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Gilles de la Tourette syndrome (GTS) is a disorder characterised by motor and vocal tics, which may represent habitual actions as a result of enhanced learning of associations between stimuli and responses (S-R). In this study, we investigated how adults with GTS and healthy controls (HC) learn two types of regularities in a sequence: statistics (non-adjacent probabilities) and rules (predefined order). Participants completed a visuomotor sequence learning task while EEG was recorded. To understand the neurophysiological underpinnings of these regularities in GTS, multivariate pattern analyses on the temporally decomposed EEG signal as well as sLORETA source localisation method were conducted. We found that people with GTS showed superior statistical learning but comparable rule-based learning compared to HC participants. Adults with GTS had different neural representations for both statistics and rules than HC adults; specifically, adults with GTS maintained the regularity representations longer and had more overlap between them than HCs. Moreover, over different time scales, distinct fronto-parietal structures contribute to statistical learning in the GTS and HC groups. We propose that hyper-learning in GTS is a consequence of the altered sensitivity to encode complex statistics, which might lead to habitual actions.
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Eletroencefalografia , Síndrome de Tourette , Humanos , Síndrome de Tourette/fisiopatologia , Masculino , Adulto , Feminino , Adulto Jovem , Aprendizagem/fisiologia , Desempenho Psicomotor/fisiologia , Pessoa de Meia-Idade , Aprendizagem por ProbabilidadeRESUMO
Gilles de la Tourette syndrome is a neurodevelopmental disorder characterized by motor and vocal tics. It is associated with enhanced processing of stimulus-response associations, including a higher propensity to learn probabilistic stimulus-response contingencies (i.e. statistical learning), the nature of which is still elusive. In this study, we investigated the hypothesis that resting-state theta network organization is a key for the understanding of superior statistical learning in these patients. We investigated the graph-theoretical network architecture of theta oscillations in adult patients with Gilles de la Tourette syndrome and healthy controls during a statistical learning task and in resting states both before and after learning. We found that patients with Gilles de la Tourette syndrome showed a higher statistical learning score than healthy controls, as well as a more optimal (small-world-like) theta network before the task. Thus, patients with Gilles de la Tourette syndrome had a superior facility to integrate and evaluate novel information as a trait-like characteristic. Additionally, the theta network architecture in Gilles de la Tourette syndrome adapted more to the statistical information during the task than in HC. We suggest that hyper-learning in patients with Gilles de la Tourette syndrome is likely a consequence of increased sensitivity to perceive and integrate sensorimotor information leveraged through theta oscillation-based resting-state dynamics. The study delineates the neural basis of a higher propensity in patients with Gilles de la Tourette syndrome to pick up statistical contingencies in their environment. Moreover, the study emphasizes pathophysiologically endowed abilities in patients with Gilles de la Tourette syndrome, which are often not taken into account in the perception of this common disorder but could play an important role in destigmatization.
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Characterizing ontogenetic changes across the lifespan is a crucial tool in understanding neurocognitive functions. While age-related changes in learning and memory functions have been extensively characterized in the past decades, the lifespan trajectory of memory consolidation, a critical function that supports the stabilization and long-term retention of memories, is still poorly understood. Here we focus on this fundamental cognitive function and probe the consolidation of procedural memories that underlie cognitive, motor, and social skills and automatic behaviors. We used a lifespan approach: 255 participants aged between 7 and 76 years performed a well-established procedural memory task in the same experimental design across the whole sample. This task enabled us to disentangle two critical processes in the procedural domain: statistical learning and general skill learning. The former is the ability to extract and learn predictable patterns of the environment, while the latter captures a general speed-up as learning progresses due to improved visuomotor coordination and other cognitive processes, independent of acquisition of the predictable patterns. To measure the consolidation of statistical and general skill knowledge, the task was administered in two sessions with a 24-h delay between them. Here, we report successful retention of statistical knowledge with no differences across age groups. For general skill knowledge, offline improvement was observed over the delay period, and the degree of this improvement was also comparable across the age groups. Overall, our findings reveal age invariance in these two key aspects of procedural memory consolidation across the human lifespan.
