Losses resulting from deliberate exploration trigger beta oscillations in frontal cortex.

We examined the neural signature of directed exploration by contrasting MEG beta (16-30 Hz) power changes between disadvantageous and advantageous choices in the two-choice probabilistic reward task. We analyzed the choices made after the participants have learned the probabilistic contingency between choices and their outcomes, i.e., acquired the inner model of choice values. Therefore, rare disadvantageous choices might serve explorative, environment-probing purposes. The study brought two main findings. Firstly, decision making leading to disadvantageous choices took more time and evidenced greater large-scale suppression of beta oscillations than its advantageous alternative. Additional neural resources recruited during disadvantageous decisions strongly suggest their deliberately explorative nature. Secondly, an outcome of disadvantageous and advantageous choices had qualitatively different impact on feedback-related beta oscillations. After the disadvantageous choices, only losses-but not gains-were followed by late beta synchronization in frontal cortex. Our results are consistent with the role of frontal beta oscillations in the stabilization of neural representations for selected behavioral rule when explorative strategy conflicts with value-based behavior. Punishment for explorative choice being congruent with its low value in the reward history is more likely to strengthen, through punishment-related beta oscillations, the representation of exploitative choices consistent with the inner utility model.

Learning of new associations invokes a major change in modulations of cortical beta oscillations in human adults.

Large-scale cortical beta (ß) oscillations were implicated in the learning processes, but their exact role is debated. We used MEG to explore the dynamics of movement-related ß-oscillations while 22 adults learned, through trial and error, novel associations between four auditory pseudowords and movements of four limbs. As learning proceeded, spatial-temporal characteristics of ß-oscillations accompanying cue-triggered movements underwent a major transition. Early in learning, widespread suppression of ß-power occurred long before movement initiation and sustained throughout the whole behavioral trial. When learning advanced and performance reached asymptote, ß-suppression after the initiation of correct motor response was replaced by a rise in ß-power mainly in the prefrontal and medial temporal regions of the left hemisphere. This post-decision ß-power predicted trial-by-trial response times (RT) at both stages of learning (before and after the rules become familiar), but with different signs of interaction. When a subject just started to acquire associative rules and gradually improved task performance, a decrease in RT correlated with the increase in the post-decision ß-band power. When the participants implemented the already acquired rules, faster (more confident) responses were associated with the weaker post-decision ß-band synchronization. Our findings suggest that maximal beta activity is pertinent to a distinct stage of learning and may serve to strengthen the newly learned association in a distributed memory network.

Pupil dilation and response slowing distinguish deliberate explorative choices in the probabilistic learning task.

This study examined whether pupil size and response time would distinguish directed exploration from random exploration and exploitation. Eighty-nine participants performed the two-choice probabilistic learning task while their pupil size and response time were continuously recorded. Using LMM analysis, we estimated differences in the pupil size and response time between the advantageous and disadvantageous choices as a function of learning success, i.e., whether or not a participant has learned the probabilistic contingency between choices and their outcomes. We proposed that before a true value of each choice became known to a decision-maker, both advantageous and disadvantageous choices represented a random exploration of the two options with an equally uncertain outcome, whereas the same choices after learning manifested exploitation and direct exploration strategies, respectively. We found that disadvantageous choices were associated with increases both in response time and pupil size, but only after the participants had learned the choice-reward contingencies. For the pupil size, this effect was strongly amplified for those disadvantageous choices that immediately followed gains as compared to losses in the preceding choice. Pupil size modulations were evident during the behavioral choice rather than during the pretrial baseline. These findings suggest that occasional disadvantageous choices, which violate the acquired internal utility model, represent directed exploration. This exploratory strategy shifts choice priorities in favor of information seeking and its autonomic and behavioral concomitants are mainly driven by the conflict between the behavioral plan of the intended exploratory choice and its strong alternative, which has already proven to be more rewarding.

Rapid Cortical Plasticity Induced by Active Associative Learning of Novel Words in Human Adults.

