Finding Pattern in the Noise: Persistent Implicit Statistical Knowledge Impacts the Processing of Unpredictable Stimuli.

Humans can extract statistical regularities of the environment to predict upcoming events. Previous research recognized that implicitly acquired statistical knowledge remained persistent and continued to influence behavior even when the regularities were no longer present in the environment. Here, in an fMRI experiment, we investigated how the persistence of statistical knowledge is represented in the brain. Participants (n = 32) completed a visual, four-choice, RT task consisting of statistical regularities. Two types of blocks constantly alternated with one another throughout the task: predictable statistical regularities in one block type and unpredictable ones in the other. Participants were unaware of the statistical regularities and their changing distribution across the blocks. Yet, they acquired the statistical regularities and showed significant statistical knowledge at the behavioral level not only in the predictable blocks but also in the unpredictable ones, albeit to a smaller extent. Brain activity in a range of cortical and subcortical areas, including early visual cortex, the insula, the right inferior frontal gyrus, and the right globus pallidus/putamen contributed to the acquisition of statistical regularities. The right insula, inferior frontal gyrus, and hippocampus as well as the bilateral angular gyrus seemed to play a role in maintaining this statistical knowledge. The results altogether suggest that statistical knowledge could be exploited in a relevant, predictable context as well as transmitted to and retrieved in an irrelevant context without a predictable structure.

Deterministic and probabilistic regularities underlying risky choices are acquired in a changing decision context.

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.

Adaptation to recent outcomes attenuates the lasting effect of initial experience on risky decisions.

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.

Neurophysiological and functional neuroanatomical coding of statistical and deterministic rule information during sequence learning.

Humans are capable of acquiring multiple types of information presented in the same information stream. It has been suggested that at least two parallel learning processes are important during learning of sequential patterns-statistical learning and rule-based learning. Yet, the neurophysiological underpinnings of these parallel learning processes are not fully understood. To differentiate between the simultaneous mechanisms at the single trial level, we apply a temporal EEG signal decomposition approach together with sLORETA source localization method to delineate whether distinct statistical and rule-based learning codes can be distinguished in EEG data and can be related to distinct functional neuroanatomical structures. We demonstrate that concomitant but distinct aspects of information coded in the N2 time window play a role in these mechanisms: mismatch detection and response control underlie statistical learning and rule-based learning, respectively, albeit with different levels of time-sensitivity. Moreover, the effects of the two learning mechanisms in the different temporally decomposed clusters of neural activity also differed from each other in neural sources. Importantly, the right inferior frontal cortex (BA44) was specifically implicated in visuomotor statistical learning, confirming its role in the acquisition of transitional probabilities. In contrast, visuomotor rule-based learning was associated with the prefrontal gyrus (BA6). The results show how simultaneous learning mechanisms operate at the neurophysiological level and are orchestrated by distinct prefrontal cortical areas. The current findings deepen our understanding on the mechanisms of how humans are capable of learning multiple types of information from the same stimulus stream in a parallel fashion.

Dissociation between two aspects of procedural learning in Tourette syndrome: Enhanced statistical and impaired sequence learning.

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.

Implicit anticipation of probabilistic regularities: Larger CNV emerges for unpredictable events.

Anticipation of upcoming events plays a crucial role in automatic behaviors. It is, however, still unclear whether the event-related brain potential (ERP) markers of anticipation could track the implicit acquisition of probabilistic regularities that can be considered as building blocks of automatic behaviors. Therefore, in a four-choice reaction time (RT) task performed by young adults (N = 36), the contingent negative variation (CNV) as an ERP marker of anticipation was measured from the onset of a cue stimulus until the presentation of a target stimulus. Due to the probability structure of the task, target stimuli were either predictable or unpredictable, but this was unknown to participants. The cue did not contain predictive information on the upcoming target. Results showed that the CNV amplitude during response preparation was larger before the unpredictable than before the predictable target stimuli. In addition, although RTs increased, the P3 amplitude decreased for the unpredictable as compared with the predictable target stimuli, possibly due to the stronger response preparation that preceded stimulus presentation. These results suggest that enhanced attentional resources are allocated to the implicit anticipation and processing of unpredictable events. This might originate from the formation of internal models on the probabilistic regularities of the stimulus stream, which primarily facilitates the processing of predictable events. Overall, we provide ERP evidence that supports the role of implicit anticipation and predictive processes in the acquisition of probabilistic regularities.

Accurate response selection and inhibition in healthy aging: An event-related potential study.