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Gilles de la Tourette syndrome (GTS) is a neuropsychiatric disorder. Because motor signs are the defining feature of GTS, addressing the neurophysiology of motor processes is central to understanding GTS. The integration of voluntary motor processes is subject to so-called "binding problems", i.e., how different aspects of an action are integrated. This was conceptualized in the theory of event coding, in which 'action files' accomplish the integration of motor features. We examined the functional neuroanatomical architecture of EEG theta band activity related to action file processing in GTS patients and healthy controls. Whereas, in keeping with previous data, behavioral performance during action file processing did not differ between GTS and controls, underlying patterns of neural activity were profoundly different. Superior parietal regions (BA7) were predominantly engaged in healthy controls, but superior frontal regions (BA9, BA10) in GTS indicated that the processing of different motor feature codes was central for action file processing in healthy controls, whereas episodic processing was more relevant in GTS. The data suggests a cascade of cognitive branching in fronto-polar areas followed by episodic processing in superior frontal regions in GTS. Patients with GTS accomplish the integration of motor plans via qualitatively different neurophysiological processes.
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Predictions supporting risky decisions could become unreliable when outcome probabilities temporarily change, making adaptation more challenging. Therefore, this study investigated whether sensitivity to the temporal structure in outcome probabilities can develop and remain persistent in a changing decision environment. In a variant of the Balloon Analogue Risk Task with 90 balloons, outcomes (rewards or balloon bursts) were predictable in the task's first and final 30 balloons and unpredictable in the middle 30 balloons. The temporal regularity underlying the predictable outcomes differed across three experimental conditions. In the deterministic condition, a repeating three-element sequence dictated the maximum number of pumps before a balloon burst. In the probabilistic condition, a single probabilistic regularity ensured that burst probability increased as a function of pumps. In the hybrid condition, a repeating sequence of three different probabilistic regularities increased burst probabilities. In every condition, the regularity was absent in the middle 30 balloons. Participants were not informed about the presence or absence of the regularity. Sensitivity to both the deterministic and hybrid regularities emerged and influenced risk taking. Unpredictable outcomes of the middle phase did not deteriorate this sensitivity. In conclusion, humans can adapt their risky choices in a changing decision environment by exploiting the statistical structure that controls how the environment changes.
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Tomada de Decisões , Recompensa , Humanos , Probabilidade , Assunção de RiscosRESUMO
Tourette's syndrome (TS) is a neurodevelopmental disorder characterized by repetitive movements and vocalizations, also known as tics. The phenomenology of tics and the underlying neurobiology of the disorder have suggested that the altered functioning of the procedural memory system might contribute to its etiology. However, contrary to the robust findings of impaired procedural memory in neurodevelopmental disorders of language, results from TS have been somewhat mixed. We review the previous studies in the field and note that they have reported normal, impaired, and even enhanced procedural performance. These mixed findings may be at least partially be explained by the diversity of the samples in both age and tic severity, the vast array of tasks used, the low sample sizes, and the possible confounding effects of other cognitive functions, such as executive functions, working memory or attention. However, we propose that another often overlooked factor could also contribute to the mixed findings, namely the multiprocess nature of the procedural system itself. We propose that a process-oriented view of procedural memory functions could serve as a theoretical framework to help integrate these varied findings. We discuss evidence suggesting heterogeneity in the neural regions and their functional contributions to procedural memory. Our process-oriented framework can help to deepen our understanding of the complex profile of procedural functioning in TS and atypical development in general.
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Tourette syndrome is a common neurodevelopmental disorder defined by multiple motor and phonic tics. Tics in Tourette syndrome resemble spontaneously occurring movements in healthy controls and are therefore sometimes difficult to distinguish from these. Tics may in fact be mis-interpreted as a meaningful action, i.e. a signal with social content, whereas they lack such information and could be conceived a surplus of action or 'motor noise'. These and other considerations have led to a 'neural noise account' of Tourette syndrome suggesting that the processing of neural noise and adaptation of the signal-to-noise ratio during information processing is relevant for the understanding of Tourette syndrome. So far, there is no direct evidence for this. Here, we tested the 'neural noise account' examining 1/f noise, also called scale-free neural activity as well as aperiodic activity, in n = 74 children, adolescents and adults with Tourette syndrome and n = 74 healthy controls during task performance using EEG data recorded during a sensorimotor integration task. In keeping with results of a previous study in adults with Tourette syndrome, behavioural data confirmed that sensorimotor integration was also stronger in this larger Tourette syndrome cohort underscoring the relevance of perceptual-action processes in this disorder. More importantly, we show that 1/f noise and aperiodic activity during sensorimotor processing is increased in patients with Tourette syndrome supporting the 'neural noise account'. This implies that asynchronous/aperiodic neural activity during sensorimotor integration is stronger in patients with Tourette syndrome compared to healthy controls, which is probably related to abnormalities of GABAergic and dopaminergic transmission in these patients. Differences in 1/f noise and aperiodic activity between patients with Tourette syndrome and healthy controls were driven by high-frequency oscillations and not lower-frequency activity currently discussed to be important in the pathophysiology of tics. This and the fact that Bayesian statistics showed that there is evidence for the absence of a correlation between neural noise and clinical measures of tics, suggest that increased 1/f noise and aperiodic activity are not directly related to tics but rather represents a novel facet of Tourette syndrome.
