated it. Touches initiated in the systole phase were held for longer periods of time than touches initiated in the diastole phase. This effect was most pronounced when elongating the duration of the touches to sense the most difficult gratings. Conversely, while touches in the control condition were coupled to the cardiac cycle, their length did not vary as a function of the phase in which these were initiated. Our results reveal that we actively spend more time sensing during systole periods, the cardiac phase associated with lower perceptual sensitivity (vs. diastole). In line with interoceptive inference accounts, these results indicate that we actively adjust the acquisition of sense data to our internal bodily cycles.

Fast cortical dynamics encode tactile grating orientation during active touch.

Touch-based object recognition relies on perception of compositional tactile features like roughness, shape, and surface orientation. However, besides roughness, it remains unclear how these different tactile features are encoded by neural activity that is linked with perception. Here, we establish a cortex-dependent perceptual task in which mice discriminate tactile gratings on the basis of orientation using only their whiskers. Multielectrode recordings in the barrel cortex reveal weak orientation tuning in average firing rates (500-ms time scale) during grating exploration despite high levels of cortical activity. Just before decision, orientation information extracted from fast cortical dynamics (100-ms time scale) more closely resembles concurrent psychophysical measurements than single neuron orientation tuning curves. This temporal code conveys both stimulus and choice/action-related information, suggesting that fast cortical dynamics during exploration of a tactile object both reflect the physical stimulus and affect the decision.

Recurrent interactions in local cortical circuits.

Most cortical synapses are local and excitatory. Local recurrent circuits could implement amplification, allowing pattern completion and other computations1-4. Cortical circuits contain subnetworks that consist of neurons with similar receptive fields and increased connectivity relative to the network average5,6. Cortical neurons that encode different types of information are spatially intermingled and distributed over large brain volumes5-7, and this complexity has hindered attempts to probe the function of these subnetworks by perturbing them individually8. Here we use computational modelling, optical recordings and manipulations to probe the function of recurrent coupling in layer 2/3 of the mouse vibrissal somatosensory cortex during active tactile discrimination. A neural circuit model of layer 2/3 revealed that recurrent excitation enhances sensory signals by amplification, but only for subnetworks with increased connectivity. Model networks with high amplification were sensitive to damage: loss of a few members of the subnetwork degraded stimulus encoding. We tested this prediction by mapping neuronal selectivity7 and photoablating9,10 neurons with specific selectivity. Ablation of a small proportion of layer 2/3 neurons (10-20, less than 5% of the total) representing touch markedly reduced responses in the spared touch representation, but not in other representations. Ablations most strongly affected neurons with stimulus responses that were similar to those of the ablated population, which is also consistent with network models. Recurrence among cortical neurons with similar selectivity therefore drives input-specific amplification during behaviour.

Frequency-specific coupling in fronto-parieto-occipital cortical circuits underlie active tactile discrimination

Processing of tactile sensory information in rodents is critically dependent on the communication between the primary somatosensory cortex (S1) and higher-order integrative cortical areas. Here, we have simultaneously characterized single-unit activity and local field potential (LFP) dynamics in the S1, primary visual cortex (V1), anterior cingulate cortex (ACC), posterior parietal cortex (PPC), while freely moving rats performed an active tactile discrimination task. Simultaneous single unit recordings from all these cortical regions revealed statistically significant neuronal firing rate modulations during all task phases (anticipatory, discrimination, response, and reward). Meanwhile, phase analysis of pairwise LFP recordings revealed the occurrence of long-range synchronization across the sampled fronto-parieto-occipital cortical areas during tactile sampling. Causal analysis of the same pairwise recorded LFPs demonstrated the occurrence of complex dynamic interactions between cortical areas throughout the fronto-parietal-occipital loop. These interactions changed significantly between cortical regions as a function of frequencies (i.e. beta, theta and gamma) and according to the different phases of the behavioral task. Overall, these findings indicate that active tactile discrimination by rats is characterized by much more widespread and dynamic complex interactions within the fronto-parieto-occipital cortex than previously anticipated.

Mechanisms of tactile sensory deterioration amongst the elderly

It is known that roughness-smoothness, hardness-softness, stickiness-slipperiness and warm-cold are predominant perceptual dimensions in macro-, micro- and nano- texture perception. However, it is not clear to what extent active tactile texture discrimination remains intact with age. The general decrease in tactile ability induces physical and emotional dysfunction in elderly, and has increasing significance for an aging population. We report a method to quantify tactile acuity based on blinded active exploration of systematically varying micro-textured surfaces and a same-different paradigm. It reveals that elderly participants show significantly reduced fine texture discrimination ability. The elderly group also displays statistically lower finger friction coefficient, moisture and elasticity, suggesting a link. However, a subpopulation of the elderly retains discrimination ability irrespective of cutaneous condition and this can be related to a higher density of somatosensory receptors on the finger pads. Skin tribology is thus not the primary reason for decline of tactile discrimination with age. The remediation of cutaneous properties through rehydration, however leads to a significantly improved tactile acuity. This indicates unambiguously that neurological tactile loss can be temporarily compensated by restoring the cutaneous contact mechanics. Such mechanical restoration of tactile ability has the potential to increase the quality of life in elderly.

