Neural mechanisms underlying adaptive actions after slips

An increase in cognitive control has been systematically observed in responses produced immediately after the commission of an error. Such responses show a delay in reaction time (post-error slowing) and an increase in accuracy. To characterize the neurophysiological mechanism involved in the adaptation of cognitive control, we examined oscillatory electrical brain activity by electroencephalogram and its corresponding neural network by event-related functional magnetic resonance imaging in three experiments. We identified a new oscillatory theta-beta component related to the degree of post-error slowing in the correct responses following an erroneous trial. Additionally, we found that the activity of the right dorsolateral prefrontal cortex, the right inferior frontal cortex, and the right superior frontal cortex was correlated with the degree of caution shown in the trial following the commission of an error. Given the overlap between this brain network and the regions activated by the need to inhibit motor responses in a stop-signal manipulation, we conclude that the increase in cognitive control observed after the commission of an error is implemented through the participation of an inhibitory mechanism.     

Dissociation in performance of children with ADHD and high-functioning autism on a task of sustained attention

Attention deficit hyperactivity disorder (ADHD) and autism are two neurodevelopmental disorders associated with prominent executive dysfunction, which may be underpinned by disruption within fronto-striatal and fronto-parietal circuits. We probed executive function in these disorders using a sustained attention task with a validated brain-behaviour basis. Twenty-three children with ADHD, 21 children with high-functioning autism (HFA) and 18 control children were tested on the Sustained Attention to Response Task (SART). In a fixed sequence version of the task, children were required to withhold their response to a predictably occurring no-go target (3) in a 1-9 digit sequence; in the random version the sequence was unpredictable. The ADHD group showed clear deficits in response inhibition and sustained attention, through higher errors of commission and omission on both SART versions. The HFA group showed no sustained attention deficits, through a normal number of omission errors on both SART versions. The HFA group showed dissociation in response inhibition performance, as indexed by commission errors. On the Fixed SART, a normal number of errors was made, however when the stimuli were randomised, the HFA group made as many commission errors as the ADHD group. Greater slow-frequency variability in response time and a slowing in mean response time by the ADHD group suggested impaired arousal processes. The ADHD group showed greater fast-frequency variability in response time, indicative of impaired top-down control, relative to the HFA and control groups. These data imply involvement of fronto-parietal attentional networks and sub-cortical arousal systems in the pathology of ADHD and prefrontal cortex dysfunction in children with HFA.     

Response variability in attention deficit hyperactivity disorder: evidence for neuropsychological heterogeneity

Response time (RT) variability is a common finding in ADHD research. RT variability may reflect frontal cortex function and may be related to deficits in sustained attention. The existence of a sustained attention deficit in ADHD has been debated, largely because of inconsistent evidence of time-on-task effects. A fixed-sequence Sustained Attention to Response Task (SART) was given to 29 control, 39 unimpaired and 24 impaired-ADHD children (impairment defined by the number of commission errors). The response time data were analysed using the Fast Fourier Transform, to define the fast-frequency and slow-frequency contributions to overall response variability. The impaired-ADHD group progressively slowed in RT over the course of the 5.5min task, as reflected in this group's greater slow-frequency variability. The fast-frequency trial-to-trial variability was also significantly greater, but did not differentially worsen over the course of the task. The higher error rates of the impaired-ADHD group did not become differentially greater over the length of the task. The progressive slowing in mean RT over the course of the task may relate to a deficit in arousal in the impaired-ADHD group. The consistently poor performance in fast-frequency variability and error rates may be due to difficulties in sustained attention that fluctuate on a trial-to-trial basis.     