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Tourette syndrome is a childhood-onset neurodevelopmental disorder characterized by motor and vocal tics. On the neural level, tics are thought to be related to the disturbances of the cortico-basal ganglia-thalamo-cortical loops, which also play an important role in procedural learning. Several studies have investigated the acquisition of procedural information and the access to established procedural information in TS. Based on these, the notion of procedural hyperfunctioning, i.e., enhanced procedural learning, has been proposed. However, one neglected area is the retention of acquired procedural information, especially following a long-term offline period. Here, we investigated the 5-hour and 1-year consolidation of two aspects of procedural memory, namely serial-order and probability-based information. Nineteen children with TS between the ages of 10 and 15 as well as 19 typically developing gender- and age-matched controls were tested on a visuomotor four-choice reaction time task that enables the simultaneous assessment of the two aspects. They were retested on the same task 5 hours and 1 year later without any practice in the offline periods. Both groups successfully acquired and retained the probability-based information both when tested 5 hours and then 1 year later, with comparable performance between the TS and control groups. Children with TS did not acquire the serial-order information during the learning phase; hence, retention could not be reliably tested. Our study showed evidence for short-term and long-term retention of one aspect of procedural memory, namely probability-based information in TS, whereas learning of serial-order information might be impaired in this disorder.
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Humans differ in their capacity for integrating perceived events and related actions. The "Theory of event coding" (TEC) conceptualizes how stimuli and actions are cognitively bound into a common functional representation (or "code"), known as the "event file". To date, however, the neural processes underlying the development of event file coding mechanisms across age are largely unclear. We investigated age-related neural changes of event file coding from late childhood to early adulthood, using EEG signal decompositions methods. We included a group of healthy participants (n = 91) between 10 and 30 years, performing an event file paradigm. Results of this study revealed age-related effects on event file coding processes both at the behavioural and the neurophysiological level. Performance accuracy data showed that event file unbinding und rebinding processes become more efficient from late childhood to early adulthood. These behavioural effects are reflected by age-related effects in two neurophysiological subprocesses associated with the superior parietal cortex (BA7) as revealed in the analyses using EEG signal decomposition. The first process entails mapping and association processes between stimulus and response; whereas, the second comprises inhibitory control subprocesses subserving the selection of the relevant motor programme amongst competing response options.
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Eletroencefalografia , Percepção , Adolescente , Adulto , Criança , Estudos Transversais , Potenciais Evocados , Feminino , Humanos , Masculino , Lobo Parietal , Adulto JovemRESUMO
Extraction of environmental patterns underlies human learning throughout the lifespan and plays a crucial role not only in cognitive but also perceptual, motor, and social skills. At least two types of regularities contribute to acquiring skills: (1) statistical, probability-based regularities, and (2) serial order-based regularities. Memory performance of probability-based and/or serial order-based regularities over short periods (from minutes to weeks) has been widely investigated across the lifespan. However, long-term (months or year-long) memory performance of such knowledge has received relatively less attention and has not been assessed in children yet. Here, we aimed to test the long-term memory performance of probability-based and serial order-based regularities over a 1-year offline period in neurotypical children between the age of 9 and 15. Participants performed a visuomotor four-choice reaction time task designed to measure the acquisition of probability-based and serial order-based regularities simultaneously. Short-term consolidation effects were controlled by retesting their performance after a 5-h delay. They were then retested on the same task 1 year later without any practice between the sessions. Participants successfully acquired both probability-based and serial order-based regularities and retained both types of knowledge over the 1-year period. The successful retention was independent of age. Our study demonstrates that the representation of probability-based and serial order-based regularities remains stable over a long period of time. These findings offer indirect evidence for the developmental invariance model of skill consolidation.