Inhibitory control is thought to be critical for appropriate response selection in an ever-changing environment and to decline with age. However, experimental paradigms (e.g., go/no-go) confound stimulus frequency with demands to respond or inhibit responding. The present study eliminated that confound by using a modified go/no-go task controlling for stimulus frequency differences (using frequent-go, infrequent-go, and infrequent no-go types of stimuli) in healthy older and young adults. Event-related potential (ERP) components related to detection of response conflict (N2) and response evaluation (P3) were also examined. Behaviorally, older and young adults were sensitive to stimulus frequencies indicated by significant slowing for the infrequent-go compared with the frequent-go stimuli observed in both groups. Furthermore, older adults were characterized by reduced commission errors and overall slowing, suggesting that they could take advantage of their slower performance. Increase of N2 amplitude was evident for correctly inhibited no-go stimuli in both groups. In contrast, no-go stimulus-related increase in P3 amplitude could be observed only in the young. Stimulus frequency-related ERP amplitude differences were not significant either in the young or in the older adults. These results suggest preserved behavioral control over inappropriate responses in older adults and indicate that efficient response inhibition is related to compensatory mechanisms. The age-related decrease in the P3 amplitude suggests that the evaluation of response inhibition (a) could be independent of the detection of response conflict and (b) supports the notion of strategic differences in performance with age. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Perceiving structure in unstructured stimuli: Implicitly acquired prior knowledge impacts the processing of unpredictable transitional probabilities.

It is unclear how implicit prior knowledge is involved and remains persistent in the extraction of the statistical structure underlying sensory input. Therefore, this study investigated whether the implicit knowledge of second-order transitional probabilities characterizing a stream of visual stimuli impacts the processing of unpredictable transitional probabilities embedded in a similar input stream. Young adults (N = 50) performed a four-choice reaction time (RT) task that consisted of structured and unstructured blocks. In the structured blocks, more probable and less probable short-range nonadjacent transitional probabilities were present. In the unstructured blocks, the unique combinations of the short-range transitional probabilities occurred with equal probability; therefore, they were unpredictable. All task blocks were visually identical at the surface level. While one-half of the participants completed the structured blocks first followed by the unstructured blocks, this was reversed in the other half of them. The change in the structure was not explicitly denoted, and no feedback was provided on the correctness of each response. Participants completing the structured blocks first showed faster RTs to more probable than to less probable short-range transitional probabilities in both the structured and unstructured blocks, indicating the persistent effect of prior knowledge. However, after extended exposure to the unstructured blocks, they updated this prior knowledge. Participants completing the unstructured blocks first showed the RT difference only in the structured blocks, which was not constrained by the preceding exposure to unpredictable stimuli. The results altogether suggest that implicitly acquired prior knowledge of predictable stimuli influences the processing of subsequent unpredictable stimuli. Updating this prior knowledge seems to require a longer stretch of time than its initial acquisition.

Expectations about word stress modulate neural activity in speech-sensitive cortical areas.

A recent dual-stream model of language processing proposed that the postero-dorsal stream performs predictive sequential processing of linguistic information via hierarchically organized internal models. However, it remains unexplored whether the prosodic segmentation of linguistic information involves predictive processes. Here, we addressed this question by investigating the processing of word stress, a major component of speech segmentation, using probabilistic repetition suppression (RS) modulation as a marker of predictive processing. In an event-related acoustic fMRI RS paradigm, we presented pairs of pseudowords having the same (Rep) or different (Alt) stress patterns, in blocks with varying Rep and Alt trial probabilities. We found that the BOLD signal was significantly lower for Rep than for Alt trials, indicating RS in the posterior and middle superior temporal gyrus (STG) bilaterally, and in the anterior STG in the left hemisphere. Importantly, the magnitude of RS was modulated by repetition probability in the posterior and middle STG. These results reveal the predictive processing of word stress in the STG areas and raise the possibility that words stress processing is related to the dorsal "where" auditory stream.

Word stress representations are language-specific: Evidence from event-related brain potentials.

Understanding speech at the basic levels entails the simultaneous and independent processing of phonemic and prosodic features. While it is well-established that phoneme perception relies on language-specific long-term traces, it is unclear if the processing of prosodic features similarly involves language-specific representations. In the present study, we investigated the processing of a specific prosodic feature, word stress, using the method of event-related brain potentials (ERPs) employing a cross-linguistic approach. Hungarian participants heard disyllabic pseudowords stressed either on the first (legal stress) or on the second (illegal stress) syllable, pronounced either by a Hungarian or a German speaker. Results obtained using a data-driven ERP analysis methodology showed that all pseudowords in the deviant position elicited an Early Differentiating Negativity and a Mismatch Negativity component, except for the Hungarian pseudowords stressed on the first syllable. This suggests that Hungarian listeners did not process the native legal stress pattern as deviant, but the same stress pattern with a nonnative accent was processed as deviant. This implies that the processing of word stress was based on language-specific long-term memory traces.