Deficient sustained attention to response task and P300 characteristics in early Huntington’s disease

Evidence for the extent and nature of attentional impairment in premanifest and manifest Huntington's disease (HD) is inconsistent. Understanding such impairments may help to better understand early functional changes in HD and could have consequences concerning care for HD patients. We investigated attentional control in both early and premanifest HD. We studied 17 early HD subjects (mean age: 51 years), 12 premanifest HD subjects (mean age: 43 years), and 15 healthy controls (mean age: 51 years), using the sustained attention to response task (SART), a simple Go/No-go test reflecting attentional and inhibitory processes through reaction time (RT) and error rates. Simultaneously recorded EEG yielded P300 amplitudes and latencies. The early HD group made more Go errors (p < 0.001) and reacted slower (p < 0.005) than the other groups. The RT pattern during the SART was remarkably different for early HD subjects compared to the other two groups (p < 0.005), apparent as significant post-error slowing. P300 data showed that for early HD the No-go amplitude was lower than for the other two groups (p < 0.05). Subjects with early HD showed a reduced capacity to effectively control attention. They proved unable to resume the task directly after having made an error, and need more time to return to pre-error performance levels. No attentional control deficits were found for the premanifest HD group.     

Not all errors are alike: modulation of error-related neural responses in musical joint action

During joint action, the sense of agency enables interaction partners to implement corrective and adaptive behaviour in response to performance errors. When agency becomes ambiguous (e.g. when action similarity encourages perceptual self–other overlap), confusion as to who produced what may disrupt this process. The current experiment investigated how ambiguity of agency affects behavioural and neural responses to errors in a joint action domain where self–other overlap is common: musical duos. Pairs of pianists performed piano pieces in synchrony, playing either the same pitches (ambiguous agency) or different pitches (unambiguous agency) while electroencephalography (EEG) was recorded for each individual. Behavioural and event-related potential results showed no effects of the agency manipulation but revealed differences in how distinct error types are processed. Self-produced ‘wrong note’ errors (substitutions) were left uncorrected, showed post-error slowing and elicited an error-related negativity (ERN) peaking before erroneous keystrokes (pre-ERN). In contrast, self-produced ‘extra note’ errors (additions) exhibited pre-error slowing, error and post-error speeding, were rapidly corrected and elicited the ERN. Other-produced errors evoked a feedback-related negativity but no behavioural effects. Overall findings shed light upon how the nervous system supports fluent interpersonal coordination in real-time joint action by employing distinct mechanisms to manage different types of errors.     

Intervention Effect of Repetitive TMS on Behavioral Adjustment After Error Commission in Long-Term Methamphetamine Addicts: Evidence From a Two-Choice Oddball Task

Behavioral adjustment plays an important role in the treatment and relapse of drug addiction. Nonetheless,few studies have examined behavioral adjustment and its plasticity following error commission in methamphetamine(METH) dependence, which is detrimental to human health. Thus, we investigated the behavioral adjustment performance following error commission in long-term METH addicts and how it varied with the application of repetitive transcranial magnetic stimulation(r TMS) of the left dorsolateral prefrontal cortex(DLPFC). Twenty-nine male long-term METH addicts(for [ 3 years) were randomly assigned to high-frequency(10 Hz, n = 15) or sham(n = 14) r TMS of the left DLPFC during a two-choice oddball task. Twenty-six age-matched, healthy male adults participated in the two-choice oddball task pretest to establish normal performance for comparison. The results showed that 10 Hz r TMS over the left DLPFC significantly decreased the post-error slowing effect in response times of METH addicts. In addition, the 10 Hz r TMS intervention remarkably reduced the reaction times during post-error trials but not post-correct trials. While the 10 Hz r TMS group showed a more pronounced post-error slowing effect than the healthy participants during the pretest, the posterror slowing effect in the posttest of this sample was similar to that in the healthy participants. These results suggest that high-frequency r TMS over the left DLPFC is a useful protocol for the improvement of behavioral adjustment after error commission in long-term METH addicts.     