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Desenvolvimento do Adolescente/fisiologia , Desenvolvimento Infantil/fisiologia , Aprendizagem/fisiologia , Memória de Longo Prazo/fisiologia , Adolescente , Atenção/fisiologia , Criança , Feminino , Humanos , Masculino , Destreza Motora/fisiologia , Tempo de Reação/fisiologiaRESUMO
Acute stress can crucially influence learning and memory processes. One of the key processes underlying human learning and memory is the ability of our brain to rapidly detect and extract regularities from sensory input across time and space leading to effective predictive processing. Here, we aimed to get an in-depth look into the effect of stress on the acquisition of two aspects of regularity extraction. We examined whether and how stress affects the learning (1) of probability-based regularities and (2) of serial order-based regularities in the same experimental design, and (3) the explicit access to the acquired information. Considering that the acquisition of probability-based regularities is a relatively rapid process, we primarily focused on the early phase of the task. We induced stress with the Socially Evaluated Cold Pressor Test in 27 young adults, while 26 participants were enrolled in the control group. Salivary cortisol levels and subjective ratings of affective states showed successful stress induction. After the stress induction, we measured regularity extraction with the cued Alternating Serial Reaction Time task. We found that stress promoted the extraction of probability-based regularities measured by the learning performance in the early phase of the task and did not alter the learning of serial order-based regularities. Post-block reports showed weaker explicit access to the serial order-based regularities in the stress group. Our results can contribute to a process-level understanding on how stress alters learning and memory functions related to predictive processes.
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Hidrocortisona/análise , Estresse Psicológico/psicologia , Estudantes/psicologia , Feminino , Humanos , Masculino , Memória , Saliva/química , Aprendizagem Seriada , Estresse Psicológico/metabolismo , Adulto JovemRESUMO
Both primarily and recently encountered information have been shown to influence experience-based risky decision making. The primacy effect predicts that initial experience will influence later choices even if outcome probabilities change and reward is ultimately more or less sparse than primarily experienced. However, it has not been investigated whether extended initial experience would induce a more profound primacy effect upon risky choices than brief experience. Therefore, the present study tested in two experiments whether young adults adjusted their risk-taking behavior in the Balloon Analogue Risk Task after an unsignaled and unexpected change point. The change point separated early "good luck" or "bad luck" trials from subsequent ones. While mostly positive (more reward) or mostly negative (no reward) events characterized the early trials, subsequent trials were unbiased. In Experiment 1, the change point occurred after one-sixth or one-third of the trials (brief vs. extended experience) without intermittence, whereas in Experiment 2, it occurred between separate task phases. In Experiment 1, if negative events characterized the early trials, after the change point, risk-taking behavior increased as compared with the early trials. Conversely, if positive events characterized the early trials, risk-taking behavior decreased after the change point. Although the adjustment of risk-taking behavior occurred due to integrating recent experiences, the impact of initial experience was simultaneously observed. The length of initial experience did not reliably influence the adjustment of behavior. In Experiment 2, participants became more prone to take risks as the task progressed, indicating that the impact of initial experience could be overcome. Altogether, we suggest that initial beliefs about outcome probabilities can be updated by recent experiences to adapt to the continuously changing decision environment.
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Tourette syndrome (TS) is a childhood-onset neurodevelopmental disorder that primarily affects the cortico-basal ganglia-thalamo-cortical (CBGTC) circuitry and is characterized by motor and vocal tics. Previous studies have found enhancement in procedural memory, which depends on the CBGTC circuitry and plays an important role in the learning and processing of numerous motor, social, and cognitive skills and habits. Based on these studies, procedural hyperfunctioning in TS has been proposed. However, the neurocognitive mechanism underlying such hyperfunctioning is poorly understood. Here, we investigated how two aspects of procedural learning, namely 1) frequency-based statistical learning and 2) order-based sequence learning, are affected in TS. Twenty-one children with TS between the ages of ten and fifteen as well as 21 typically developing controls were tested on a probabilistic sequence learning task that enables the parallel assessment of these two aspects. We found that children with TS showed enhanced sensitivity to statistical information but impaired sequence learning compared to typically developing children. The deconstruction of procedural memory suggests that procedural hyperfunctioning in TS may be supported by enhanced sensitivity to statistical information. These results can provide a potential path for improving therapy methods and skill-oriented educational programs for TS.
