Rapid learning and unlearning of predicted sensory delays in self-generated touch.
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ABSTRACT:
SUBMITTER: Kilteni K
PROVIDER: S-EPMC6860990 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Pressure-sensitive touch panels can measure pressure and location (3D) information simultaneously and provide an intuitive and natural method for expressing one's intention with a higher level of controllability and interactivity. However, they have been generally realized by a simple combination of pressure and location sensor or a stylus-based interface, which limit their implementation in a wide spectrum of applications. Here, we report a first demonstration (to our knowledge) of a transparent and flexible 3D touch which can sense the 3D information in a single device with the assistance of functionally designed self-generated multiscale structures. The single 3D touch system is demonstrated to draw a complex three-dimensional structure by utilizing the pressure as a third coordinate. Furthermore, rigorous theoretical analysis is carried out to achieve the target pressure performances with successful 3D data acquisition in wireless and wearable conditions, which in turn, paves the way for future wearable devices.
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Project description:The nervous systems of diverse species, including worms and humans, possess mechanisms for distinguishing between sensations arising from self-generated (i.e., expected) movements from those arising from other-generated (i.e., unexpected) movements [1-3]. To make this critical distinction, animals generate copies, or corollary discharges, of motor commands [4, 5]. Corollary discharge facilitates the selective gating of reafferent signals arising from self-generated movements, thereby enhancing detection of novel stimuli [6-10]. However, for a developing nervous system, such sensory gating would be counterproductive if it impedes transmission of the very activity upon which activity-dependent mechanisms depend [11]. In infant rats during active (or REM) sleep--a behavioral state that predominates in early infancy [12-16]--neural circuits within the brainstem [17, 18] trigger hundreds of thousands of myoclonic twitches each day [19]. The putative contribution of these self-generated movements to the activity-dependent development of the sensorimotor system is supported by the observation that reafference from twitching limbs reliably and substantially triggers brain activity [20-23]. In contrast, under identical testing conditions, even the most vigorous wake movements reliably fail to trigger reafferent brain activity [21-23]. One hypothesis that accounts for this paradox is that twitches, uniquely among self-generated movements, lack corollary discharge [23]. Here, we test this hypothesis in newborn rats by manipulating the degree to which self-generated movements are expected and, therefore, their presumed recruitment of corollary discharge. We show that twitches, although self-generated, are processed as if they are unexpected.
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Project description:Self-generated touch feels less intense than external touch of the same intensity. According to theory, this is because the brain predicts and attenuates the somatosensory consequences of our movements using a copy of the motor command, i.e., the efference copy. However, whether the efference copy is necessary for this somatosensory attenuation is unclear. Alternatively, a predictable contact of two body parts could be sufficient. Here we quantified the attenuation of touch applied on the participants' left index finger when the touch was triggered by the active or passive movement of the right index finger and when it was externally generated. We observed attenuation only when the touch was triggered by the participants' active movement. In contrast, during the passive movement, the touch was perceived to be as strong as when the touch was externally triggered. Our results suggest that the efference copy is necessary for the attenuation of self-generated touch.
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Project description:Since the early 1970s, numerous behavioral studies have shown that self-generated touch feels less intense and less ticklish than the same touch applied externally. Computational motor control theories have suggested that cerebellar internal models predict the somatosensory consequences of our movements and that these predictions attenuate the perception of the actual touch. Despite this influential theoretical framework, little is known about the neural basis of this predictive attenuation. This is due to the limited number of neuroimaging studies, the presence of conflicting results about the role and the location of cerebellar activity, and the lack of behavioral measures accompanying the neural findings. Here, we combined psychophysics with fMRI to detect the neural processes underlying somatosensory attenuation in male and female healthy human participants. Activity in bilateral secondary somatosensory areas was attenuated when the touch was presented during a self-generated movement (self-generated touch) than in the absence of movement (external touch). An additional attenuation effect was observed in the cerebellum that is ipsilateral to the passive limb receiving the touch. Importantly, we further found that the degree of functional connectivity between the ipsilateral cerebellum and the contralateral primary and bilateral secondary somatosensory areas was linearly and positively related to the degree of behaviorally assessed attenuation; that is, the more participants perceptually attenuated their self-generated touches, the stronger this corticocerebellar coupling. Collectively, these results suggest that the ipsilateral cerebellum is fundamental in predicting self-generated touch and that this structure implements somatosensory attenuation via its functional connectivity with somatosensory areas.SIGNIFICANCE STATEMENT When we touch our hand with the other, the resulting sensation feels less intense than when another person or a machine touches our hand with the same intensity. Early computational motor control theories have proposed that the cerebellum predicts and cancels the sensory consequences of our movements; however, the neural correlates of this cancelation remain unknown. By means of fMRI, we show that the more participants attenuate the perception of their self-generated touch, the stronger the functional connectivity between the cerebellum and the somatosensory cortical areas. This provides conclusive evidence about the role of the cerebellum in predicting the sensory feedback of our movements and in attenuating the associated percepts via its connections to early somatosensory areas.