Neuronal Assemblies Evidence Distributed Interactions within a Tactile Discrimination Task in Rats.

Accumulating evidence suggests that neural interactions are distributed and relate to animal behavior, but many open questions remain. The neural assembly hypothesis, formulated by Hebb, states that synchronously active single neurons may transiently organize into functional neural circuits—neuronal assemblies (NAs)—and that would constitute the fundamental unit of information processing in the brain. However, the formation, vanishing, and temporal evolution of NAs are not fully understood. In particular, characterizing NAs in multiple brain regions over the course of behavioral tasks is relevant to assess the highly distributed nature of brain processing. In the context of NA characterization, active tactile discrimination tasks with rats are elucidative because they engage several cortical areas in the processing of information that are otherwise masked in passive or anesthetized scenarios. In this work, we investigate the dynamic formation of NAs within and among four different cortical regions in long-range fronto-parieto-occipital networks (primary somatosensory, primary visual, prefrontal, and posterior parietal cortices), simultaneously recorded from seven rats engaged in an active tactile discrimination task. Our results first confirm that task-related neuronal firing rate dynamics in all four regions is significantly modulated. Notably, a support vector machine decoder reveals that neural populations contain more information about the tactile stimulus than the majority of single neurons alone. Then, over the course of the task, we identify the emergence and vanishing of NAs whose participating neurons are shown to contain more information about animal behavior than randomly chosen neurons. Taken together, our results further support the role of multiple and distributed neurons as the functional unit of information processing in the brain (NA hypothesis) and their link to active animal behavior.

Simultaneous top-down modulation of the primary somatosensory cortex and thalamic nuclei during active tactile discrimination.

The rat somatosensory system contains multiple thalamocortical loops (TCLs) that altogether process, in fundamentally different ways, tactile stimuli delivered passively or actively sampled. To elucidate potential top-down mechanisms that govern TCL processing in awake, behaving animals, we simultaneously recorded neuronal ensemble activity across multiple cortical and thalamic areas while rats performed an active aperture discrimination task. Single neurons located in the primary somatosensory cortex (S1), the ventroposterior medial, and the posterior medial thalamic nuclei of the trigeminal somatosensory pathways exhibited prominent anticipatory firing modulations before the whiskers touching the aperture edges. This cortical and thalamic anticipatory firing could not be explained by whisker movements or whisker stimulation, because neither trigeminal ganglion sensory-evoked responses nor EMG activity were detected during the same period. Both thalamic and S1 anticipatory activity were predictive of the animal's discrimination accuracy. Inactivation of the primary motor cortex (M1) with muscimol affected anticipatory patterns in S1 and the thalamus, and impaired the ability to predict the animal's performance accuracy based on thalamocortical anticipatory activity. These findings suggest that neural processing in TCLs is launched in anticipation of whisker contact with objects, depends on top-down effects generated in part by M1 activity, and cannot be explained by the classical feedforward model of the rat trigeminal system.

Layer-specific somatosensory cortical activation during active tactile discrimination.

Ensemble neuronal activity was recorded in each layer of the whisker area of the primary somatosensory cortex (SI) while rats performed a whisker-dependent tactile discrimination task. Comparison of this activity with SI activity evoked by similar passive whisker stimulation revealed fundamental differences in tactile signal processing during active and passive stimulation. Moreover, significant layer-specific functional differences in SI activity were observed during active discrimination. These differences could not be explained solely by variations in ascending thalamocortical input to SI. Instead, these results suggest that top-down influences during active discrimination may alter the overall functional nature of SI as well as layer-specific mechanisms of tactile processing.

Cerebellar dentate activity during active tactile discrimination is related to the motor demands of the task

Cerebellar dentate activity during active tactile discrimination is related to the motor demands of the task

Gender Difference in Premotor Activity during Active Tactile Discrimination

To investigate possible gender differences in tactile discrimination tasks, we measured cerebral blood flow of seven men and seven women using positron emission tomography and 15O water during tactile tasks performed with the right index finger. A nondiscrimination, somatosensory control task activated the left primary sensorimotor cortex and the left parietal operculum extending to the posterior insula without any gender difference. Compared with the control task, discrimination tasks activated the superior and inferior parietal lobules bilaterally, right dorsal premotor cortex, and dorsolateral prefrontal cortex in both genders, consistent with the notion of right hemisphere involvement during exploratory attentional movements. In both genders, symmetric activation of the superior and inferior parietal lobules and asymmetric activation of the right dorsolateral prefrontal cortex were confirmed. The former is consistent with the spatial representation of the tactile input and the latter with the spatial working memory. However, activation of the dorsal premotor cortex was asymmetric in men, whereas it was symmetric in women, the gender difference being statistically significant. This may suggest gender differences in motor programs for exploration in manipulospatial tasks such as tactile discrimination with active touch, possibly by greater interhemispheric interaction through the dorsal premotor cortices in women than in men.