Human speech requires that new words are routinely memorized, yet neurocognitive mechanisms of such acquisition of memory remain highly debatable. Major controversy concerns the question whether cortical plasticity related to word learning occurs in neocortical speech-related areas immediately after learning, or neocortical plasticity emerges only on the second day after a prolonged time required for consolidation after learning. The functional spatiotemporal pattern of cortical activity related to such learning also remains largely unknown. In order to address these questions, we examined magnetoencephalographic responses elicited in the cerebral cortex by passive presentations of eight novel pseudowords before and immediately after an operant conditioning task. This associative procedure forced participants to perform an active search for unique meaning of four pseudowords that referred to movements of left and right hands and feet. The other four pseudowords did not require any movement and thus were not associated with any meaning. Familiarization with novel pseudowords led to a bilateral repetition suppression of cortical responses to them; the effect started before or around the uniqueness point and lasted for more than 500 ms. After learning, response amplitude to pseudowords that acquired meaning was greater compared with response amplitude to pseudowords that were not assigned meaning; the effect was significant within 144-362 ms after the uniqueness point, and it was found only in the left hemisphere. Within this time interval, a learning-related selective response initially emerged in cortical areas surrounding the Sylvian fissure: anterior superior temporal sulcus, ventral premotor cortex, the anterior part of intraparietal sulcus and insula. Later within this interval, activation additionally spread to more anterior higher-tier brain regions, and reached the left temporal pole and the triangular part of the left inferior frontal gyrus extending to its orbital part. Altogether, current findings evidence rapid plastic changes in cortical representations of meaningful auditory word-forms occurring almost immediately after learning. Additionally, our results suggest that familiarization resulting from stimulus repetition and semantic acquisition resulting from an active learning procedure have separable effects on cortical activity.

Enhanced Theta-Band Coherence Between Midfrontal and Posterior Parietal Areas Reflects Post-feedback Adjustments in the State of Outcome Uncertainty.

Medial frontal cortex is currently viewed as the main hub of the performance monitoring system; upon detection of an error committed, it establishes functional connections with brain regions involved in task performance, thus leading to neural adjustments in them. Previous research has identified targets of such adjustments in the dorsolateral prefrontal cortex, posterior cortical regions, motor cortical areas, and subthalamic nucleus. Yet most of such studies involved visual tasks with relatively moderate cognitive load and strong dependence on motor inhibition - thus highlighting sensory, executive and motor effects while underestimating sensorimotor transformation and related aspects of decision making. Currently there is ample evidence that posterior parietal cortical areas are involved in task-specific neural processes of decision making (including evidence accumulation, sensorimotor transformation, attention, etc.) - yet, to our knowledge, no EEG studies have demonstrated post-error increase in functional connectivity in the theta-band between midfrontal and posterior parietal areas during performance on non-visual tasks. In the present study, we recorded EEG while subjects were performing an auditory version of the cognitively demanding attentional condensation task; this task involves rather non-straightforward stimulus-to-response mapping rules, thus, creating increased load on sensorimotor transformation. We observed strong pre-response alpha-band suppression in the left parietal area, which presumably reflected involvement of the posterior parietal cortex in task-specific decision-making processes. Negative feedback was followed by increased midfrontal theta-band power and increased functional coupling in the theta band between midfrontal and left parietal regions. This could be interpreted as activation of the performance monitoring system and top-down influence of this system on the posterior parietal regions involved in decision making, respectively. This inter-site coupling related to negative feedback was stronger for subjects who tended to commit errors with slower response times. Generally, current findings support the idea that slower errors are related to the state of outcome uncertainty caused by failures of task-specific processes, associated with posterior parietal regions.

Feature binding in auditory modality requires attention as indexed by mismatch negativity and N2b in an active discrimination task.

Currently, there are two opposing views on feature binding in the auditory modality: according to behavioral studies, this process requires focused attention, whereas electrophysiological studies suggest that feature binding may be fully automatic and independent of attention. Here, we examined whether feature binding depends on higher-level attentional processes by manipulating the attentional focus. We used four auditory stimuli that differed in two features: pitch and location. Two rare deviants could be detected within a sequence of two frequent standards exclusively by feature conjunctions rather than by any single feature alone. Event-related potentials to auditory stimuli were analyzed for four conditions: selective attention to target auditory deviants, selective ignoring of nontarget auditory deviants, nonselective distributed attention to all stimuli within auditory modality, and selective attention diverted from auditory to visual modality. The negative difference (Nd) between event-related potentials to deviants and standards was measured within two time intervals, corresponding to mismatch negativity (100-200 ms) and N2b (200-300 ms). Only under the condition of selective attention to specific feature conjunctions, prominent Nd was observed in mismatch negativity as well in N2b time ranges, whereas no significant Nd was observed in other conditions. As Nd is considered a marker of deviance processing, our results support the view that deviance was not detected unless attention was focused on the stimuli, thus supporting the view that feature binding requires attention.