Tracking the implicit acquisition of nonadjacent transitional probabilities by ERPs.

The implicit acquisition of complex probabilistic regularities has been found to be crucial in numerous automatized cognitive abilities, including language processing and associative learning. However, it has not been completely elucidated how the implicit extraction of second-order nonadjacent transitional probabilities is reflected by neurophysiological processes. Therefore, this study investigated the sensitivity of event-related brain potentials (ERPs) to these probabilistic regularities embedded in a sequence of visual stimuli without providing explicit information on the structure of the stimulus stream. Healthy young adults (N = 32) performed a four-choice RT task that included a sequential regularity between nonadjacent trials yielding a complex transitional probability structure. ERPs were measured relative to both stimulus and response onset. RTs indicated the rapid acquisition of the sequential regularity and the transitional probabilities. The acquisition process was also tracked by the stimulus-locked and response-locked P3 component: The P3 peak was larger for the sequence than for the random stimuli, while the late P3 was larger for less probable than for more probable short-range relations among the random stimuli. According to the RT and P3 effects, sensitivity to the sequential regularity is assumed to be supported by the initial sensitivity to the transitional probabilities. These results suggest that stimulus-response contingencies on the probabilistic regularities of the ongoing stimulus context are implicitly mapped and constantly revised. Overall, this study (1) highlights the role of predictive processes during implicit memory formation, and (2) delineates a potential to gain further insight into the dynamics of implicit acquisition processes.

A novel virtual plus-maze for studying electrophysiological correlates of spatial reorientation.

Quick reorientation is an essential part of successful navigation. Despite growing attention to this ability, little is known about how reorientation happens in humans. To this aim, we recorded EEG from 34 participants. Participants were navigating a simple virtual reality plus-maze where at the beginning of each trial they were randomly teleported to either the North or the South alley. Results show that the teleportation event caused a quick reorientation effect over occipito-parietal areas as early as 100 ms; meaning that despite the known stochastic nature of the teleportation, participants built up expectations for their place of arrival. This result has important consequences for the optimal design of virtual reality locomotion.

ERP evidence for implicit L2 word stress knowledge in listeners of a fixed-stress language.

Languages with contrastive stress, such as English or German, distinguish some words only via the stress status of their syllables, such as "CONtent" and "conTENT" (capitals indicate a stressed syllable). Listeners with a fixed-stress native language, such as Hungarian, have difficulties in explicitly discriminating variation of the stress position in a second language (L2). However, Event-Related Potentials (ERPs) indicate that Hungarian listeners implicitly notice variation from their native fixed-stress pattern. Here we used ERPs to investigate Hungarian listeners' implicit L2 processing. In a cross-modal word fragment priming experiment, we presented spoken stressed and unstressed German word onsets (primes) followed by printed versions of initially stressed and initially unstressed German words (targets). ERPs reflected stress priming exerted by both prime types. This indicates that Hungarian listeners implicitly linked German words with the stress status of the primes. Thus, the formerly described explicit stress discrimination difficulty associated with a fixed-stress native language does not generalize to implicit aspects of L2 word stress processing.

ERPs differentiate the sensitivity to statistical probabilities and the learning of sequential structures during procedural learning.

Procedural learning facilitates the efficient processing of complex environmental stimuli and contributes to the acquisition of automatic behaviors. Although earlier findings suggest different temporal trajectories of the multiple learning processes within procedural learning, this has not been clarified at the level of neurocognitive correlates. Therefore, we investigated whether two prominent learning processes - statistical learning and sequence learning - can be distinguished using event-related brain potentials (ERPs) within the same experimental setting. Healthy young adults (N = 40) performed the Alternating Serial Reaction Time task while RTs and ERPs were measured time-locked to the onset of the task's stimuli. Both RT and N2 effects reflected the rapid acquisition of statistical probabilities. At the same time, these effects reflected the gradual learning of sequential structures. The amplitude change of the P3 reflected only gradual sequence learning. The P1 component was sensitive to both learning processes, which did not change as the task progressed. Our results altogether indicate that statistical learning and sequence learning develop differently at the level of both ERPs and overt responses. These findings could provide insight to the dynamic change of multiple parallel learning processes that occur during procedural memory formation.

Is procedural memory enhanced in Tourette syndrome? Evidence from a sequence learning task.