Deficient post-error slowing in children with ADHD is limited to the inattentive subtype

Post-error slowing (i.e., slowing of a response on correct trials following an error) is thought to reflect adaptive behavior that may be impaired in Attention-Deficit/Hyperactivity Disorder (ADHD). The current study examined post-error slowing in children with ADHD and typically developing controls on two cognitive tasks. Fifty-one ADHD-Combined type, 53 ADHD-Inattentive type, and 47 controls completed a Choice Discrimination and Stop Signal Task with incentive and event rate manipulations. Linear mixed models were used to examine reaction times surrounding errors (trial-by-trial). Pre-error speeding and pre- to post-error slowing occurred on both tasks. Impaired post-error slowing was only present on the Choice Discrimination Task for the ADHD-Inattentive type. Post-error slowing is impaired in children with ADHD-Inattentive type, but not ADHD-Combined type, on a simple attention task. These findings highlight the importance of considering task demands and ADHD subtype when examining post-error slowing and also provide a novel approach to quantifying post-error slowing.     

Dissociation in response to methylphenidate on response variability in a group of medication naïve children with ADHD

Increased variability in reaction time (RT) has been proposed as a cardinal feature of attention deficit hyperactivity disorder (ADHD). Increased variability during sustained attention tasks may reflect inefficient fronto-striatal and fronto-parietal circuitry; activity within these circuits is modulated by the catecholamines. A disruption to dopamine signaling is suggested in ADHD that may be ameliorated by methylphenidate (MPH). This study investigated the effects of MPH administration on the variability in RT and error performance on a sustained attention task of a group of 31 medication naïve children with ADHD, compared with 22 non-ADHD, non-medicated, control children. All children performed the fixed-sequence sustained attention to response task (SART) at two time-points: at baseline and after six weeks. The children with ADHD were tested when medication naive at baseline and after six weeks of treatment with MPH and whilst on medication. The medication naïve children with ADHD performed the SART with greater errors of commission and omission when compared with the control group. They demonstrated greater standard deviation of RT and fast moment-to-moment variability. They did not differ significantly from the control group in terms of slow variability in RT. MPH administration resulted in reduced and normalised levels of commission errors and fast, moment-to-moment variability in RT. MPH did not affect the rate of omission errors, standard deviation of RT or slow frequency variability in RT. MPH administration may have a specific effect on those performance components that reflect sustained attention and top–down control rather than arousal.     

A neurophysiological study of the detrimental effects of alprazolam on human action monitoring

In order to adapt their behavior to different unexpected situations, humans need to be able to monitor their performance and detect and correct errors. Benzodiazepines have long been shown to impair performance in humans, but the performance-related neurophysiological processes targeted by these drugs remain largely unknown. In the present article, we assessed the impact of alprazolam administration on relevant aspects of action monitoring, i.e., the monitoring of response conflict and the detection and correction of errors by means of neurophysiological measures. Multichannel event-related brain potentials (ERPs) were recorded to assess the impact of the benzodiazepine alprazolam (0.25 mg and 1.00 mg) on action monitoring and motor preparation in a group of twelve healthy male volunteers who participated in a double-blind cross-over placebo-controlled clinical trial involving a letter flanker task. Error detection was evaluated using the error-related negativity (ERN); response conflict on correct trials was measured by means of the N2 amplitude difference between congruent and incongruent trials; motor preparation was assessed by means of the lateralized readiness potentials (LRPs); and post-error adjustments were assessed by measuring post-error slowing in reaction time. Alprazolam significantly reduced the amplitude of the ERN and the number of corrective responses and increased reaction time and LRP latencies. The drug had no effect on amplitude differences in the N2 component between congruent and incongruent trials or on post-error slowing. Thus, alprazolam was shown to affect brain correlates of error detection (ERN) and motor preparation (LRPs), while it did not disturb conflict monitoring on correct trials (N2) or post-error adjustments of behavior.     