Slow and Fast Responses: Two Mechanisms of Trial Outcome Processing Revealed by EEG Oscillations.

Cognitive control includes maintenance of task-specific processes related to attention, and non-specific regulation of motor threshold. Depending upon the nature of the behavioral tasks, these mechanisms may predispose to different kinds of errors, with either increased or decreased response time (RT) of erroneous responses relative to correct responses. Specifically, slow responses are related to attentional lapses and decision uncertainty, these conditions tending to delay RTs of both erroneous and correct responses. Here we studied if RT may be a valid approximation distinguishing trials with high and low levels of sustained attention and decision uncertainty. We analyzed response-related and feedback-related modulations in theta, alpha and beta band activity in the auditory version of the two-choice condensation task, which is highly demanding for sustained attention while involves no inhibition of prepotent responses. Depending upon response speed and accuracy, trials were divided into slow correct, slow erroneous, fast correct and fast erroneous. We found that error-related frontal midline theta (FMT) was present only on fast erroneous trials. The feedback-related FMT was equally strong on slow erroneous and fast erroneous trials. Late post-response posterior alpha suppression was stronger on erroneous slow trials. Feedback-related frontal beta was present only on slow correct trials. The data obtained cumulatively suggests that RT allows distinguishing the two types of trials, with fast trials related to higher levels of attention and low uncertainty, and slow trials related to lower levels of attention and higher uncertainty.

Early suppression effect in human primary visual cortex during Kanizsa illusion processing: A magnetoencephalographic evidence.

Detection of illusory contours (ICs) such as Kanizsa figures is known to depend primarily upon the lateral occipital complex. Yet there is no universal agreement on the role of the primary visual cortex in this process; some existing evidence hints that an early stage of the visual response in V1 may involve relative suppression to Kanizsa figures compared with controls. Iso-oriented luminance borders, which are responsible for Kanizsa illusion, may evoke surround suppression in V1 and adjacent areas leading to the reduction in the initial response to Kanizsa figures. We attempted to test the existence, as well as to find localization and timing of the early suppression effect produced by Kanizsa figures in adult nonclinical human participants. We used two sizes of visual stimuli (4.5 and 9.0°) in order to probe the effect at two different levels of eccentricity; the stimuli were presented centrally in passive viewing conditions. We recorded magnetoencephalogram, which is more sensitive than electroencephalogram to activity originating from V1 and V2 areas. We restricted our analysis to the medial occipital area and the occipital pole, and to a 40-120 ms time window after the stimulus onset. By applying threshold-free cluster enhancement technique in combination with permutation statistics, we were able to detect the inverted IC effect-a relative suppression of the response to the Kanizsa figures compared with the control stimuli. The current finding is highly compatible with the explanation involving surround suppression evoked by iso-oriented collinear borders. The effect may be related to the principle of sparse coding, according to which V1 suppresses representations of inner parts of collinear assemblies as being informationally redundant. Such a mechanism is likely to be an important preliminary step preceding object contour detection.

Distributed feature binding in the auditory modality: experimental evidence toward reconciliation of opposing views on the basis of mismatch negativity and behavioral measures.