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Project description:Despite the fact that any successful achievement of willed actions necessarily entails the sense of body ownership (the feeling of owning the moving body parts), it is still unclear how this happens. To address this issue at both behavioral and neural levels, we capitalized on sensory attenuation (SA) phenomenon (a self-generated stimulus is perceived as less intense than an identical externally generated stimulus). We compared the intensity of somatosensory stimuli produced by one's own intended movements and by movements of an embodied fake hand. Then, we investigated if in these two conditions SA was equally affected by interfering with the activity of the supplementary motor area (SMA; known to be related to motor intention and SA) using single-pulse transcranial magnetic stimulation. We showed that ownership of the fake hand triggered attenuation of somatosensory stimuli generated by its movements that were comparable to the attenuation of self-generated stimuli. Furthermore, disrupting the SMA eliminated the SA effect regardless of whether it was triggered by actual participant's movements or by illusory ownership. Our findings suggest that SA triggered by body ownership relies, at least in part, on the activation of the same brain structures as SA triggered by motor-related signals.
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Project description:The brain predicts the sensory consequences of our movements and uses these predictions to attenuate the perception of self-generated sensations. Accordingly, self-generated touch feels weaker than an externally generated touch of identical intensity. In schizophrenia, this somatosensory attenuation is substantially reduced, suggesting that patients with positive symptoms fail to accurately predict and process self-generated touch. If an impaired prediction underlies the positive symptoms of schizophrenia, then a similar impairment should exist in healthy nonclinical individuals with high positive schizotypal traits. One hundred healthy participants (53 female), assessed for schizotypal traits, underwent a well-established psychophysics force discrimination task to quantify how they perceived self-generated and externally generated touch. The perceived intensity of tactile stimuli delivered to their left index finger (magnitude) and the ability to discriminate the stimuli (precision) was measured. We observed that higher positive schizotypal traits were associated with reduced somatosensory attenuation and poorer somatosensory precision of self-generated touch, both when treating schizotypy as a continuous or categorical variable. These effects were specific to positive schizotypy and were not observed for the negative or disorganized dimensions of schizotypy. The results suggest that positive schizotypal traits are associated with a reduced ability to predict and process self-generated touch. Given that the positive dimension of schizotypy represents the analogue of positive psychotic symptoms of schizophrenia, deficits in processing self-generated tactile information could indicate increased liability to schizophrenia.
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Project description:Cortical development is an activity-dependent process [1-3]. Regarding the role of activity in the developing somatosensory cortex, one persistent debate concerns the importance of sensory feedback from self-generated movements. Specifically, recent studies claim that cortical activity is generated intrinsically, independent of movement [3, 4]. However, other studies claim that behavioral state moderates the relationship between movement and cortical activity [5-7]. Thus, perhaps inattention to behavioral state leads to failures to detect movement-driven activity [8]. Here, we resolve this issue by associating local field activity (i.e., spindle bursts) and unit activity in the barrel cortex of 5-day-old rats with whisker movements during wake and myoclonic twitches of the whiskers during active (REM) sleep. Barrel activity increased significantly within 500 ms of whisker movements, especially after twitches. Also, higher-amplitude movements were more likely to trigger barrel activity; when we controlled for movement amplitude, barrel activity was again greater after a twitch than a wake movement. We then inverted the analysis to assess the likelihood that increases in barrel activity were preceded within 500 ms by whisker movements: at least 55% of barrel activity was attributable to sensory feedback from whisker movements. Finally, when periods with and without movement were compared, 70%-75% of barrel activity was movement related. These results confirm the importance of sensory feedback from movements in driving activity in sensorimotor cortex and underscore the necessity of monitoring sleep-wake states to ensure accurate assessments of the contributions of the sensory periphery to activity in developing somatosensory cortex.