Discharge properties of neurones in the hand area of primary somatosensory cortex in monkeys in relation to the performance of an active tactile discrimination task. II. Area 2 as compared to areas 3b and 1.

The discharge patterns of 144 single cortical neurones, within the cutaneous representation of the hand in area 2 (primary somatosensory cortex, SI), were studied in two rhesus monkeys during the performance of an active tactile discrimination task. These were compared to those previously described for units within areas 3b and 1 recorded from the same animals. The task consisted of making a single scanning movement of the digit tips over a surface (first half smooth; second half either smooth or rough). The nature of the texture encountered over the second half of the surface was indicated by the monkey making a differential lever response (push or pull) with the opposite hand. During the task, area 2 units with cutaneous receptive fields (RFs) on the digit tips of interest (those scanned over the surfaces) generally showed an increase in their discharge (75%); patterns of decreased discharge or no modulation (respectively, 12 and 13%) were rarely observed. Units with digital cutaneous RFs not in contact with the stimuli were much more likely to show either a pattern of decreased discharge or no modulation whatsoever (47% in each case), suggesting that there is some selection of cutaneous inputs in this task in that non-active inputs are selectively gated. For units with a cutaneous RF, the sign of modulation changed significantly across SI, in a manner consistent with a pattern of increased convergence onto the more caudal regions of SI. Overall, the proportions of area 2 units with digital RFs on the tips of interest that were classified as either texture-related (25%) or movement-related (26%) were similar to those reported previously for areas 3b and 1, suggesting that their presumed roles in, respectively, the analysis of surface texture and the representation of the physical parameters of movement are shared and distributed across the three cytoarchitectonic subdivisions of SI under consideration. In addition, the discharge patterns of single texture-related cells in areas 3b, 1 and 2 did not reliably signal whether or not the animal successfully discriminated the surfaces, suggesting that information from a population of cells is required for the performance of the task. Texture-related responses in area 2 were, however, unique in two ways. Firstly, 35% of the texture-related units had additional discharges related to the performance of the scanning movement (texture- and movement-related cells); no such units were found in area 3b, and only one was encountered in area 1.(ABSTRACT TRUNCATED AT 400 WORDS)

Discharge properties of neurones in the hand area of primary somatosensory cortex in monkeys in relation to the performance of an active tactile discrimination task

The present experiments were designed to characterize the discharge patterns of single cortical neurons within the cutaneous representation of the hand in postcentral cortex (areas 3b and 1) in awake monkeys during the performance of an active tactile discrimination task. The task consisted of making a single scanning movement over a surface (first half smooth; second half smooth or rough); the texture encountered over the second half of the surface was indicated by the animal, respectively, pushing or pulling a lever. Unitary discharge was recorded from 118 cells receiving input from the hand or distal forearm of two monkeys. Units with cutaneous fields on the digit tips in contact with the surfaces to be discriminated showed an increase in discharge (58%), a decrease in discharge (11%) or no change (31%) during the task. Units with cutaneous fields not in contact with the discriminanda were much more likely to show decreased discharge during the task (25%), suggesting that there is some selection of cutaneous inputs in this task. Cutaneous units in areas 3b and 1 were equally likely to signal differences in texture (respectively, 18% and 26% of those with digital receptive fields (RFs] and most of the texture-related units (78%) had a large RF, spanning several digits. The discharge patterns of single texture-related cells did not reliably signal whether or not the animal successfully discriminated the surfaces: unitary responses were occasionally absent even though the animal correctly identified the surface or they were present when an incorrect response was made. This observation suggested that information derived from a population of cells is required for the performance of the task, since no single cell's discharge contained sufficient information upon which the animal could base its behavioural response. A group of cells with digital RFs (24% of area 3b cells and 15% of area 1 units) were classified as movement-related. Their discharge signalled precisely the onset and/or end of movement, and they were generally insensitive to the texture of the surfaces scanned. Such cells may serve as an independent source of information for primary somatosensory cortex related to the physical parameters of movement. Most cells with digital RFs were more responsive during active tactile discrimination than during passive movement of the digits over the surfaces (monkey no longer required to discriminate the surface texture). For area 3b units, peripheral factors (RF orientation, speed of movement) were likely responsible for this observation.(ABSTRACT TRUNCATED AT 400 WORDS)