Multiple frontal systems controlling response speed

This study evaluated a model of attention that postulates several distinct component processes, each mediated by specific neural systems in the human frontal lobes. A series of reaction time (RT) tests (simple, choice, and prepare) examined the hypothesis that different attentional processes are related to distinct regions within the frontal lobes. These tests were given to 38 patients with frontal lesions and 38 age-matched control subjects. Lesions were localized both by general regions (superior medial, inferior medial, left and right lateral) and by individual architectonic areas. Lesions in the superior medial (SM) frontal lobes, particularly involving areas 24 and 32 on the right, were associated with slow RT in all tests and with failure to decrease RT after a warning signal. Lesions in the right lateral (RL) frontal lobe, centred in area 9/46v, prevented the decrease in RT with increasing foreperiod that was seen in normal subjects and in patients with lesions elsewhere in the frontal lobes. The ability to energize a response for rapid RT, either generally or specifically following a warning stimulus, is sensitive to lesions of the right SM. Monitoring of stimulus occurrence and response behaviour in order to enhance the speed of response to upcoming stimuli is sensitive to RL lesions.     

Error processing in the adolescent brain: Age-related differences in electrophysiology,behavioral adaptation,and brain morphology

Detecting errors and adjusting behaviour appropriately are fundamental cognitive abilities that are known to improve through adolescence. The cognitive and neural processes underlying this development, however, are still poorly understood. To address this knowledge gap, we performed a thorough investigation of error processing in a Flanker task in a cross-sectional sample of participants 8 to 19 years of age (n = 98). We examined age-related differences in event-related potentials known to be associated with error processing, namely the error-related negativity (ERN) and the error positivity (Pe), as well as their relationships with task performance, post-error adjustments and regional cingulate cortex thickness and surface area. We found that ERN amplitude increased with age, while Pe amplitude remained constant. A more negative ERN was associated with higher task accuracy and faster reaction times, while a more positive Pe was associated with higher accuracy, independently of age. When estimating post-error adjustments from trials following both incongruent and congruent trials, post-error slowing and post-error improvement in accuracy both increased with age, but this was only found for post-error slowing when analysing trials following incongruent trials. There were no age-independent associations between either ERN or Pe amplitude and cingulate cortex thickness or area measures.     

Genetic marker of norepinephrine synthesis predicts individual differences in post-error slowing: A pilot study

When our brain detects the commission of an error, we slow down immediately thereafter: a phenomenon called post-error slowing (PES). Some researchers have speculated that slowing after unexpected errors or negative feedback is related to the activity of the neuromodulatory locus coeruleus–norepinephrine system. In the present pilot study, we tested whether individual differences in the size of PES are related to differences in genetic predisposition related to norepinephrine synthesis. In a sample of 100 healthy adults, we studied the dependency of an individual′s size of PES on the DBH5′-ins/del polymorphism—a variation in the DBH gene associated with the production of the enzyme dopamine β-hydroxylase, which catalyzes the conversion of dopamine to norepinephrine. DBH5′-ins/del heterozygotes, who have intermediate levels of plasma DβH activity, showed increased PES in a Simon task compared to del/del homozygotes and ins/ins homozygotes, who have low and high levels of plasma DβH activity, respectively. This outcome pattern presents preliminary evidence that the size of PES varies with DβH activity and, presumably, NE release according to an inverted U-shape: intermediate levels of DβH activity and NE release are associated with larger post-error adjustments.     

Cognitive remediation in ADHD: effects of periodic non-contingent alerts on sustained attention to response

Few studies have attempted direct cognitive remediation of attention deficits in attention-deficit hyperactivity disorder (ADHD). The present study investigated the efficacy of periodic non-informative alerting cues for improving sustaining attention in ADHD. This technique is known to improve sustained attention in right frontal injury patients and may be effective in ADHD, given that this disorder has also been linked with right frontal dysfunction. Fifteen children with ADHD and 15 matched controls completed four blocks of a modified version of the Sustained Attention to Response Task (SART). Eight random non-contingent alerts were introduced on two of these blocks as a cue for participants to adopt a more supervisory stance to their performance. While the alerting cues did not alter the total number of commission errors committed by ADHD children over a task block, they did produce a significant short-term reduction in commission errors in the period immediately following an alerting cue. Our data demonstrate that sustained attention performance can be enhanced in children with ADHD using a simple cognitive training strategy. Methods from the field of cognitive rehabilitation may be viably applied to the remediation of attention deficits in ADHD.     