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Project description:Dominant motor control theories propose that the brain predicts and attenuates the somatosensory consequences of actions, referred to as somatosensory attenuation. Support comes from psychophysical and neuroimaging studies showing that touch applied on a passive hand elicits attenuated perceptual and neural responses if it is actively generated by one's other hand, compared to an identical touch from an external origin. However, recent experimental findings have challenged this view by providing psychophysical evidence that the perceived intensity of touch on the passive hand is enhanced if the active hand does not receive touch simultaneously with the passive hand (somatosensory enhancement) and by further attributing attenuation to the double tactile stimulation of the hands upon contact. Here, we directly contrasted the hypotheses of the attenuation and enhancement models regarding how action influences somatosensory perception by manipulating whether the active hand contacts the passive hand. We further assessed somatosensory perception in the absence of any predictive cues in a condition that turned out to be essential for interpreting the experimental findings. In three pre-registered experiments, we demonstrate that action does not enhance the predicted touch (Experiment 1), that the previously reported 'enhancement' effects are driven by the reference condition used (Experiment 2), and that self-generated touch is robustly attenuated regardless of whether the two hands make contact (Experiment 3). Our results provide conclusive evidence that action does not enhance but attenuates predicted touch and prompt a reappraisal of recent experimental findings upon which theoretical frameworks proposing a perceptual enhancement by action prediction are based.
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Project description:Increasingly large MRI neuroimaging datasets are becoming available, including many highly multi-site multi-scanner datasets. Combining the data from the different scanners is vital for increased statistical power; however, this leads to an increase in variance due to nonbiological factors such as the differences in acquisition protocols and hardware, which can mask signals of interest. We propose a deep learning based training scheme, inspired by domain adaptation techniques, which uses an iterative update approach to aim to create scanner-invariant features while simultaneously maintaining performance on the main task of interest, thus reducing the influence of scanner on network predictions. We demonstrate the framework for regression, classification and segmentation tasks with two different network architectures. We show that not only can the framework harmonise many-site datasets but it can also adapt to many data scenarios, including biased datasets and limited training labels. Finally, we show that the framework can be extended for the removal of other known confounds in addition to scanner. The overall framework is therefore flexible and should be applicable to a wide range of neuroimaging studies.
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Project description:BackgroundA 'continuum of psychosis' refers to the concept that psychotic-like experiences occur to certain extents in the healthy population and to more severe extents in individuals with psychotic disorders. If this concept is valid, neurophysiological abnormalities exhibited by patients with schizophrenia should also be present, to some degree, in non-clinical individuals who score highly on the personality dimension of schizotypy. Patients with schizophrenia have consistently been shown to exhibit electrophysiological suppression abnormalities to self-generated speech. The present study aimed to investigate whether these electrophysiological suppression abnormalities were also present in non-clinical individuals who scored highly on schizotypy.MethodsThirty-seven non-clinical individuals scoring High (above median) and 37 individuals scoring Low (below median) on the Schizotypal Personality Questionnaire (SPQ; a commonly used schizotypy scale) underwent electroencephalographic (EEG) recording. The amplitude of the N1 component of the auditory-evoked potential was measured while participants (a) vocalized simple syllables (Talk condition), (b) passively listened to a recording of these vocalizations (Listen condition) and (c) listened to a recording of the vocalizations while simultaneously watching a video depicting the sound-wave of the forthcoming vocalizations, allowing them to be temporally predicted (Cued Listen condition).ResultsThe Low Schizotypy group exhibited significantly reduced N1-amplitude in the Talk condition relative to both the Listen and Cued Listen conditions; that is, they exhibited significant N1-suppression. The High Schizotypy group exhibited significantly lower levels of N1-suppression compared to the Low Schizotypy group. Furthermore, while the Cued Listen condition induced significantly lower N1-amplitudes compared to the Listen condition in the Low Schizotypy group, this was not the case for the High Schizotypy group.ConclusionsThe results suggest that non-clinical, highly schizotypal individuals exhibit subnormal levels of N1-suppression to self-generated speech, similar to the N1-suppression abnormalities which have previously been reported in patients with schizophrenia. This finding provides empirical support for the existence of a neurophysiological 'continuum of psychosis'.
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