Procedural memory, which is rooted in the basal ganglia, underlies the learning and processing of numerous automatized motor and cognitive skills, including in language. Not surprisingly, disorders with basal ganglia abnormalities have been found to show impairments of procedural memory. However, brain abnormalities could also lead to atypically enhanced function. Tourette syndrome (TS) is a candidate for enhanced procedural memory, given previous findings of enhanced TS processing of grammar, which likely depends on procedural memory. We comprehensively examined procedural learning, from memory formation to retention, in children with TS and typically developing (TD) children, who performed an implicit sequence learning task over two days. The children with TS showed sequence learning advantages on both days, despite a regression of sequence knowledge overnight to the level of the TD children. This is the first demonstration of procedural learning advantages in any disorder. The findings may further our understanding of procedural memory and its enhancement. The evidence presented here, together with previous findings suggesting enhanced grammar processing in TS, underscore the dependence of language on a system that also subserves visuomotor sequencing.

Dynamics of EEG functional connectivity during statistical learning.

Statistical learning is a fundamental mechanism of the brain, which extracts and represents regularities of our environment. Statistical learning is crucial in predictive processing, and in the acquisition of perceptual, motor, cognitive, and social skills. Although previous studies have revealed competitive neurocognitive processes underlying statistical learning, the neural communication of the related brain regions (functional connectivity, FC) has not yet been investigated. The present study aimed to fill this gap by investigating FC networks that promote statistical learning in humans. Young adults (N=28) performed a statistical learning task while 128-channels EEG was acquired. The task involved probabilistic sequences, which enabled to measure incidental/implicit learning of conditional probabilities. Phase synchronization in seven frequency bands was used to quantify FC between cortical regions during the first, second, and third periods of the learning task, respectively. Here we show that statistical learning is negatively correlated with FC of the anterior brain regions in slow (theta) and fast (beta) oscillations. These negative correlations increased as the learning progressed. Our findings provide evidence that dynamic antagonist brain networks serve a hallmark of statistical learning.

Procedural learning in Tourette syndrome, ADHD, and comorbid Tourette-ADHD: Evidence from a probabilistic sequence learning task.

Procedural memory, which is rooted in the basal ganglia, plays an important role in the implicit learning of motor and cognitive skills. Few studies have examined procedural learning in either Tourette syndrome (TS) or Attention Deficit Hyperactivity Disorder (ADHD), despite basal ganglia abnormalities in both of these neurodevelopmental disorders. We aimed to assess procedural learning in children with TS (n=13), ADHD (n=22), and comorbid TS-ADHD (n=20), as well as in typically developing children (n=21). Procedural learning was measured with a well-studied implicit probabilistic sequence learning task, the alternating serial reaction time task. All four groups showed evidence of sequence learning, and moreover did not differ from each other in sequence learning. This result, from the first study to examine procedural memory across TS, ADHD and comorbid TS-ADHD, is consistent with previous findings of intact procedural learning of sequences in both TS and ADHD. In contrast, some studies have found impaired procedural learning of non-sequential probabilistic categories in TS. This suggests that sequence learning may be spared in TS and ADHD, while at least some other forms of learning in procedural memory are impaired, at least in TS. Our findings indicate that disorders associated with basal ganglia abnormalities do not necessarily show procedural learning deficits, and provide a possible path for more effective diagnostic tools, and educational and training programs.

Temporal dynamics of object location processing in allocentric reference frame.

The spatial location of objects is processed in egocentric and allocentric reference frames, the early temporal dynamics of which have remained relatively unexplored. Previous experiments focused on ERP components related only to egocentric navigation. Thus, we designed a virtual reality experiment to see whether allocentric reference frame-related ERP modulations can also be registered. Participants collected reward objects at the end of the west and east alleys of a cross maze, and their ERPs to the feedback objects were measured. Participants made turn choices from either the south or the north alley randomly in each trial. In this way, we were able to discern place and response coding of object location. Behavioral results indicated a strong preference for using the allocentric reference frame and a preference for choosing the rewarded place in the next trial, suggesting that participants developed probabilistic expectations between places and rewards. We also found that the amplitude of the P1 was sensitive to the allocentric place of the reward object, independent of its value. We did not find evidence for egocentric response learning. These results show that early ERPs are sensitive to the location of objects during navigation in an allocentric reference frame.

Statistical learning leads to persistent memory: Evidence for one-year consolidation.

Statistical learning is a robust mechanism of the brain that enables the extraction of environmental patterns, which is crucial in perceptual and cognitive domains. However, the dynamical change of processes underlying long-term statistical memory formation has not been tested in an appropriately controlled design. Here we show that a memory trace acquired by statistical learning is resistant to inference as well as to forgetting after one year. Participants performed a statistical learning task and were retested one year later without further practice. The acquired statistical knowledge was resistant to interference, since after one year, participants showed similar memory performance on the previously practiced statistical structure after being tested with a new statistical structure. These results could be key to understand the stability of long-term statistical knowledge.