Cognitive remediation in ADHD: Effects of periodic non-contingent alerts on sustained attention to response

Few studies have attempted direct cognitive remediation of attention deficits in attention-deficit hyperactivity disorder (ADHD). The present study investigated the efficacy of periodic non-informative alerting cues for improving sustaining attention in ADHD. This technique is known to improve sustained attention in right frontal injury patients and may be effective in ADHD, given that this disorder has also been linked with right frontal dysfunction. Fifteen children with ADHD and 15 matched controls completed four blocks of a modified version of the Sustained Attention to Response Task (SART). Eight random non-contingent alerts were introduced on two of these blocks as a cue for participants to adopt a more supervisory stance to their performance. While the alerting cues did not alter the total number of commission errors committed by ADHD children over a task block, they did produce a significant short-term reduction in commission errors in the period immediately following an alerting cue. Our data demonstrate that sustained attention performance can be enhanced in children with ADHD using a simple cognitive training strategy. Methods from the field of cognitive rehabilitation may be viably applied to the remediation of attention deficits in ADHD.     

Developmental changes in error monitoring: an event-related potential study

The aim of the study was to investigate the developmental trajectory of error monitoring. For this purpose, children (age 7-8), young adolescents (age 13-14) and adults (age 23-24) performed a Go/No-Go task and were compared on overt reaction time (RT) performance and on event-related potentials (ERPs), thought to reflect error detection (error-related negativity: ERN) and conscious evaluation (error positivity: Pe) of the error. RT on correct trials, variability of responding and percentage of errors decreased with age. The latencies of incorrect responses, compared to correct responses, were shorter in children and adolescents than in adults, indicative of developmental changes in impulsive response style. Groups did not differ in the ability to adjust response strategies after making an error (post-error slowing). The ERN amplitude increased with age, the Pe amplitude did not change with age. Possible explanations for the developmental changes in ERN are discussed.     

Schizophrenia patients show intact immediate error-related performance adjustments on an antisaccade task

OBJECTIVE: Schizophrenia patients consistently show impairments on tasks requiring inhibition such as the antisaccade task. Deficits in performance monitoring including the detection of errors and subsequent adjustments to performance may contribute to such impairments. We examined whether immediate error-related performance adjustments during the antisaccade task were intact in schizophrenia. METHOD: We compared 21 schizophrenia patients and 14 healthy control subjects on the following measures: 1) error-related, trial-by-trial adjustments in reaction time (pre-error speeding, faster errors and post-error slowing); 2) the speed-accuracy trade-off (SATO) function; and 3) the frequency and type of error self-correction. RESULTS: Although antisaccade performance in schizophrenia was characterized by increased errors and latency of correct responses, measures of immediate error-related performance adjustments were intact. CONCLUSION: Schizophrenia is characterized by intact immediate error-related performance adjustments, even in the context of impaired antisaccade performance. It is possible that deficiencies in other aspects of error processing, indexed by electrophysiological and hemodynamic markers, contribute to antisaccade and other cognitive deficits in schizophrenia.     

Riluzole and D-amphetamine interactions in humans

In preclinical studies, medications which decrease glutamate release have been shown to block some of the effects of psychostimulants. One such medication is riluzole, marketed for the treatment of Amyotrophic Lateral Sclerosis (ALS). The goal of this study was to determine riluzole's effects on acute physiological and subjective responses to d-amphetamine in healthy volunteers. Seven male and 5 female subjects participated in an outpatient double-blind, placebo-controlled, crossover study. Across 4 sessions, subjects were randomly assigned to a sequence of 4 oral treatments: placebo, 20 mg D-amphetamine alone, 100 mg riluzole alone, or d-amphetamine plus riluzole. Outcome measures included heart rate, blood pressure, plasma cortisol, performance on the Sustained Attention to Response Test (SART), and subjective measures. d-amphetamine increased heart rate, blood pressure and plasma cortisol levels while inducing psychostimulant-type subjective effects. On the SART, d-amphetamine enhanced the speed of correct responses but also significantly increased the number of errors of commission. Riluzole at 100 mg did not block, the typical subjective and physiological responses to 20 mg D-amphetamine. Riluzole alone induced amphetamine-like subjective responses. On the SART test, riluzole increased the number errors of commission, but unlike d-amphetamine, did not speed reaction time. The mechanism accounting for these findings is unclear, but may involve processes other than decreased glutamate release by riluzole. The effects of glutamate medications on psychostimulant responses need to be further examined.     