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Síndrome de Tourette , Gânglios da Base , Criança , Humanos , AprendizagemRESUMO
Performing a goal-directed movement consists of a chain of complex preparatory mechanisms. Such planning especially requires integration (or binding) of various action features, a process that has been conceptualized in the "theory of event coding." Theoretical considerations and empirical research suggest that these processes are subject to developmental effects from adolescence to adulthood. The aim of the present study was to investigate age-related modulations in action feature binding processes and to shed light on underlying neurophysiological development from preadolescence to early adulthood. We examined a group of healthy participants (n = 61) between 10 and 30 yr of age, who performed a task that requires a series of bimanual response selections in an embedded paradigm. For an in-depth analysis of the underlying neural correlates, we applied EEG signal decomposition together with source localization analyses. Behavioral results across the whole group did not show binding effects in reaction times but in intraindividual response variability. From age 10 to 30 yr, there was a decrease in reaction times and reaction time variability but no age-related effect in action file binding. The latter were corroborated by Bayesian data analyses. On the brain level, the developmental effects on response selection were associated with activation modulations in the superior parietal cortex (BA7). The results show that mechanisms of action execution and speed, but not those of action feature binding, are subject to age-related changes between the age of 10 and 30 yr.NEW & NOTEWORTHY Different aspects of an action need to be integrated to allow smooth unfolding of behavior. We examine developmental effects in these processes and show that mechanisms of action execution and speed, but not those of action feature binding, are subject to age-related changes between the age of 10 and 30 yr.
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Desenvolvimento Humano/fisiologia , Atividade Motora/fisiologia , Lobo Parietal/fisiologia , Desempenho Psicomotor/fisiologia , Tempo de Reação/fisiologia , Adolescente , Adulto , Fatores Etários , Criança , Eletroencefalografia , Feminino , Humanos , Masculino , Adulto JovemRESUMO
Tourette syndrome is a neurodevelopmental disorder that is characterized by motor and vocal tics and by alterations in the cortico-basal ganglia-thalamo-cortical (CBGTC) circuitry. The CBGTC circuitry plays an important role in procedural learning, in the acquisition of skills and habits. Tics and habits are similar phenomenologically since tics can be described as overlearned habits. Based on these characteristics, prior studies proposed enhanced pro - ce dural learning, i.e., procedural hyperfunctioning in Tourette syndrome. A growing body of evidence supports this notion. The focus of the present review article is to discuss procedural hyperfunctioning in Tourette syndrome. We aim to shed light on a cognitive advantage in Tourette syndrome and to draw attention to the notion that pathologies and developmental disorder can be characterized not only with impairments and cognitive dysfunctions but with enhanced functions as well.
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Cognição/fisiologia , Aprendizagem/fisiologia , Vias Neurais , Síndrome de Tourette/psicologia , HumanosRESUMO
Background and aims Television series watching stepped into a new golden age with the appearance of online series. Being highly involved in series could potentially lead to negative outcomes, but the distinction between highly engaged and problematic viewers should be distinguished. As no appropriate measure is available for identifying such differences, a short and valid measure was constructed in a multistudy investigation: the Series Watching Engagement Scale (SWES). Methods In Study 1 (NSample1 = 740 and NSample2 = 740), exploratory structural equation modeling and confirmatory factor analysis were used to identify the most important facets of series watching engagement. In Study 2 (N = 944), measurement invariance of the SWES was investigated between males and females. In Study 3 (N = 1,520), latent profile analysis (LPA) was conducted to identify subgroups of viewers. Results Five factors of engagement were identified in Study 1 that are of major relevance: persistence, identification, social interaction, overuse, and self-development. Study 2 supported the high levels of equivalence between males and females. In Study 3, three groups of viewers (low-, medium-, and high-engagement viewers) were identified. The highly engaged at-risk group can be differentiated from the other two along key variables of watching time and personality. Discussion The present findings support the overall validity, reliability, and usefulness of the SWES and the results of the LPA showed that it might be useful to identify at-risk viewers before the development of problematic use.