Current understanding of feature binding remains controversial. Studies involving mismatch negativity (MMN) measurement show a low level of binding, whereas behavioral experiments suggest a higher level. We examined the possibility that the two levels of feature binding coexist and may be shown within one experiment. The electroencephalogram was recorded while participants were engaged in an auditory two-alternative choice task, which was a combination of the oddball and the condensation tasks. Two types of deviant target stimuli were used - complex stimuli, which required feature conjunction to be identified, and simple stimuli, which differed from standard stimuli in a single feature. Two behavioral outcomes - correct responses and errors - were analyzed separately. Responses to complex stimuli were slower and less accurate than responses to simple stimuli. MMN was prominent and its amplitude was similar for both simple and complex stimuli, whereas the respective stimuli differed from standards in a single feature or two features respectively. Errors in response only to complex stimuli were associated with decreased MMN amplitude. P300 amplitude was greater for complex stimuli than for simple stimuli. Our data are compatible with the explanation that feature binding in auditory modality depends on two concurrent levels of processing. We speculate that the earlier level related to MMN generation is an essential and critical stage. Yet, a later analysis is also carried out, affecting P300 amplitude and response time. The current findings provide resolution to conflicting views on the nature of feature binding and show that feature binding is a distributed multilevel process.

Theta and Alpha Band Modulations Reflect Error-Related Adjustments in the Auditory Condensation Task.

Error commission leads to adaptive adjustments in a number of brain networks that subserve goal-directed behavior, resulting in either enhanced stimulus processing or increased motor threshold depending on the nature of errors committed. Here, we studied these adjustments by analyzing post-error modulations of alpha and theta band activity in the auditory version of the two-choice condensation task, which is highly demanding for sustained attention while involves no inhibition of prepotent responses. Errors were followed by increased frontal midline theta (FMT) activity, as well as by enhanced alpha band suppression in the parietal and the left central regions; parietal alpha suppression correlated with the task performance, left central alpha suppression correlated with the post-error slowing, and FMT increase correlated with both behavioral measures. On post-error correct trials, left-central alpha band suppression started earlier before the response, and the response was followed by weaker FMT activity, as well as by enhanced alpha band suppression distributed over the entire scalp. These findings indicate that several separate neuronal networks are involved in post-error adjustments, including the midfrontal performance monitoring network, the parietal attentional network, and the sensorimotor network. Supposedly, activity within these networks is rapidly modulated after errors, resulting in optimization of their functional state on the subsequent trials, with corresponding changes in behavioral measures.

Temperament: an event-related potential study using the oddball paradigm

The present study examined the structure of interrelations between brain event-related potentials and behavioral measures and temperament dimensions during an attention task. Three temperament questionnaires were used: Eysenck Personality Inventory, Strelau Temperament Inventory, and Rusalov Structure of Temperament Questionnaire. Event-related potentials were recorded using the active auditory oddball paradigm. The stimuli (85 dB; 1050 and 1000 Hz sinusoidal tones as targets and non-targets, respectively) were easily discriminated by all of the participants. A complex framework of interrelations between temperament and personality dimensions, behavioral measures, and event-related potentials was found. P3 amplitude was negatively correlated with the number of response omissions. Emotionality was positively correlated with P2 and N1-P2 complex amplitudes. Extraversion and Mobility of Nervous Processes were negatively correlated with the amplitude of the N1-P2 complex, and Social Ergonicity was negatively correlated with N2 latency. The results indicate that Extraversion tends to be associated with both the intensity and temporal aspects of temperament and suggest the importance of using a multidimensional approach in temperament studies...

Temperament: an event-related potential study using the oddball paradigm

The present study examined the structure of interrelations between brain event-related potentials and behavioral measures and temperament dimensions during an attention task. Three temperament questionnaires were used: Eysenck Personality Inventory, Strelau Temperament Inventory, and Rusalov Structure of Temperament Questionnaire. Event-related potentials were recorded using the active auditory oddball paradigm. The stimuli (85 dB; 1050 and 1000 Hz sinusoidal tones as targets and non-targets, respectively) were easily discriminated by all of the participants. A complex framework of interrelations between temperament and personality dimensions, behavioral measures, and event-related potentials was found. P3 amplitude was negatively correlated with the number of response omissions. Emotionality was positively correlated with P2 and N1-P2 complex amplitudes. Extraversion and Mobility of Nervous Processes were negatively correlated with the amplitude of the N1-P2 complex, and Social Ergonicity was negatively correlated with N2 latency. The results indicate that Extraversion tends to be associated with both the intensity and temporal aspects of temperament and suggest the importance of using a multidimensional approach in temperament studies.(AU)