Reduced error monitoring in children with autism spectrum disorder: an ERP study

This study investigated self-monitoring in children with autism spectrum disorder (ASD) with event-related potentials looking at both the error-related negativity (ERN) and error-related positivity (Pe). The ERN is related to early error/conflict detection, and the Pe has been associated with conscious error evaluation or attention allocation. In addition, post-error slowing in reaction times (RTs) was measured. Children with ASD and age- and IQ- matched controls were administered an easy and a hard version of an auditory decision task. Results showed that the ERN was smaller in children with ASD but localized in the anterior cingulate cortex (ACC) in both groups. In addition we found a negativity on correct trials (CRN) that did not differ between the groups. Furthermore, a reduced Pe and a lack of post-error slowing in RTs were found in children with ASD. The reduced ERN in children with ASD, in the presence of an intact CRN, might suggest a specific insensitivity to detect situations in which the chance of making errors is enhanced. This might in turn lead to reduced error awareness/attention allocation to the erroneous event (reduced Pe) and eventually in a failure in change of strategy to deal with a situation, as becomes evident from the lack of post-error slowing in the ASD group. This relates well to the perseverative behaviour that is seen in children with ASD. We discuss these results in terms of a general deficit in self-monitoring, underlying social disturbance in ASD and the involvement of the ACC.     

Abnormal prediction error processing in schizophrenia and depression

To make adaptive decisions under uncertainty, individuals need to actively monitor the discrepancy between expected outcomes and actual outcomes, known as prediction errors. Reward‐based learning deficits have been shown in both depression and schizophrenia patients. For this study, we compiled studies that investigated prediction error processing in depression and schizophrenia patients and performed a series of meta‐analyses. In both groups, positive t‐maps of prediction error tend to yield striatum activity across studies. The analysis of negative t‐maps of prediction error revealed two large clusters within the right superior and inferior frontal lobes in schizophrenia and the medial prefrontal cortex and bilateral insula in depression. The concordant posterior cingulate activity was observed in both patient groups, more prominent in the depression group and absent in the healthy control group. These findings suggest a possible role in dopamine‐rich areas associated with the encoding of prediction errors in depression and schizophrenia.     

Measuring sustained attention after traumatic brain injury: differences in key findings from the sustained attention to response task (SART)

Clinical reports after traumatic brain injury (TBI) suggest frequent difficulties with sustained attention, but their objective measurement has proved difficult. In 1997, Robertson and colleagues reported on a new sustained attention assessment tool, the sustained attention to response task (SART). Individuals with TBI were reported to produce more errors of commission on the SART than control participants, and both groups showed a relationship between SART errors and everyday lapses of attention as measured by the cognitive failures questionnaire (CFQ). Although few direct replications of these findings have been reported, the SART has been used widely as a measure of sustained attention in TBI, in normal controls, and in various other clinical samples. As part of a program of research on attention in TBI, we administered the SART and the CFQ to a sample of 34 survivors of moderate to severe TBI and to 35 control participants. CFQ scores reported by significant others showed clear group differences in everyday lapses of attention. Despite this, group differences in SART errors of commission were small and non-significant, and the correlations between SART errors and CFQ scores were small within both groups. Further analyses excluding participants with invalid score profiles, or restricting the analysis to the first performance of the SART failed to alter the results. These findings suggest that more research is needed to establish the validity of the SART as a measure of sustained attention after TBI, and to determine under what circumstances the original findings hold.